Grzimek animal life encyclopedia volume 12 mammals i

Grzimek’sAnimal Life Encyclopedia

Second Edition

● ● ● ●

Volume 12 title pages 10/27/03 1:35 PM Page 1

Grzimek’sAnimal Life Encyclopedia

Second Edition

● ● ● ●

Volume 12Mammals I

Devra G. Kleiman, Advisory EditorValerius Geist, Advisory Editor

Melissa C. McDade, Project Editor

Joseph E. Trumpey, Chief Scientific Illustrator

Michael Hutchins, Series EditorI n a s s o c i a t i o n w i t h t h e A m e r i c a n Z o o a n d A q u a r i u m A s s o c i a t i o n

Volume 12 title pages 10/27/03 1:35 PM Page 3

Grzimek’s Animal Life Encyclopedia, Second EditionVolume 12: Mammals I

Project EditorMelissa C. McDade

EditorialStacey Blachford, Deirdre S. Blanchfield, Madeline Harris, Christine Jeryan, KateKretschmann, Mark Springer, Ryan Thomason

Indexing ServicesSynapse, the Knowledge Link Corporation

PermissionsMargaret Chamberlain

Imaging and MultimediaRandy Bassett, Mary K. Grimes, Lezlie Light,Christine O’Bryan, Barbara Yarrow, Robyn V.Young

Product DesignTracey Rowens, Jennifer Wahi

ManufacturingWendy Blurton, Dorothy Maki, Evi Seoud, MaryBeth Trimper

© 2004 by Gale. Gale is an imprint of TheGale Group, Inc., a division of ThomsonLearning Inc.

Gale and Design® and Thomson Learning™are trademarks used herein under license.

For more information contactThe Gale Group, Inc.27500 Drake Rd.Farmington Hills, MI 48331-3535Or you can visit our Internet site athttp://www.gale.com

ALL RIGHTS RESERVEDNo part of this work covered by the copy-right hereon may be reproduced or used inany form or by any means—graphic, elec-tronic, or mechanical, including photocopy-ing, recording, taping, Web distribution, orinformation storage retrieval systems—with-out the written permission of the publisher.

For permission to use material from thisproduct, submit your request via Web athttp://www.gale-edit.com/permissions, or youmay download our Permissions Request formand submit your request by fax or mail to:The Gale Group, Inc., Permissions Depart-ment, 27500 Drake Road, Farmington Hills,MI, 48331-3535, Permissions hotline: 248-699-8074 or 800-877-4253, ext. 8006, Fax: 248-699-8074 or 800-762-4058.

Cover photo of numbat (Myrmecobius fasciatus) by Frans Lanting/Minden Pictures.Back cover photos of sea anemone byAP/Wide World Photos/University of Wisconsin-Superior; land snail, lionfish, golden frog, andgreen python by JLM Visuals; red-legged lo-cust © 2001 Susan Sam; hornbill by MargaretF. Kinnaird; and tiger by Jeff Lepore/Photo Re-searchers. All reproduced by permission.

While every effort has been made to en-sure the reliability of the information presented

in this publication, The Gale Group, Inc. doesnot guarantee the accuracy of the data con-tained herein. The Gale Group, Inc. accepts nopayment for listing; and inclusion in the publi-cation of any organization, agency, institution,publication, service, or individual does not im-ply endorsement of the editors and publisher.Errors brought to the attention of the pub-lisher and verified to the satisfaction of thepublisher will be corrected in future editions.ISBN 0-7876-5362-4 (vols. 1–17 set)

0-7876-6573-8 (vols. 12–16 set)0-7876-5788-3 (vol. 12)0-7876-5789-1 (vol. 13)0-7876-5790-5 (vol. 14)0-7876-5791-3 (vol. 15)0-7876-5792-1 (vol. 16)

This title is also available as an e-book.ISBN 0-7876-7750-7 (17-vol set)Contact your Gale sales representative for or-dering information.

Recommended citation: Grzimek’s Animal Life Encyclopedia, 2nd edition. Volumes 12–16, Mammals I–V, edited by MichaelHutchins, Devra G. Kleiman, Valerius Geist, and Melissa C. McDade. Farmington Hills, MI: Gale Group, 2003.

LIBRARY OF CONGRESS CATALOGING-IN-PUBLICATION DATA

Grzimek, Bernhard.[Tierleben. English]Grzimek’s animal life encyclopedia.— 2nd ed.

v. cm.Includes bibliographical references.Contents: v. 1. Lower metazoans and lesser deuterosomes / Neil Schlager,editor — v. 2. Protostomes / Neil Schlager, editor — v. 3. Insects /Neil Schlager, editor — v. 4-5. Fishes I-II / Neil Schlager, editor —v. 6. Amphibians / Neil Schlager, editor — v. 7. Reptiles / NeilSchlager, editor — v. 8-11. Birds I-IV / Donna Olendorf, editor — v.12-16. Mammals I-V / Melissa C. McDade, editor — v. 17. Cumulative index /Melissa C. McDade, editor.ISBN 0-7876-5362-4 (set hardcover : alk. paper)

1. Zoology—Encyclopedias. I. Title: Animal life encyclopedia. II.Schlager, Neil, 1966- III. Olendorf, Donna IV. McDade, Melissa C. V. American Zooand Aquarium Association. VI. Title.QL7 .G7813 2004

590’.3—dc212002003351

Printed in Canada10 9 8 7 6 5 4 3 2 1

Foreword ............................................................................ ixHow to use this book ........................................................ xiiAdvisory boards.................................................................. xivContributing writers .......................................................... xviContributing illustrators.................................................... xx

Volume 12: Mammals IWhat is a mammal? ........................................................... 3Ice Age giants..................................................................... 17Contributions of molecular genetics to phylogenetics...................................................................... 26Structure and function....................................................... 36Adaptations for flight......................................................... 52Adaptations for aquatic life ............................................... 62Adaptations for subterranean life ...................................... 69Sensory systems, including echolocation.......................... 79Life history and reproduction ........................................... 89Reproductive processes...................................................... 101Ecology............................................................................... 113Nutritional adaptations...................................................... 120Distribution and biogeography ......................................... 129Behavior.............................................................................. 140Cognition and intelligence ................................................ 149Migration............................................................................ 164Mammals and humans: Domestication and commensals ........................................................................ 171Mammals and humans: Mammalian invasives and pests .................................................................................... 182Mammals and humans: Field techniques for studying mammals............................................................................. 194Mammals and humans: Mammals in zoos........................ 203Conservation ...................................................................... 213

Order MONOTREMATAMonotremes ....................................................................... 227

Family: Echidnas......................................................... 235Family: Duck-billed platypus ..................................... 243

Order DIDELPHIMORPHIANew World opossums

Family: New World opossums................................... 249

Order PAUCITUBERCULATAShrew opossums

Family: Shrew opossums ............................................ 267

Order MICROBIOTHERIAMonitos del monte

Family: Monitos del monte ........................................ 273

Order DASYUROMORPHIAAustralasian carnivorous marsupials.................................. 277

Family: Marsupial mice and cats, Tasmanian devil.............................................................................. 287Family: Numbat .......................................................... 303Family: Tasmanian wolves ......................................... 307

For further reading ............................................................ 311Organizations ..................................................................... 316Contributors to the first edition ....................................... 318Glossary .............................................................................. 325Mammals species list ......................................................... 330Geologic time scale............................................................ 364Index ................................................................................... 365

Volume 13: Mammals IIOrder PERAMELEMORPHIABandicoots and bilbies ....................................................... 1

Family: Bandicoots...................................................... 9Subfamily: Bilbies........................................................ 19

Order NOTORYCTEMORPHIAMarsupial moles

Family: Marsupial moles............................................. 25

Order DIPROTODONTIAKoala, wombats, possums, wallabies, and kangaroos ....... 31

Family: Koalas............................................................. 43Family: Wombats........................................................ 51Family: Possums and cuscuses.................................... 57Family: Musky rat-kangaroos ..................................... 69Family: Rat-kangaroos ................................................ 73Family: Wallabies and kangaroos............................... 83Family: Pygmy possums ............................................. 105Family: Ringtail and greater gliding possums ........... 113Family: Gliding and striped possums ........................ 125

Grzimek’s Animal Life Encyclopedia v

• • • • •

Contents

Family: Honey possums.............................................. 135Family: Feather-tailed possums.................................. 139

Order XENARTHRASloths, anteaters, and armadillos....................................... 147

Family: West Indian sloths and two-toed tree sloths............................................................................ 155Family: Three-toed tree sloths................................... 161Family: Anteaters ........................................................ 171Family: Armadillos ...................................................... 181

Order INSECTIVORAInsectivores......................................................................... 193

Family: Gymnures and hedgehogs............................. 203Family: Golden moles................................................. 215Family: Tenrecs .......................................................... 225Family: Solenodons..................................................... 237Family: Extinct West Indian shrews.......................... 243Family: ShrewsI: Red-toothed shrews............................................. 247II: White-toothed shrews......................................... 265Family: Moles, shrew moles, and desmans................ 279

Order SCANDENTIATree shrews

Family: Tree shrews ................................................... 289

Order DERMOPTERAColugos

Family: Colugos .......................................................... 299

Order CHIROPTERABats ..................................................................................... 307

Family: Old World fruit batsI: Pteropus................................................................. 319II: All other genera................................................... 333Family: Mouse-tailed bats .......................................... 351Family: Sac-winged bats, sheath-tailed bats, and ghost bats ............................................................. 355Family: Kitti’s hog-nosed bats ................................... 367Family: Slit-faced bats ................................................ 371Family: False vampire bats ......................................... 379Family: Horseshoe bats .............................................. 387Family: Old World leaf-nosed bats ........................... 401Family: American leaf-nosed bats .............................. 413Family: Moustached bats ............................................ 435Family: Bulldog bats ................................................... 443Family: New Zealand short-tailed bats...................... 453Family: Funnel-eared bats .......................................... 459Family: Smoky bats..................................................... 467Family: Disk-winged bats ........................................... 473Family: Old World sucker-footed bats...................... 479Family: Free-tailed bats and mastiff bats................... 483Family: Vespertilionid batsI: Vespertilioninae................................................... 497II: Other subfamilies ................................................ 519

For further reading ............................................................ 527Organizations ..................................................................... 532Contributors to the first edition ....................................... 534

Glossary.............................................................................. 541Mammals species list ......................................................... 546Geologic time scale............................................................ 580Index ................................................................................... 581

Volume 14: Mammals IIIOrder PRIMATESPrimates.............................................................................. 1

Family: Lorises and pottos ......................................... 13Family: Bushbabies ..................................................... 23Family: Dwarf lemurs and mouse lemurs.................. 35Family: Lemurs ........................................................... 47Family: Avahis, sifakas, and indris.............................. 63Family: Sportive lemurs.............................................. 73Family: Aye-ayes ......................................................... 85Family: Tarsiers .......................................................... 91Family: New World monkeysI: Squirrel monkeys and capuchins ........................ 101II: Marmosets, tamarins, and Goeldi’s monkey...... 115Family: Night monkeys .............................................. 135Family: Sakis, titis, and uakaris .................................. 143Family: Howler monkeys and spider monkeys ......... 155Family: Old World monkeysI: Colobinae............................................................. 171II: Cercopithecinae................................................... 187Family: Gibbons.......................................................... 207Family: Great apes and humansI: Great apes............................................................ 225II: Humans................................................................ 241

Order CARNIVORALand and marine carnivores.............................................. 255

Family: Dogs, wolves, coyotes, jackals, and foxes ............................................................................. 265Dogs and cats.............................................................. 287Family: Bears............................................................... 295Family: Raccoons and relatives .................................. 309Family: Weasels, badgers, skunks, and otters ........... 319Family: Civets, genets, and linsangs .......................... 335Family: Mongooses and fossa..................................... 347Family: Aardwolf and hyenas ..................................... 359Family: Cats ................................................................ 369Family: Eared seals, fur seals, and sea lions .............. 393Family: Walruses......................................................... 409Family: True seals....................................................... 417

For further reading ............................................................ 437Organizations ..................................................................... 442Contributors to the first edition ....................................... 444Glossary.............................................................................. 451Mammals species list ......................................................... 456Geologic time scale............................................................ 490Index ................................................................................... 491

Volume 15: Mammals IVOrder CETACEAWhales, dolphins, and porpoises....................................... 1

Family: Ganges and Indus dolphins........................... 13

vi Grzimek’s Animal Life Encyclopedia

Contents

Family: Baijis ............................................................... 19Family: Franciscana dolphins ..................................... 23Family: Botos .............................................................. 27Family: Porpoises ........................................................ 33Family: Dolphins......................................................... 41Family: Beaked whales...................................................59Family: Sperm whales ................................................. 73Family: Belugas and narwhals .................................... 81Family: Gray whales ................................................... 93Family: Pygmy right whales ....................................... 103Family: Right whales and bowhead whales ............... 107Family: Rorquals ......................................................... 119

The ungulates .................................................................... 131Ungulate domestication..................................................... 145

Order TUBULIDENTATAAardvarks

Family: Aardvarks........................................................ 155

Order PROBOSCIDEAElephants

Family: Elephants ....................................................... 161

Order HYRACOIDEAHyraxes

Family: Hyraxes .......................................................... 177

Order SIRENIADugongs, sea cows, and manatees .................................... 191

Family: Dugongs and sea cows .................................. 199Family: Manatees ........................................................ 205

Order PERISSODACTYLAOdd-toed ungulates ........................................................... 215

Family: Horses, zebras, and asses .............................. 225Family: Tapirs ............................................................. 237Family: Rhinoceroses.................................................. 249

Order ARTIODACTYLAEven-toed ungulates .......................................................... 263

Family: Pigs................................................................. 275Family: Peccaries......................................................... 291Family: Hippopotamuses ............................................ 301Family: Camels, guanacos, llamas, alpacas, and vicuñas ......................................................................... 313Family: Chevrotains .................................................... 325Family: Deer

Subfamily: Musk deer ............................................ 335Subfamily: Muntjacs............................................... 343Subfamily: Old World deer................................... 357Subfamily: Chinese water deer.............................. 373Subfamily: New World deer ................................. 379

Family: Okapis and giraffes ........................................ 399Family: Pronghorn...................................................... 411

For further reading ............................................................ 419Organizations ..................................................................... 424Contributors to the first edition ....................................... 426Glossary.............................................................................. 433Mammals species list ......................................................... 438

Geologic time scale............................................................ 472Index ................................................................................... 473

Volume 16: Mammals VFamily: Antelopes, cattle, bison, buffaloes, goats, and sheep..................................................................... 1I: Kudus, buffaloes, and bison................................ 11II: Hartebeests, wildebeests, gemsboks, oryx, and reedbucks.............................................................. 27III: Gazelles, springboks, and saiga antelopes.......... 45IV: Dikdiks, beiras, grysboks, and steenboks ........... 59V: Duikers................................................................. 73VI: Sheep, goats, and relatives .................................. 87

Order PHOLIDOTAPangolins

Family: Pangolins........................................................ 107

Order RODENTIARodents .............................................................................. 121

Family: Mountain beavers .......................................... 131Family: Squirrels and relativesI: Flying squirrels .................................................... 135II: Ground squirrels ................................................. 143III: Tree squirrels ...................................................... 163Family: Beavers ........................................................... 177Family: Pocket gophers .............................................. 185Family: Pocket mice, kangaroo rats, and kangaroo mice.............................................................................. 199Family: Birch mice, jumping mice, and jerboas........ 211Family: Rats, mice, and relativesI: Voles and lemmings ............................................ 225II: Hamsters.............................................................. 239III: Old World rats and mice.................................... 249IV: South American rats and mice ........................... 263V: All others ............................................................. 281Family: Scaly-tailed squirrels...................................... 299Family: Springhares .................................................... 307Family: Gundis ............................................................ 311Family: Dormice ......................................................... 317Family: Dassie rats ...................................................... 329Family: Cane rats ........................................................ 333Family: African mole-rats ........................................... 339Family: Old World porcupines .................................. 351Family: New World porcupines................................. 365Family: Viscachas and chinchillas .............................. 377Family: Pacaranas ........................................................ 385Family: Cavies and maras ........................................... 389Family: Capybaras ....................................................... 401Family: Agoutis............................................................ 407Family: Pacas ............................................................... 417Family: Tuco-tucos ..................................................... 425Family: Octodonts....................................................... 433Family: Chinchilla rats................................................ 443Family: Spiny rats........................................................ 449Family: Hutias ............................................................. 461Family: Giant hutias.................................................... 469Family: Coypus ........................................................... 473

Grzimek’s Animal Life Encyclopedia vii

Contents

Order LAGOMORPHAPikas, rabbits, and hares .................................................... 479

Family: Pikas ............................................................... 491Family: Hares and rabbits .......................................... 505

Order MACROSCELIDEASengis

Family: Sengis ............................................................. 517

For further reading ............................................................ 533Organizations ..................................................................... 538Contributors to the first edition ....................................... 540Glossary .............................................................................. 547Mammals species list ......................................................... 552Geologic time scale............................................................ 586Index ................................................................................... 587

viii Grzimek’s Animal Life Encyclopedia

Contents

Earth is teeming with life. No one knows exactly how manydistinct organisms inhabit our planet, but more than 5 mil-lion different species of animals and plants could exist, rang-ing from microscopic algae and bacteria to gigantic elephants,redwood trees and blue whales. Yet, throughout this won-derful tapestry of living creatures, there runs a single thread:Deoxyribonucleic acid or DNA. The existence of DNA, anelegant, twisted organic molecule that is the building blockof all life, is perhaps the best evidence that all living organ-isms on this planet share a common ancestry. Our ancientconnection to the living world may drive our curiosity, andperhaps also explain our seemingly insatiable desire for in-formation about animals and nature. Noted zoologist, E. O.Wilson, recently coined the term “biophilia” to describe thisphenomenon. The term is derived from the Greek bios mean-ing “life” and philos meaning “love.” Wilson argues that weare human because of our innate affinity to and interest in theother organisms with which we share our planet. They are,as he says, “the matrix in which the human mind originatedand is permanently rooted.” To put it simply and metaphor-ically, our love for nature flows in our blood and is deeply en-grained in both our psyche and cultural traditions.

Our own personal awakenings to the natural world are asdiverse as humanity itself. I spent my early childhood in ruralIowa where nature was an integral part of my life. My fatherand I spent many hours collecting, identifying and studyinglocal insects, amphibians and reptiles. These experiences hada significant impact on my early intellectual and even spiri-tual development. One event I can recall most vividly. I hadcollected a cocoon in a field near my home in early spring.The large, silky capsule was attached to a stick. I brought thecocoon back to my room and placed it in a jar on top of mydresser. I remember waking one morning and, there, perchedon the tip of the stick was a large moth, slowly moving itsdelicate, light green wings in the early morning sunlight. Ittook my breath away. To my inexperienced eyes, it was oneof the most beautiful things I had ever seen. I knew it was amoth, but did not know which species. Upon closer exami-nation, I noticed two moon-like markings on the wings andalso noted that the wings had long “tails”, much like the ubiq-uitous tiger swallow-tail butterflies that visited the lilac bushin our backyard. Not wanting to suffer my ignorance anylonger, I reached immediately for my Golden Guide to North

American Insects and searched through the section on mothsand butterflies. It was a luna moth! My heart was poundingwith the excitement of new knowledge as I ran to share thediscovery with my parents.

I consider myself very fortunate to have made a living asa professional biologist and conservationist for the past 20years. I’ve traveled to over 30 countries and six continents tostudy and photograph wildlife or to attend related conferencesand meetings. Yet, each time I encounter a new and unusualanimal or habitat my heart still races with the same excite-ment of my youth. If this is biophilia, then I certainly possessit, and it is my hope that others will experience it too. I amtherefore extremely proud to have served as the series editorfor the Gale Group’s rewrite of Grzimek’s Animal Life Ency-clopedia, one of the best known and widely used referenceworks on the animal world. Grzimek’s is a celebration of an-imals, a snapshot of our current knowledge of the Earth’s in-credible range of biological diversity. Although many otheranimal encyclopedias exist, Grzimek’s Animal Life Encyclopediaremains unparalleled in its size and in the breadth of topicsand organisms it covers.

The revision of these volumes could not come at a moreopportune time. In fact, there is a desperate need for a deeperunderstanding and appreciation of our natural world. Manyspecies are classified as threatened or endangered, and the sit-uation is expected to get much worse before it gets better.Species extinction has always been part of the evolutionaryhistory of life; some organisms adapt to changing circum-stances and some do not. However, the current rate of speciesloss is now estimated to be 1,000–10,000 times the normal“background” rate of extinction since life began on Earthsome 4 billion years ago. The primary factor responsible forthis decline in biological diversity is the exponential growthof human populations, combined with peoples’ unsustainableappetite for natural resources, such as land, water, minerals,oil, and timber. The world’s human population now exceeds6 billion, and even though the average birth rate has begunto decline, most demographers believe that the global humanpopulation will reach 8–10 billion in the next 50 years. Muchof this projected growth will occur in developing countries inCentral and South America, Asia and Africa—regions that arerich in unique biological diversity.

Grzimek’s Animal Life Encyclopedia ix

• • • • •

Foreword

Finding solutions to conservation challenges will not beeasy in today’s human-dominated world. A growing numberof people live in urban settings and are becoming increasinglyisolated from nature. They “hunt” in supermarkets and malls,live in apartments and houses, spend their time watching tele-vision and searching the World Wide Web. Children andadults must be taught to value biological diversity and thehabitats that support it. Education is of prime importance nowwhile we still have time to respond to the impending crisis.There still exist in many parts of the world large numbers ofbiological “hotspots”—places that are relatively unaffected byhumans and which still contain a rich store of their originalanimal and plant life. These living repositories, along with se-lected populations of animals and plants held in profession-ally managed zoos, aquariums and botanical gardens, couldprovide the basis for restoring the planet’s biological wealthand ecological health. This encyclopedia and the collectiveknowledge it represents can assist in educating people aboutanimals and their ecological and cultural significance. Perhapsit will also assist others in making deeper connections to na-ture and spreading biophilia. Information on the conserva-tion status, threats and efforts to preserve various species havebeen integrated into this revision. We have also included in-formation on the cultural significance of animals, includingtheir roles in art and religion.

It was over 30 years ago that Dr. Bernhard Grzimek, thendirector of the Frankfurt Zoo in Frankfurt, Germany, editedthe first edition of Grzimek’s Animal Life Encyclopedia. Dr. Grz-imek was among the world’s best known zoo directors andconservationists. He was a prolific author, publishing ninebooks. Among his contributions were: Serengeti Shall Not Die,Rhinos Belong to Everybody and He and I and the Elephants. Dr.Grzimek’s career was remarkable. He was one of the firstmodern zoo or aquarium directors to understand the impor-tance of zoo involvement in in situ conservation, that is, oftheir role in preserving wildlife in nature. During his tenure,Frankfurt Zoo became one of the leading western advocatesand supporters of wildlife conservation in East Africa. Dr.Grzimek served as a Trustee of the National Parks Board ofUganda and Tanzania and assisted in the development of sev-eral protected areas. The film he made with his son Michael,Serengeti Shall Not Die, won the 1959 Oscar for best docu-mentary.

Professor Grzimek has recently been criticized by somefor his failure to consider the human element in wildlife con-servation. He once wrote: “A national park must remain a pri-mordial wilderness to be effective. No men, not even nativeones, should live inside its borders.” Such ideas, although con-sidered politically incorrect by many, may in retrospect actu-ally prove to be true. Human populations throughout Africacontinue to grow exponentially, forcing wildlife into small is-lands of natural habitat surrounded by a sea of humanity. Theillegal commercial bushmeat trade—the hunting of endan-gered wild animals for large scale human consumption—ispushing many species, including our closest relatives, the go-rillas, bonobos and chimpanzees, to the brink of extinction.The trade is driven by widespread poverty and lack of eco-nomic alternatives. In order for some species to survive it willbe necessary, as Grzimek suggested, to establish and enforce

a system of protected areas where wildlife can roam free fromexploitation of any kind.

While it is clear that modern conservation must take theneeds of both wildlife and people into consideration, what willthe quality of human life be if the collective impact of short-term economic decisions is allowed to drive wildlife popula-tions into irreversible extinction? Many rural populationsliving in areas of high biodiversity are dependent on wild an-imals as their major source of protein. In addition, wildlifetourism is the primary source of foreign currency in many de-veloping countries and is critical to their financial and socialstability. When this source of protein and income is gone,what will become of the local people? The loss of species isnot only a conservation disaster; it also has the potential tobe a human tragedy of immense proportions. Protected ar-eas, such as national parks, and regulated hunting in areas out-side of parks are the only solutions. What critics do not realizeis that the fate of wildlife and people in developing countriesis closely intertwined. Forests and savannas emptied of wildlifewill result in hungry, desperate people, and will, in the long-term lead to extreme poverty and social instability. Dr. Grz-imek’s early contributions to conservation should berecognized, not only as benefiting wildlife, but as benefitinglocal people as well.

Dr. Grzimek’s hope in publishing his Animal Life Encyclo-pedia was that it would “...disseminate knowledge of the ani-mals and love for them”, so that future generations would“...have an opportunity to live together with the great diver-sity of these magnificent creatures.” As stated above, our goalsin producing this updated and revised edition are similar.However, our challenges in producing this encyclopedia weremore formidable. The volume of knowledge to be summa-rized is certainly much greater in the twenty-first century thanit was in the 1970’s and 80’s. Scientists, both professional andamateur, have learned and published a great deal about theanimal kingdom in the past three decades, and our under-standing of biological and ecological theory has also pro-gressed. Perhaps our greatest hurdle in producing this revisionwas to include the new information, while at the same timeretaining some of the characteristics that have made Grzimek’sAnimal Life Encyclopedia so popular. We have therefore strivedto retain the series’ narrative style, while giving the informa-tion more organizational structure. Unlike the original Grz-imek’s, this updated version organizes information underspecific topic areas, such as reproduction, behavior, ecologyand so forth. In addition, the basic organizational structure isgenerally consistent from one volume to the next, regardlessof the animal groups covered. This should make it easier forusers to locate information more quickly and efficiently. Likethe original Grzimek’s, we have done our best to avoid anyoverly technical language that would make the work difficultto understand by non-biologists. When certain technical ex-pressions were necessary, we have included explanations orclarifications.

Considering the vast array of knowledge that such a workrepresents, it would be impossible for any one zoologist tohave completed these volumes. We have therefore sought spe-cialists from various disciplines to write the sections with

x Grzimek’s Animal Life Encyclopedia

Foreword

which they are most familiar. As with the original Grzimek’s,we have engaged the best scholars available to serve as topiceditors, writers, and consultants. There were some complaintsabout inaccuracies in the original English version that mayhave been due to mistakes or misinterpretation during thecomplicated translation process. However, unlike the origi-nal Grzimek’s, which was translated from German, this revi-sion has been completely re-written by English-speakingscientists. This work was truly a cooperative endeavor, and Ithank all of those dedicated individuals who have written,edited, consulted, drawn, photographed, or contributed to itsproduction in any way. The names of the topic editors, au-thors, and illustrators are presented in the list of contributorsin each individual volume.

The overall structure of this reference work is based onthe classification of animals into naturally related groups, adiscipline known as taxonomy or biosystematics. Taxonomyis the science through which various organisms are discov-ered, identified, described, named, classified and catalogued.It should be noted that in preparing this volume we adoptedwhat might be termed a conservative approach, relying pri-marily on traditional animal classification schemes. Taxon-omy has always been a volatile field, with frequent argumentsover the naming of or evolutionary relationships between var-ious organisms. The advent of DNA fingerprinting and otheradvanced biochemical techniques has revolutionized the fieldand, not unexpectedly, has produced both advances and con-fusion. In producing these volumes, we have consulted withspecialists to obtain the most up-to-date information possi-ble, but knowing that new findings may result in changes atany time. When scientific controversy over the classificationof a particular animal or group of animals existed, we did ourbest to point this out in the text.

Readers should note that it was impossible to include asmuch detail on some animal groups as was provided on oth-ers. For example, the marine and freshwater fish, with vast

numbers of orders, families, and species, did not receive asdetailed a treatment as did the birds and mammals. Due topractical and financial considerations, the publishers couldprovide only so much space for each animal group. In suchcases, it was impossible to provide more than a broad overviewand to feature a few selected examples for the purposes of il-lustration. To help compensate, we have provided a few keybibliographic references in each section to aid those inter-ested in learning more. This is a common limitation in all ref-erence works, but Grzimek’s Encyclopedia of Animal Life is stillthe most comprehensive work of its kind.

I am indebted to the Gale Group, Inc. and Senior EditorDonna Olendorf for selecting me as Series Editor for this pro-ject. It was an honor to follow in the footsteps of Dr. Grz-imek and to play a key role in the revision that still bears hisname. Grzimek’s Animal Life Encyclopedia is being publishedby the Gale Group, Inc. in affiliation with my employer, theAmerican Zoo and Aquarium Association (AZA), and I wouldlike to thank AZA Executive Director, Sydney J. Butler; AZAPast-President Ted Beattie (John G. Shedd Aquarium,Chicago, IL); and current AZA President, John Lewis (JohnBall Zoological Garden, Grand Rapids, MI), for approvingmy participation. I would also like to thank AZA Conserva-tion and Science Department Program Assistant, MichaelSouza, for his assistance during the project. The AZA is a pro-fessional membership association, representing 215 accred-ited zoological parks and aquariums in North America. AsDirector/William Conway Chair, AZA Department of Con-servation and Science, I feel that I am a philosophical de-scendant of Dr. Grzimek, whose many works I have collectedand read. The zoo and aquarium profession has come a longway since the 1970s, due, in part, to innovative thinkers suchas Dr. Grzimek. I hope this latest revision of his work willcontinue his extraordinary legacy.

Silver Spring, Maryland, 2001Michael Hutchins

Series Editor

Grzimek’s Animal Life Encyclopedia xi

Foreword

Gzimek’s Animal Life Encyclopedia is an internationallyprominent scientific reference compilation, first published inGerman in the late 1960s, under the editorship of zoologistBernhard Grzimek (1909-1987). In a cooperative effort be-tween Gale and the American Zoo and Aquarium Association,the series is being completely revised and updated for the firsttime in over 30 years. Gale is expanding the series from 13to 17 volumes, commissioning new color images, and updat-ing the information while also making the set easier to use.The order of revisions is:

Vol 8–11: Birds I–IVVol 6: AmphibiansVol 7: ReptilesVol 4–5: Fishes I–IIVol 12–16: Mammals I–VVol 1: Lower Metazoans and Lesser DeuterostomesVol 2: ProtostomesVol 3: InsectsVol 17: Cumulative Index

Organized by taxonomy

The overall structure of this reference work is based onthe classification of animals into naturally related groups, adiscipline known as taxonomy—the science through whichvarious organisms are discovered, identified, described,named, classified, and catalogued. Starting with the simplestlife forms, the lower metazoans and lesser deuterostomes, involume 1, the series progresses through the more complexanimal classes, culminating with the mammals in volumes12–16. Volume 17 is a stand-alone cumulative index.

Organization of chapters within each volume reinforcesthe taxonomic hierarchy. In the case of the Mammals vol-umes, introductory chapters describe general characteristicsof all organisms in these groups, followed by taxonomic chap-ters dedicated to Order, Family, or Subfamily. Species ac-counts appear at the end of the Family and Subfamily chaptersTo help the reader grasp the scientific arrangement, each typeof chapter has a distinctive color and symbol:

● =Order Chapter (blue background)

●▲ =Monotypic Order Chapter (green background)

▲ =Family Chapter (yellow background)

� =Subfamily Chapter (yellow background)

Introductory chapters have a loose structure, reminiscentof the first edition. While not strictly formatted, Order chap-ters are carefully structured to cover basic information aboutmember families. Monotypic orders, comprised of a singlefamily, utilize family chapter organization. Family and sub-family chapters are most tightly structured, following a pre-scribed format of standard rubrics that make information easyto find and understand. Family chapters typically include:

Thumbnail introductionCommon nameScientific nameClassOrderSuborderFamilyThumbnail descriptionSizeNumber of genera, speciesHabitatConservation status

Main essayEvolution and systematicsPhysical characteristicsDistributionHabitatBehaviorFeeding ecology and dietReproductive biologyConservation statusSignificance to humans

Species accountsCommon nameScientific nameSubfamilyTaxonomyOther common namesPhysical characteristicsDistributionHabitatBehavior

xii Grzimek’s Animal Life Encyclopedia

• • • • •

How to use this book

Feeding ecology and dietReproductive biologyConservation statusSignificance to humans

ResourcesBooksPeriodicalsOrganizationsOther

Color graphics enhance understandingGrzimek’s features approximately 3,000 color photos, in-

cluding approximately 1,560 in five Mammals volumes; 3,500total color maps, including nearly 550 in the Mammals vol-umes; and approximately 5,500 total color illustrations, in-cluding approximately 930 in the Mammals volumes. Eachfeatured species of animal is accompanied by both a distrib-ution map and an illustration.

All maps in Grzimek’s were created specifically for the pro-ject by XNR Productions. Distribution information was pro-vided by expert contributors and, if necessary, furtherresearched at the University of Michigan Zoological Museumlibrary. Maps are intended to show broad distribution, notdefinitive ranges.

All the color illustrations in Grzimek’s were created specif-ically for the project by Michigan Science Art. Expert con-tributors recommended the species to be illustrated andprovided feedback to the artists, who supplemented this in-formation with authoritative references and animal skins fromUniversity of Michgan Zoological Museum library. In addi-tion to species illustrations, Grzimek’s features conceptualdrawings that illustrate characteristic traits and behaviors.

About the contributorsThe essays were written by scientists, professors, and other

professionals. Grzimek’s subject advisors reviewed the com-pleted essays to insure consistency and accuracy.

Standards employedIn preparing these volumes, the editors adopted a conser-

vative approach to taxonomy, relying on Wilson and Reeder’sMammal Species of the World: a Taxonomic and Geographic Ref-erence (1993) as a guide. Systematics is a dynamic disciplinein that new species are being discovered continuously, andnew techniques (e.g., DNA sequencing) frequently result inchanges in the hypothesized evolutionary relationships amongvarious organisms. Consequently, controversy often exists re-garding classification of a particular animal or group of ani-mals; such differences are mentioned in the text.

Grzimek’s has been designed with ready reference in mindand the editors have standardized information wherever fea-sible. For Conservation status, Grzimek’s follows the IUCNRed List system, developed by its Species Survival Commis-sion. The Red List provides the world’s most comprehensiveinventory of the global conservation status of plants and an-imals. Using a set of criteria to evaluate extinction risk, theIUCN recognizes the following categories: Extinct, Extinctin the Wild, Critically Endangered, Endangered, Vulnerable,Conservation Dependent, Near Threatened, Least Concern,and Data Deficient. For a complete explanation of each cat-egory, visit the IUCN web page at <http://www.iucn.org/>.

Grzimek’s Animal Life Encyclopedia xiii

How to use this book

Series advisorMichael Hutchins, PhDDirector of Conservation and Science/William ConwayChairAmerican Zoo and Aquarium AssociationSilver Spring, Maryland

Subject advisors

Volume 1: Lower Metazoans and Lesser Deuterostomes

Dennis A. Thoney, PhDDirector, Marine Laboratory & FacilitiesHumboldt State UniversityArcata, California

Volume 2: Protostomes

Sean F. Craig, PhDAssistant Professor, Department of Biological SciencesHumboldt State UniversityArcata, California

Dennis A. Thoney, PhDDirector, Marine Laboratory & FacilitiesHumboldt State UniversityArcata, California

Volume 3: Insects

Arthur V. Evans, DScResearch Associate, Department of EntomologySmithsonian InstitutionWashington, DC

Rosser W. Garrison, PhDResearch Associate, Department of EntomologyNatural History MuseumLos Angeles, California

Volumes 4–5: Fishes I– II

Paul V. Loiselle, PhDCurator, Freshwater Fishes

New York AquariumBrooklyn, New YorkDennis A. Thoney, PhDDirector, Marine Laboratory & FacilitiesHumboldt State UniversityArcata, California

Volume 6: AmphibiansWilliam E. Duellman, PhDCurator of Herpetology EmeritusNatural History Museum and Biodiversity Research CenterUniversity of KansasLawrence, Kansas

Volume 7: ReptilesJames B. Murphy, DScSmithsonian Research AssociateDepartment of HerpetologyNational Zoological ParkWashington, DC

Volumes 8–11: Birds I–IVWalter J. Bock, PhDPermanent secretary, International Ornithological CongressProfessor of Evolutionary BiologyDepartment of Biological Sciences,Columbia UniversityNew York, New YorkJerome A. Jackson, PhDProgram Director, Whitaker Center for Science, Mathe-matics, and Technology EducationFlorida Gulf Coast UniversityFt. Myers, Florida

Volumes 12–16: Mammals I–VValerius Geist, PhDProfessor Emeritus of Environmental ScienceUniversity of CalgaryCalgary, AlbertaCanada

xiv Grzimek’s Animal Life Encyclopedia

• • • • •

Advisory boards

Devra G. Kleiman, PhDSmithsonian Research AssociateNational Zoological ParkWashington, DC

Library advisorsJames BobickHead, Science & Technology DepartmentCarnegie Library of PittsburghPittsburgh, Pennsylvania

Linda L. CoatesAssociate Director of LibrariesZoological Society of San Diego LibrarySan Diego, California

Lloyd Davidson, PhDLife Sciences bibliographer and head, Access ServicesSeeley G. Mudd Library for Science and EngineeringEvanston, Illinois

Thane JohnsonLibrarianOklahoma City ZooOklahoma City, Oklahoma

Charles JonesLibrary Media SpecialistPlymouth Salem High SchoolPlymouth, Michigan

Ken KisterReviewer/General Reference teacherTampa, Florida

Richard NaglerReference LibrarianOakland Community CollegeSouthfield CampusSouthfield, Michigan

Roland PersonLibrarian, Science DivisionMorris LibrarySouthern Illinois UniversityCarbondale, Illinois

Grzimek’s Animal Life Encyclopedia xv

Advisory board

Mammals I–VClarence L. Abercrombie, PhDWofford CollegeSpartanburg, South Carolina

Cleber J. R. Alho, PhDDepartamento de Ecologia (retired)Universidade de BrasíliaBrasília, Brazil

Carlos Altuna, LicSección EtologíaFacultad de CienciasUniversidad de la República Orientaldel UruguayMontevideo, Uruguay

Anders Angerbjörn, PhDDepartment of ZoologyStockholm UniversityStockholm, Sweden

William Arthur AtkinsAtkins Research and ConsultingNormal, Illinois

Adrian A. Barnett, PhDCentre for Research in EvolutionaryAnthropologySchool of Life SciencesUniversity of Surrey RoehamptonWest Will, LondonUnited Kingdom

Leonid Baskin, PhDInstitute of Ecology and EvolutionMoscow, Russia

Paul J. J. Bates, PhDHarrison InstituteSevenoaks, KentUnited Kingdom

Amy-Jane Beer, PhDOrigin Natural ScienceYork, United Kingdom

Cynthia Berger, MSNational Association of Science Writers

Richard E. Bodmer, PhDDurrell Institute of Conservation andEcologyUniversity of KentCanterbury, KentUnited Kingdom

Daryl J. Boness, PhDNational Zoological ParkSmithsonian InstitutionWashington, DC

Justin S. Brashares, PhDCentre for Biodiversity ResearchUniversity of British ColumbiaVancouver, British ColumbiaCanada

Hynek Burda, PhDDepartment of General Zoology Fac-ulty of Bio- and GeosciencesUniversity of EssenEssen, Germany

Susan Cachel, PhDDepartment of AnthropologyRutgers UniversityNew Brunswick, New Jersey

Alena Cervená, PhDDepartment of ZoologyNational Museum PragueCzech Republic

Jaroslav Cerveny, PhDInstitute of Vertebrate BiologyCzech Academy of SciencesBrno, Czech Republic

David J. Chivers, MA, PhD, ScDHead, Wildlife Research GroupDepartment of Anatomy

University of CambridgeCambridge, United Kingdom

Jasmin Chua, MSFreelance Writer

Lee Curtis, MADirector of PromotionsFar North Queensland Wildlife Res-cue AssociationFar North Queensland, Australia

Guillermo D’Elía, PhDDepartamento de Biología AnimalFacultad de CienciasUniversidad de la RepúblicaMontevideo, Uruguay

Tanya DeweyUniversity of Michigan Museum ofZoologyAnn Arbor, Michigan

Craig C. Downer, PhDAndean Tapir FundMinden, Nevada

Amy E. DunhamDepartment of Ecology and EvolutionState University of New York at StonyBrookStony Brook, New York

Stewart K. Eltringham, PhDDepartment of ZoologyUniversity of CambridgeCambridge, United Kingdom.

Melville Brockett Fenton, PhDDepartment of BiologyUniversity of Western OntarioLondon, OntarioCanada

Kevin F. Fitzgerald, BSFreelance Science WriterSouth Windsor, Connecticut

xvi Grzimek’s Animal Life Encyclopedia

• • • • •

Contributing writers

Theodore H. Fleming, PhDDepartment of BiologyUniversity of MiamiCoral Gables, Florida

Gabriel Francescoli, PhDSección EtologíaFacultad de CienciasUniversidad de la República Orientaldel UruguayMontevideo, Uruguay

Udo Gansloßer, PhDDepartment of ZoologyLehrstuhl IUniversity of Erlangen-NürnbergFürth, Germany

Valerius Geist, PhDProfessor Emeritus of EnvironmentalScienceUniversity of CalgaryCalgary, AlbertaCanada

Roger Gentry, PhDNOAA FisheriesMarine Mammal DivisionSilver Spring, Maryland

Kenneth C. Gold, PhDChicago, Illinois

Steve Goodman, PhDField Museum of Natural HistoryChicago, Illinois and WWF MadagascarProgramme OfficeAntananarivo, Madagascar

Nicole L. GottdenkerSt. Louis ZooUniversity of MissouriSt. Louis, Missouri and The CharlesDarwin Research StationGalápagos Islands, Ecuador

Brian W. Grafton, PhDDepartment of Biological SciencesKent State UniversityKent, Ohio

Joel H. GrossmanFreelance WriterSanta Monica, California

Mark S. Hafner, PhDLowery Professor and Curator ofMammalsMuseum of Natural Science and De-partment of Biological SciencesLouisiana State UniversityBaton Rouge, Louisiana

Alton S. Harestad, PhDFaculty of ScienceSimon Fraser University BurnabyVancouver, British ColumbiaCanada

Robin L. HayesBat Conservation of Michigan

Kristofer M. HelgenSchool of Earth and EnvironmentalSciencesUniversity of AdelaideAdelaide, Australia

Eckhard W. Heymann, PhDDepartment of Ethology and EcologyGerman Primate CenterGöttingen, Germany

Hannah Hoag, MSScience Journalist

Hendrik Hoeck, PhDMax-Planck- Institut für Verhal-tensphysiologieSeewiesen, Germany

David Holzman, BAFreelance WriterJournal Highlights EditorAmerican Society for Microbiology

Rodney L. Honeycutt, PhDDepartments of Wildlife and FisheriesSciences and Biology and Faculty ofGeneticsTexas A&M UniversityCollege Station, Texas

Ivan Horácek, Prof. RNDr, PhDHead of Vertebrate ZoologyCharles University PraguePraha, Czech Republic

Brian Douglas Hoyle, PhDPresident, Square Rainbow LimitedBedford, Nova ScotiaCanada

Graciela Izquierdo, PhDSección EtologíaFacultad de CienciasUniversidad de la República Orientaldel UruguayMontevideo, Uruguay

Jennifer U. M. Jarvis, PhDZoology DepartmentUniversity of Cape TownRondebosch, South Africa

Christopher Johnson, PhDDepartment of Zoology and TropicalEcologyJames Cook UniversityTownsville, QueenslandAustralia

Menna Jones, PhDUniversity of Tasmania School of Zo-ologyHobart, TasmaniaAustralia

Mike J. R. Jordan, PhDCurator of Higher VertebratesNorth of England Zoological SocietyChester ZooUpton, ChesterUnited Kingdom

Corliss KarasovScience WriterMadison, Wisconsin

Tim Karels, PhDDepartment of Biological SciencesAuburn UniversityAuburn, Alabama

Serge Larivière, PhDDelta Waterfowl FoundationManitoba, Canada

Adrian ListerUniversity College LondonLondon, United Kingdom

W. J. Loughry, PhDDepartment of BiologyValdosta State UniversityValdosta, Georgia

Geoff Lundie-Jenkins, PhDQueensland Parks and Wildlife ServiceQueensland, Australia

Peter W. W. Lurz, PhDCentre for Life Sciences ModellingSchool of BiologyUniversity of NewcastleNewcastle upon Tyne, United King-dom

Colin D. MacLeod, PhDSchool of Biological Sciences (Zool-ogy)University of AberdeenAberdeen, United Kingdom

James Malcolm, PhDDepartment of BiologyUniversity of RedlandsRedlands, California

Grzimek’s Animal Life Encyclopedia xvii


David P. Mallon, PhDGlossopDerbyshire, United Kingdom

Robert D. Martin, BA (Hons), DPhil,DScProvost and Vice PresidentAcademic AffairsThe Field MuseumChicago, Illinois

Gary F. McCracken, PhDDepartment of Ecology and Evolu-tionary BiologyUniversity of TennesseeKnoxville, Tennessee

Colleen M. McDonough, PhDDepartment of BiologyValdosta State UniversityValdosta, Georgia

William J. McShea, PhDDepartment of Conservation BiologyConservation and Research CenterSmithsonian National Zoological ParkWashington, DC

Rodrigo A. Medellín, PhDInstituto de EcologíaUniversidad Nacional Autónoma deMéxicoMexico City, Mexico

Leslie Ann Mertz, PhDFish Lake Biological ProgramWayne State UniversityDetroit, Michigan

Gus Mills, PhDSAN Parks/HeadCarnivore Conservation Group,EWTSkukuza, South Africa

Patricia D. Moehlman, PhDIUCN Equid Specialist Group

Paula Moreno, MSTexas A&M University at GalvestonMarine Mammal Research ProgramGalveston, Texas

Virginia L. Naples, PhDDepartment of Biological SciencesNorthern Illinois UniversityDeKalb, Illinois

Ken B. Naugher, BSConservation and Enrichment Pro-grams ManagerMontgomery ZooMontgomery, Alabama

Derek William Niemann, BARoyal Society for the Protection ofBirdsSandy, BedfordshireUnited Kingdom

Carsten Niemitz, PhDProfessor of Human BiologyDepartment of Human Biology andAnthropologyFreie Universität BerlinBerlin, Germany

Daniel K. Odell, PhDSenior Research BiologistHubbs-SeaWorld Research InstituteOrlando, Florida

Bart O’Gara, PhDUniversity of Montana (adjunct retiredprofessor)Director, Conservation Force

Norman Owen-Smith, PhDResearch Professor in African EcologySchool of Animal, Plant and Environ-mental SciencesUniversity of the WitwatersrandJohannesburg, South Africa

Malcolm Pearch, PhDHarrison InstituteSevenoaks, KentUnited Kingdom

Kimberley A. Phillips, PhDHiram CollegeHiram, Ohio

David M. Powell, PhDResearch AssociateDepartment of Conservation BiologyConservation and Research CenterSmithsonian National Zoological ParkWashington, DC

Jan A. Randall, PhDDepartment of BiologySan Francisco State UniversitySan Francisco, California

Randall Reeves, PhDOkapi Wildlife AssociatesHudson, QuebecCanada

Peggy Rismiller, PhDVisiting Research FellowDepartment of Anatomical SciencesUniversity of AdelaideAdelaide, Australia

Konstantin A. Rogovin, PhDA.N. Severtsov Institute of Ecologyand Evolution RASMoscow, Russia

Randolph W. Rose, PhDSchool of ZoologyUniversity of TasmaniaHobart, TasmaniaAustralia

Frank RosellTelemark University CollegeTelemark, Norway

Gretel H. SchuellerScience and Environmental WriterBurlington, Vermont

Bruce A. Schulte, PhDDepartment of BiologyGeorgia Southern UniversityStatesboro, Georgia

John H. Seebeck, BSc, MSc, FAMSAustralia

Melody Serena, PhDConservation BiologistAustralian Platypus ConservancyWhittlesea, Australia

David M. Shackleton, PhDFaculty of Agricultural of SciencesUniversity of British ColumbiaVancouver, British ColumbiaCanada

Robert W. Shumaker, PhDIowa Primate Learning SanctuaryDes Moines, Iowa and Krasnow Insti-tute at George Mason UniversityFairfax, Virginia

Andrew T. Smith, PhDSchool of Life SciencesArizona State UniversityPhoenix, Arizona

Karen B. Strier, PhDDepartment of AnthropologyUniversity of WisconsinMadison, Wisconsin

Karyl B. Swartz, PhDDepartment of PsychologyLehman College of The City Univer-sity of New YorkBronx, New York

Bettina Tassino, MScSección Etología

xviii Grzimek’s Animal Life Encyclopedia


Facultad de CienciasUniversidad de la República Orientaldel UruguayMontevideo, Uruguay

Barry Taylor, PhDUniversity of NatalPietermaritzburg, South Africa

Jeanette Thomas, PhDDepartment of Biological SciencesWestern Illinois University-QuadCitiesMoline, Illinois

Ann ToonArnside, CumbriaUnited Kingdom

Stephen B. ToonArnside, CumbriaUnited Kingdom

Hernán Torres, PhDSantiago, Chile

Rudi van Aarde, BSc (Hons), MSc,PhDDirector and Chair of ConservationEcology Research UnitUniversity of PretoriaPretoria, South Africa

Mac van der Merwe, PhDMammal Research InstituteUniversity of PretoriaPretoria, South Africa

Christian C. Voigt, PhDResearch Group Evolutionary EcologyLeibniz-Institute for Zoo and WildlifeResearchBerlin, Germany

Sue WallaceFreelance WriterSanta Rosa, California

Lindy Weilgart, PhDDepartment of BiologyDalhousie UniversityHalifax, Nova ScotiaCanada

Randall S. Wells, PhDChicago Zoological SocietyMote Marine LaboratorySarasota, Florida

Nathan S. WeltonFreelance Science WriterSanta Barbara, California

Patricia Wright, PhDState University of New York at StonyBrookStony Brook, New York

Marcus Young Owl, PhDDepartment of Anthropology and Department of Biological SciencesCalifornia State UniversityLong Beach, California

Jan Zima, PhDInstitute of Vertebrate BiologyAcademy of Sciences of the Czech RepublicBrno, Czech Republic

Grzimek’s Animal Life Encyclopedia xix


Drawings by Michigan Science ArtJoseph E. Trumpey, Director, AB, MFAScience Illustration, School of Art and Design, Universityof Michigan

Wendy Baker, ADN, BFA

Ryan Burkhalter, BFA, MFA

Brian Cressman, BFA, MFA

Emily S. Damstra, BFA, MFA

Maggie Dongvillo, BFA

Barbara Duperron, BFA, MFA

Jarrod Erdody, BA, MFA

Dan Erickson, BA, MS

Patricia Ferrer, AB, BFA, MFA

George Starr Hammond, BA, MS, PhD

Gillian Harris, BA

Jonathan Higgins, BFA, MFA

Amanda Humphrey, BFA

Emilia Kwiatkowski, BS, BFA

Jacqueline Mahannah, BFA, MFA

John Megahan, BA, BS, MS

Michelle L. Meneghini, BFA, MFA

Katie Nealis, BFA

Laura E. Pabst, BFA

Amanda Smith, BFA, MFA

Christina St.Clair, BFA

Bruce D. Worden, BFA

Kristen Workman, BFA, MFA

Thanks are due to the University of Michigan, Museumof Zoology, which provided specimens that served as mod-els for the images.

xx Grzimek’s Animal Life Encyclopedia

• • • • •

Contributing illustrators

Maps by XNR ProductionsPaul Exner, Chief cartographerXNR Productions, Madison, WI

Tanya Buckingham

Jon Daugherity

Laura ExnerAndy GrosvoldCory JohnsonPaula Robbins

Topic overviewsWhat is a mammal?

Ice Age giants

Contributions of molecular genetics to phylogenetics

Structure and function

Adaptations for flight

Adaptations for aquatic life

Adaptations for subterranean life

Sensory systems

Life history and reproduction

Mammalian reproductive processes

Ecology

Nutritional adaptations of mammals

Distribution and biogeography

Behavior

Cognition and intelligence

Migration

Mammals and humans: Domestication and commensals

Mammals and humans: Mammalian invasives and pests

Mammals and humans: Field techniques for studying mammals

Mammals and humans: Mammals in zoos

Conservation

• • • • •

At first sight, this is not a difficult question. Every child isable to identify an animal as a mammal. Since its earliest ageit can identify what is a cat, dog, rabbit, bear, fox, wolf, mon-key, deer, mouse, or pig and soon experiences that with any-one who lacks such a knowledge there would be little chanceto communicate about other things as well. To identify ananimal as a mammal is indeed easy. But by which character-istics? The child would perhaps explain: Mammals are hairyfour-legged animals with faces.

A child answers: A hairy four-legged animalwith a face

Against expectation, the three characteristics reported bythis naive description express almost everything that is mostessential about mammals.

Hair, or fur, probably the most obvious mammalian fea-ture, is a structure unique to that group, and unlike the feath-ers of birds is not related to the dermal scales of reptiles. Amammal has several types of hairs that comprise the pelage.Specialized hairs, called vibrissae, mostly concentrated in thefacial region of the head, perform a tactile function. Pelageis seasonally replaced in most mammals, usually once or twicea year by the process called molting. In some mammals, suchas ermines, the brown summer camouflage can be changedto a white coat in winter. In others, such as humans, ele-phants, rhinoceroses, naked mole rats, and aardvarks, and inparticular the aquatic mammals such as walruses, hip-popotami, sirenia, or cetaceans, the hair coat is secondarilyreduced (though only in the latter group is it absent com-pletely, including vibrissae). In the aquatic mammals (but notonly in them), the role of the pelage is performed by a thicklayer of subcutaneous adipose tissue by which the surface ofbody is almost completely isolated from its warm core andthe effect of a cold ambient environment is substantially re-duced. Thanks to this tissue, some mammals can forage evenin cold arctic waters and, as a seal does, rest on ice withoutrisk of freezing to it. In short, the essential role of the sub-cutaneous adipose layer and pelage is in thermal isolation, inpreventing loss of body heat. Mammals, like birds, are en-dotherms (heat is generated from inside of the body by con-tinuous metabolic processes) and homeotherms (the bodytemperature is maintained within a narrow constant range).

The body temperature of mammals, about 98.6°F (37°C), isoptimal for most enzymatic reactions. A broad variety offunctions are, therefore, kept ready for an immediate trig-gering or ad hoc mutual coupling. All this also increases theversatility of various complex functions such as locomotion,defensive reactions, and sensory performances or neural pro-cessing of sensory information and its association analysis.The constant body temperature permits, among other things,a high level of activity at night and year-round colonizationof the low temperature regions and habitats that are not ac-cessible to the ectothermic vertebrates. In short, endothermyhas a number of both advantages and problems. Endothermyis very expensive and the high metabolic rate of mammals re-quires quite a large energetic intake. In response, mammalsdeveloped a large number of very effective feeding adapta-tions and foraging strategies, enabling them to exploit an ex-treme variety of food resources from insects and smallvertebrates (a basic diet for many groups) to green plants (awidely accessible but indigestible substance for most non-mammals). At the same time, mammals have also developeddiverse ways to efficiently control energy expenditure.

Besides structural adaptations such as hair, mammals havealso developed diverse physiological and behavioral meansto prevent heat and water loss, such as burrowing into un-derground dens; seasonal migrations or heterothermy; andthe controlled drop of body temperature and metabolic ex-penditure during part of the day, or even the year (hiberna-tion in temperate bats, bears, and rodents as well as summerestivation in some desert mammals). So, considerable adap-tive effort in both directions increases foraging efficiencyand energy expenditure control. When integrated with mor-phological, physiological, behavioral, and social aspects, it isan essential feature of mammalian evolution and has con-tributed to the appearance of the mammalian character inmany respects.

Four legs, each with five toes, are common not only to manymammals, but to all terrestrial vertebrates (amphibians, rep-tiles, birds, and mammals), a clade called Tetrapoda. Never-theless, in the arrangement of limbs and the modes oflocomotion that it promotes, mammals differ extensively fromthe remaining groups. The difference is so clear that it allowsus to identify a moving animal in a distance as a mammal evenin one blink of an eye. In contrast to the “splayed” reptilian

Grzimek’s Animal Life Encyclopedia 3

• • • • •

What is a mammal?

stance (i.e. horizontal from the body and parallel to theground), the limbs of mammals are held directly beneath thebody and move in a plane parallel to the long axis of the body.In contrast to reptiles, whose locomotion is mostly restrictedto the lateral undulation of the trunk, mammals flex their ver-tebrate column vertically during locomotion. This arrange-ment enables a powered directional movement, such assustained running or galloping, very effective for escapingfrom a predator, chasing mobile prey, or exploring spatiallydispersed food resources. The respective rearrangements alsobring another effect. By strengthening the vertebral columnagainst lateral movement, the thoracic cavity can be consid-erably enlarged and the thoracic muscles released from a lo-comotory engagement, promoting changes to the effectivevolume of the thoracic cavity. With a synergetic support fromanother strictly mammalian structure, a muscular diaphragmseparating the thoracic and visceral cavity, the volume of thethoracic cavity can change during a breathing cycle muchmore than with any other vertebrates. With the alveolar lungs,typical for mammals, that are designed to respond to volumechanges, breathing performance enormously increases. Thisenables a mammal to not only keep its basal metabolic rateat a very high level (a prerequisite for endothermy) but, inparticular, to increase it considerably during locomotion. Inthis connection, it should be stressed that the biomechanicsof mammalian locomotion not only allow a perfect synchro-nization of limb movements and breathing cycles but, withthe vertical flex of the vertebral column, are synergetic to thebreathing movements and support it directly. As a result, theinstantly high locomotory activity that characterizes a mam-mal increases metabolic requirements but at the same timehelps to respond to them.

The face is the essential source of intra-group social infor-mation not only for humans but for many other mammal

groups. The presence of sophisticated mechanisms of socialintegration and an enlarged role in interindividual discrimi-nation and social signaling are broadly characteristic of mam-mals. Nevertheless, each isolated component contributing tothe complex image of the mammalian face says something im-portant regarding the nature of the mammalian constitution,and, moreover, they are actually unique characters of thegroup. This is particularly valid for fleshy cheeks and lips, themuscular belt surrounding the opening of a mouth. The lipsand the spacious pocket behind them between the cheeks andteeth (the vestibulum oris) are closely related to feeding, andnot only in that they enlarge the versatility of food process-ing in an adult mammal. The lips, cheeks and vestibulum orisare completely developed at the time of birth and since thattime have engaged in the first behavioral skill performed bya mammal. Synergetic contraction of lip and cheek musclesproducing a low pressure in the vestibulum oris is the key component of the suckling reflex, the elementary feedingadaptation of a newborn mammal. All mammals, without ex-ception, nourish their young with milk and all female mam-mals have large paired apocrine glands specialized for thisrole—the mammary glands, or mammae. Nevertheless, not

4 Grzimek’s Animal Life Encyclopedia

Vol. 12: Mammals IWhat is a mammal?

Red kangaroos (Macropus rufus) on the move. (Photo by Animals An-imals ©Gerard Lacz. Reproduced by permission.)

A spotted hyena (Crocuta crocuta) stands on its meal of a baby ele-phant. (Photo by Harald Schütz. Reproduced by permission.)

all mammalian newborns actually suck the milk. In the egg-lying monotremes (the Australian duck-billed platypus andspiny anteaters), mammary glands lack the common milkducts and nipples, so young do not suck but instead lick themilk using their tongue. All other mammals, both marsupialsand eutherians, together denoted as Theria, bear a distinctivestructure supporting suckling—the paired mammary nipples.The nipples originate independently from mammary glands,they are present both in males and females, and their num-ber and position is an important character of individual clades.The therian mammals are all viviparous. For the most vul-nerable period of their lives they are protected first by the in-trauterine development with placental attachment of theembryo and then by prolonged postnatal parental care. A milkdiet during the latter stage postpones the strict functional con-trol on jaws and dentition and enables postnatal growth, theessential factor for the feeding efficiency of an adult mammal.At the same time this provides extra time for development ofother advanced and often greatly specialized mammaliancharacteristics: an evolving brain and the refinement of mo-tor capacities and behavioral skills. Thanks to the extendedparental investment that mammalian offspring have at the be-ginning of their independent life, they enjoy a much higherchance for post-weaning survival than the offspring of mostother vertebrates. The enormous cost of the parental invest-ment places, of course, a significant limit upon the numberof offspring that can be produced. Despite the great variationin reproductive strategies among individual mammalian

clades, in comparison to other vertebrates (excepting elasmo-branchians and birds), the mammals are clearly the K-strate-gists (producing few; but well-cared for, offspring) in general.

The other components of the mammalian face provide cor-respondingly significant information on the nature of theseanimals. The vivid eyes with movable eyelids, external auri-cles, nose, and last but not least long whiskers (vibrissae, thehairs specialized for tactile functions), show that a mammal isa sensory animal. Most extant mammals are noctural or cre-puscular and this was almost certainly also the case with theirancestors. In contrast to other tetrapods, which are mostly di-urnal and perceive almost all spatial information from vision,mammals were forced to build up a sensory image of the worldfrom a combination of different sources, in particular olfac-tion and hearing. Nevertheless, vision is well developed inmost mammals and is capable of very fine structural and colordiscrimination, and some mammals are secondarily just opti-cal animals. For example, primates exhibit a greatly enlargedcapability for stereoscopic vision. In any case, all mammalshave structurally complete eyes, though the eyes may be cov-


What is a mammal?Vol. 12: Mammals I

Some mammals, such as this goat, have rather dramatic antlers orhorns. (Photo by Animals Animals ©Robert Maier. Reproduced by per-mission.)

A baby gray bat (Myotis grisescens). (Photo by Merlin D. Tuttle/BatConservation International/Photo Researchers, Inc. Reproduced by per-mission.)

ered by skin in some fossorial mammals (such as blind molerats, or marsupial moles) or their performance may be re-duced in some respect. In comparison with other vertebrates,the performance of vision is particularly high under low lightintensities, and the eyes are quite mobile. The latter charac-ter may compensate for a reduced ability of head rotation inmammals due to the bicondylous occipital joint contrastingto a monocondylous joint in birds or reptiles. The eyes arecovered by movable eyelids (not appearing in reptiles), sig-nificant both in protecting the eyes and in social signaling.The remaining two structures—nose and auricles—are par-ticularly unique for mammals and are related to the sensesthat are especially important for mammals: olfaction and hear-ing. Not only the nose and auricles themselves, but also theother structures associated with the senses of smell and hear-ing feature many traits unique to mammals.

Mammals construct much of their spatial information withthe sole aid of olfactory, acoustic, or tactile stimuli combinedwith information from low-intensity vision. This task neces-sitated not only a considerable increase in the capacity andsensory versatility of the respective organs, but also the re-finement of the semantic analysis of the information they pro-vide. As a result, the brain structures responsible for thesetasks are greatly enlarged in mammals. The tectum mesen-

cephali, a center for semantic analysis of optical information,bi-lobed in other vertebrates, is supplemented by a distinctcenter of acoustic analysis by which the tectum of mammalsbecomes a four-lobed structure, the corpora quadrigemina.The forebrain or telencephalon, a structure related to olfac-tory analysis, is by far the largest part of the mammalian brain.Its enlargement is particularly due to the enlarging of the neo-cortex, a multi-layered surface structure of the brain, whichfurther channels inputs from other brain structures and playsthe role of a superposed integrative center for all sensory, sensory-motor, and social information.

A zoologist answers: A highly derived amnioteMany of the characters common to mammals do not ap-

pear in other animals. Some of them, of course, can be ob-served also in birds—a very high (in respect to both maximumand mean values) metabolic rate and activity level or com-plexity of particular adaptations such as advanced parental careand social life, increased sensory capacities, and new pathwaysof processing sensory information or enormous ecological ver-satility. Fine differences between birds and mammals suggestthat the respective adaptations are homoplasies—that is, theyevolved in both groups independently.



Near Kilimanjaro, a giraffe (Giraffa camelopardalis) pauses to survey for predators. Giraffes are the tallest extant mammals, males reaching 18ft (5.5 m) in height. (Photo by Harald Schütz. Reproduced by permission.)

Other mammalian characteristics are synapomorphies ofAmniota, the characteristics shared because of common an-cestry. The amniotes, a group including reptiles, birds, andmammals, are the terrestrial vertebrates in which embryonicdevelopment takes place under the protection of fetal mem-branes (amnion, chorion, allantois). As in other amniotes,mammals are further characterized by an increased role ofparental investment, internal fertilization, keratinized skin de-rivatives, an advanced type of kidney (metanephros) with aspecific ureter, an advanced type of lung respiration, and thedecisive role of dermal bones in skull morphology. Of course,at the same time, mammals share a large number of charac-teristics with all other vertebrates, including the general bodyplan, solid inner skeleton, the design of homeostatic mecha-nisms (including pathways of neural and humoral regulation),and functional integration of particular developmental mod-ules. Mammals also share with other vertebrates the patternsof segmentation of trunk skeleton and muscles and the spe-cific arrangements of the homeobox genes organizing thebody segmentation as well as a lack of their expression in thehead region, etc. These characters are synapomorphies of ver-tebrates, which are at least partly retained not only in someamniotes but throughout all other vertebrate clades. With re-spect to mammals, these are symplesiomorphies, the primi-tive characters that do not reveal closer relations of the classbut on its broadest phylogenetic context.

Mammals also exhibit a large number of qualities that arefully unique to them, the autapomorphies. The autapomor-phies are the characteristics by which a taxon can be clearlydistinguished and diagnosed. Thus, though many character-istics of mammals are not specific just to them, answeringthe question “what is a mammal?” means first demonstrat-ing the autapomorphies of that group. A simplified list ofthem includes:

(1) The young are nourished with milk produced by (2) mam-mary glands. These glands appear in all female mammals, andare the structure from which the class Mammalia got its name.(3) Obligatory vivipary (in Theria, i.e., marsupials and placen-tals) is the reproductive mode with a specialized organ inter-connecting the embryo and maternal tissues, the chorioallantoicplacenta (in Eutheria, i.e., placentals). (4) Hairs, covering thebody, grow from deep invaginations of the germinal layer ofepidermis called follicles. Similar to other amniotes, the hairis composed of keratin and pigments, but its structure isunique for mammals. (5) Skin is rich in various glands. Mostmammals have sweat glands (contributing to water balanceand cooling the body surface), scent glands, and sebaceousglands. (6) The specific integumental derivatives, characteristicof particular groups of mammals, are composed either exclu-sively of keratin (such as claws, nails, and hoofs, which pro-tect the terminal phalanx of the digits and adapt them to a



Black-handed spider monkeys (Ateles geoffroyi) grooming. (Photo by Gail M. Shumway. Bruce Coleman, Inc. Reproduced by permission.)

specific way of locomotion or foraging) or of keratin in com-bination with dermal bone structures (horns of bovids andantlers of cervid artiodactyls, which play a considerable rolein social signaling). A large variety of integumental deriva-tives are included in defensive adaptations: dermal armors ofarmadillos or keratinized scales of pangolins, spines modifiedfrom hairs in echidnas, hedgehogs, tenrecs, porcupines, orspiny mice, or the accumulations of hairlike fibers keratinizedinto a horn structure in rhinoceroses. (7) Limb position andfunction are modified to support specific locomotory modesof mammals such as jumping, galloping, or sustained runningand can be specifically rearranged. The extreme rearrange-ments are seen in bats, which fly using a forelimb wing, andin specialized marine mammals, pinnipedian carnivores,cetaceans, and sirenia, whose forelimbs take the shape of a fin(the external hind limbs are absent in the latter two groups).(8) Pectoral girdle is simplified in comparison to the non-mam-malian state: coracoid, precoracoid and interclavicle bones arelost (except for monotremes, which retain them) or partly in-cluded in the scapula. Also the clavicle, the last skeletal ele-ment that fixes the limb to the axial and thoracic skeleton, is

lost in many groups. With these rearrangements the forelimbsget new locomotory qualities (such as extensive protraction),supporting abilities such as climbing and fine limb movementsand providing a new spectrum of manipulative functions fromcleaning hair to a variety of prey manipulations. (9) The bonesof the pelvic girdle are fused into a single bone, with enlarged andhorizontally prolonged ilium.

(10) A great degree of regional differentiation of the vertebralcolumn. All mammals (except some edentates and manatees)have seven cervical vertebrae with the first two (atlas and axis)specifically rearranged to support powered head movements.(11) The vertebral column is strengthened against lateral move-ments but is greatly disposed to the vertical flexion. This isseen first of all in the lumbar section, whose vertebrae, in con-trast to the non-mammalian ancestors, lack ribs. (12) Themammalian skull is bicondylous (the first vertebra, atlas, jointsthe skull via paired occipital condyles located on the lateralsides of the large occipital foramen), with (13) an enlargedbraincase, (14) massive zygomatic arches (formed by the jugaleand squamosum bones), and (15) a spacious nasal cavity witha labyrith of nasal turbinalia covered by vascularized tissue im-portant both for olfaction (ethmoidal turbinalia) and/or heatand water exchange during breathing (maxillary turbinalia).(16) The nostrils open at a common structure called the nose,obviously the most prominent point of the head. The ances-tral form of the nose, the rhinarium, is a hairless field ofdensely circular-patterned skin surrounding the nostril open-ings. The rhinarium is particularly large in macrosmatic(highly developed sense of smell) mammals (such as carni-vores or artiodactyls), in lagomorphs, some rodents, and bats.In strepsirhine primates it is incised by a central groove, thephlitrum, while in some other groups such as in macroscelidsor in elephants, the nose is prolonged and attains a numberof supplementary functions. In contrast, all these structuresare absent in cetaceans in which the nasal cavity is reducedand the nostrils (or a single nostril opening in Odontoceti)appear at the top of the head and their function is restrictedto respiration. (17) Left and right maxillary and palatal bonesare fused in early development and form the secondary bonypalate, which is further extended by a fleshy soft palate. Thesestructures provide a complete separation of the respiratoryand alimentary tracts. The early appearance of such a sepa-ration is one of the essential prerequisites for suckling milkby a newborn and, hence, it seems probable that the secondarypalate first appeared simply as an adaptation for this. (18) Theheart is a large four-chambered organ (as in birds) with the leftaorta persistent (not the right one, as in birds). (19) Erythro-cytes, the red blood cells, are biconcave and lack nuclei. Thrombo-cytes are transformed to nonnucleated blood platelets.

(20) Lungs have an alveolar structure, ventilated by volumechanges performed by the counteraction of two independentmuscular systems, and a (21) muscular diaphragm, unique formammals. (22) The voice organ in the larynx, with several pairsof membranous muscles, is unique for mammals. It is capa-ble of very specialized functions such as the production of var-ious communicative signals or high-frequency echolocationcalls in bats and cetaceans. (23) There are three ossicles in themiddle ear (malleus, incus, stapes). The former two are uniqueto mammals and are derived from the elements of the pri-



A silverback jackal (Canis mesomelas) and an African elephant (Lox-odonta africana) at a watering hole in Chobe National Park, Botswana.(Photo by © Theo Allofs/Corbis. Reproduced by permission.)

mary mandibular joint—articulare and quadratum—whichstill retain their original function in the immediate mam-malian ancestors. The third bone of the primary mandibularjoint, the angulare, changes in mammals into the tympanicbone, which fixes the tympanic membrane and finally enlargesinto a bony cover of the middle ear—the bulae tympani. (24)The sound receptor (Corti´s organ of the inner ear) is quite longand spirally coiled in mammals (except for monotremes) andsurrounded by petrosum, a very compact bone created by a fu-sion of several elements. (25) With an enlarged braincase, themiddle ear and tympanic membrane are thus located deeperin the head and open to the external environment by a longauditory meatus terminating with (26) a large movable externalauricle. Auricles (pinnae) are specifically shaped in particularclades and contribute to the lateral discrimination of the au-ditory stimuli and directionality of hearing. They may be ab-sent in some aquatic mammals (cetaceans, sirenia, walruses),while they are extremely pronounced and diversified in othergroups such as bats, for which the acoustic stimuli (echoes ofthe ultrasonic calls they emit) are by far the most importantsource of spatial information. (27) In contrast to other am-niotes, the lower jaw, or mandible, is composed of a single bone,dentary or dentale, which directly articulates with the tem-poral bone of the skull at the (28) dentary-squamosal joint. Thisarrangement not only fastens the jaw joint to resist the forcesexerted during strong biting but also simplifies the functionalrearrangements of jaw morphology responding to differentdemands of particular feeding specializations. (29) In allmammals, the posterior part of the mandible extends dorsallyinto the ramus mandibulae, which provides an area of attach-ment for the massive temporal muscles responsible for thepowered adduction of the mandible.

(30) Essentially, all mammals have large teeth despite con-siderable variation in number, shape, and function in partic-ular groups and/or the fact that some mammals secondarilylack any teeth at all (anteaters of different groups, and theplatypus). Teeth are deep-rooted in bony sockets called alve-oles. Only three bones host the teeth in mammals: the pre-maxilla and maxilla in the upper jaw and the dentary in thelower jaw. (31) Mammalian dentition is generally heterodont (ofdifferent size, shape, etc.). Besides the conical or unicuspidateteeth (incisors and a single pair of canines in each jaw) mam-mals also have large complex multicuspidate molars (three inplacentals, four in marsupials, in each jaw quadrant) and pre-molars situated between canines and molars whose shape andnumber varies considerably among particular groups. The lat-ter two teeth types are sometimes called “postcanines” or“cheek teeth.” (32) The molars are unique to mammals. Thebasic molar type ancestral to all particular groups of mam-mals is called tribosphenic. It consists of three sharp conesconnected with sharp blades. In combination with the deepcompression chambers between blades, such an arrangementprovides an excellent tool both for shearing soft tissues andcrushing insect exoskeletons. This type of molar is retainedin all groups feeding on insects, such as many marsupials, ten-recs, macroscelids, true insectivores such as moles, shrews orhedgehogs, bats, tree shrews, and prosimian primates, but thedesign of the molar teeth is often extensively rearranged inother groups. The multicuspidate structure of molars bearsenormous potential for morphogenetic and functional re-

arrangements, one of the prerequisites of the large diversityof feeding adaptations in mammals. (33) Mammalian denti-tion is diphyodont. This means that there are two generationsat each tooth position (except for molars): the milk or decid-uous teeth of the young and the permanent teeth of an adultmammal. Diphyodonty solves a functional-morphologicaldilemma: the size of teeth, an essential factor in feeding effi-ciency, is limited by the size of the jaws. While the jaws cangrow extensively, the posteruption size of the teeth cannot bechanged due to the rigidity of their enamel cover, which isthe essential quality of a tooth. With diphyodonty, the sizeof the late erupting permanent teeth can be maximized andadapted to adult jaw size while the deciduous dentition pro-vides a corresponding solution for the postweaning period.Dental morphology and the patterns of tooth replacement arespecifically modified in some clades. In marsupials, only onemilk tooth—the last premolar—comes in eruption, while theothers are resorbed prior to eruption. Dolphins, aardvarks,and armadillos have a homodont dentition without any toothreplacement. No tooth replacement occurs in small and short-living mammals with greatly specialized dentition, such asshrews or muroid rodents (deciduous teeth are resorbed in-stead of eruption), while in some large herbivores tooth re-placement can become a continuous process by which thetooth row enlarges gradually by subsequent eruption of stilllarger molar teeth in the posterior part of the jaws. In ele-phants and manatees, this process includes a horizontal shiftof the erupting tooth, which thus replaces the preceding cheektooth. All these processes are well synchronized with thegrowth of jaws, the course of tooth wear, and subsequent pro-longing of time available for tooth development. (34) A gen-eral enlargement of the brain related perhaps not only to anincrease in the amount of sensory information and/or a needto integrate sensory information from different sources, butalso to more locomotory activity, high versatility in locomo-



Many young mammals practice skills needed for survival. These lioncubs practice hunting in the grass. (Photo by K. Ammann. Bruce Cole-man, Inc. Reproduced by permission.)

tory functions, a greatly diversified social life, and a consid-erably expanded role for social and individual learning. (38)The extended spectrum of behavioral reactions and their in-terconnections with an increased capacity of social and indi-vidual learning and interindividual discrimination should alsobe mentioned. In fact, this characteristic is very significant formammals, as are the following two: (39) Growth is terminatedboth by hormonal control and structural factors. The mostinfluential structural aspect of body growth is the appearanceof cartilaginous epiphyseal discs separating diaphyses and epiphysesof long bones. With completed ossification, the discs disap-pear and growth is finished. Corresponding mechanisms de-termine the size of the skull (except in cetaceans, which havea telescoped skull in which the posterior bones of the craniumoverlap each other). (40) Sex is determined by chromosomalconstitution (XY system, heterogametic sex is a male).

Almost all of these (and other) characteristics undergo sig-nificant variations and their modifications are often largelyspecific for particular clades of mammals. What is commonfor all is perhaps that in mammals all the characters are moredensely interrelated than in other groups (except for birds).The morphological adaptations related to locomotion or feed-ing are often also integrated for social signaling, physiologi-cal regulation, or reproductive strategy, and often arecontrolled by quite distant and non-apparent factors. Thus,the excessive structures of ruminant artiodactyls, such as thehorns of bovids and antlers of deer, are undoubtedly signifi-cant in social signaling, in courtship and display behavior, andfrequently are discussed as excessive products of sexual selec-tion. However, the proximate factor of these structures, thehereditary disposition for excessive production of mineralizedbone tissue, can actually be selected rather by its much less

obvious effect in a female: her ability to produce a large, ex-tremely precocial newborn with highly mineralized longbones that enable it to walk immediately after parturition. Thefemale preference for the excessive state of the correlatedcharacters in a male, his large body size and display qualities,possibly supported by social learning, supplement the mech-anisms of the selection in quite a non-trivial way. Such amulti-layered arrangement of different factors included in aparticular adaptation is indeed something very mammalian.

A paleontologist answers: The product of theearliest divergence of amniotes and index fos-sils of the Cenozoic

Mammals are the only extant descendants of the synap-sids—the first well-established group of amniotes, named af-ter a rounded temporal opening behind the orbit bordered bythe jugale and squamosum bones. Since the beginning of am-niotes, evolution of synapsids proceeded separately from theother amniotes, which later diversified in particular reptilelineages including dinosaurs and birds. The first amniotesrecorded from the middle Carboniferous (320 million yearsago) were just synapsids and just this clade predominated inthe fossil record of the terrestrial vertebrates until the earlyTriassic. A large number of taxa appearing among early synap-sids represented at least two different clades: Eupelycosauriaand Caseasauria. The former included large carnivorousforms and the latter were generalized small- or medium-sizedomnivores. Since the middle Permian (260 mya), anothergroup of synapsids called Therapsida dominated the terres-trial record. In comparison with pelycosaurs, therapsids hadmuch larger temporal openings, a single pair of large canines,



A cheetah (Acinonyx jubatus) chases a Thomson’s gazelle (Gazella thomsonii). The cheetah is the fastest land animal and can reach speeds of70 mph (113 kph). (Photo by Tom Brakefield. Bruce Coleman, Inc. Reproduced by permission.)

and clear functional and shape differences between the ante-rior and the posterior teeth. Two lineages of that group, Di-cynodontia and Cynodontia, survived the mass extinction atthe Permian/Triassic boundary (248 mya).

Immediate ancestors of mammals are found among thecynodonts. Mammals are closely related to cynodont groupscalled tritylodontids and trithelodontids, which first ap-peared during the late Triassic. All three groups, includingmammals, had additional cusps on posterior teeth, a well-developed ramus mandibulae, and a complete secondarypalate. In some of them (Diarthrognathus), the jaw joint wasformed both by the original articulation (articulare-quadra-tum) and by the mammal-like process (dentary-squamosal).In the oldest true mammals, the former jaw articulation isabandoned and removed in the middle ear. These charactersare the index diagnostic features of a mammal in the fossilrecord (no. 23, 26, 27 of the above list).

The oldest mammals, Sinoconodon, Adelobasileus, Kuehneo-therium, or Morganucodon (about 200–225 million years old),were all very small, with long heterodont dentition and a tri-angular arrangement of molar cusps designed for shearing.They were most probably quite agile night creatures resem-bling today’s insectivores. The relative brain volume in theearliest mammals was close to that found in extant insecti-vores and about three times higher than in cynodonts. Ofcourse, they still differed from the modern mammals in manyrespects. The derived characters of modern mammals (as re-viewed in the preceding text) did not evolve together but weresubsequently accumulated during the long history of synap-sid evolution.

In contrast to the medium- to large-sized diurnal dinosaurs,birds, and other reptiles that had dominated the terrestrialhabitats, the early mammals were quite small, nocturnal crea-tures. Nevertheless, since the Jurassic period they grew ingreatly diversified groups and at least four lineages of that radiation survived the mass extinction at the Cretaceous/Tertiary boundary (65 mya). Three of these groups, mono-tremes, marsupials, and placentals, are extant; the fourthgroup, multituberculates, survived until the end of Oligocene.Multituberculates resembled rodents in design of dentition(two pairs of prominent incisors separated from a series ofcheek teeth by a toothless diastema), but their cheek teeth andskull morphology were quite different from those in any othergroups of mammals.

The major radiation of mammals appeared at the begin-ning of Tertiary, in the Paleocene. That radiation producedmany groups that are now extinct (including nine extinct or-ders) as well as almost all the orders of modern mammals. Dur-ing the Paleocene and Eocene, other groups occupied theniches of current mammalian groups. In Eurasia and NorthAmerica it was Dinocerata, Taeniodonta, and Tillodontia asherbivores and Pantodonta and Creodonta as their predators.All these are extinct lineages not related to any of the recentorders. The most isolated situation was in Australia, which hadbeen cut-off from the other continents since the Cretaceousand was not influenced by the intervention of the eutherianmammals. The mammalian evolution in South America afterits separation from Africa at the early Paleocene was equally

isolated. Besides the marsupials (clade of Ameridelphia) andedentates with giant glyptodonts, mylodonts, and megalony-chids, whose relatives survived until recently, a great varietyof strange eutherians appeared here during the Paleocene andEocene. This includes the large herbivores of the orders No-toungulata, Astrapotheria, Litopterna, and Xenungulata, aswell as the Pyrotheria (resembling proboscideans) and theirgiant marsupial predators, such as Thylacosmilus, resemblingthe large saber-toothed cats. The mammalian fauna of SouthAmerica was further supplemented by special clades of hys-tricognathe rodents, haplorhine primates, and several cladesof bats, particularly the leaf-nosed bats. These groups proba-bly entered South America during the Paleocene or Eoceneby rafting from Africa. The evolution in splendid isolation ofSouth America terminated with the appearance of a land bridgewith North America some 3 mya, which heavily impacted thefauna of both continents. The impact of African and Asianfauna on the European mammalian evolution by the end ofEocene was of a similar significance.

It is important to remember that the fossil record of mam-mals, including detailed pathways of evolutionary divergencesand/or the stories of particular clades, is much more completeand rich in information than in any other group of vertebrates.This is due to the fact that the massive bones of mammals,and in particular their teeth, which provide most informationon both the relationship and feeding adaptation of a taxon, areparticularly well suited to be preserved in fossil deposits. Dueto this factor, the fossil record of mammals is perhaps the mostcomplete among the vertebrates. Also, during the late Ceno-zoic, Neogene, and Quaternary, the fossil record of somemammalian groups (such as rodents, insectivores, and ungu-lates) is so rich that the phylogeny of many clades can be tracedin surprisingly great detail by the respective fossil record. Forthe same reason, some of these fossils (e.g., voles in the Qua-ternary period) are the most important terrestrial index fossilsand are of key significance not only for local biostratigraphiesand precise dating of the late Cenozoic deposits, but also forlarge-scale paleobiogeography and even for intercontinentalcorrelations. The late Cenozoic period is characterized bygradually increasing effects of climatic oscillations, includingrepeated periods of cold and dry climate—glacials—followedby the evolution of grass and the treeless grassland country.Many clades of mammals responded to these changes and pro-duced the extreme specialists in food resources of the glacialhabitats, such as mammoths, woolly rhinos, lemmings, cavebears, and cave lions.

The most diversified animalsThere are about 4,600 species of mammals. This is a rel-

atively small number compared to the 9,600 species of birdsor 35,000 fish species and almost nothing in comparison toabout 100,000 species of mollusks or some 10,000,000 speciesof crustaceans and insects. Even such groups as extant rep-tiles (with 6,000 species) and frogs (with about 5,200 species)are more diversified at the species level. Nevertheless, in diversity of body sizes, locomotory types, habitat adaptations,or feeding strategies, the mammals greatly exceed all that iscommon in other classes.



Only birds and arthropods may approach such variety.However, at least in diversity of body size, the mammalsclearly surpass even them. The body mass of the largest ex-tant terrestial mammal—the African elephant Loxodontaafricana— with shoulder height of 11.5 ft (3.5 m), reaches to6.6 tons (6,000 kg). The extinct rhinocerotid Baluchitheriumwas about 18 ft (5.5 m) and 20 tons (18,000 kg), respectively.The largest animal to ever appear—the blue whale (Bal-aenoptera musculus)—with up to 98 ft (30 m) in length, reaches220 tons (200,000 kg). In contrast to dinosaurs or elesmo-branchians, which also produced quite large forms, the aver-age mammal is a small animal the size of a rat, and the smallestmammals such as a pygmy white-toothed shrew (Suncus etrus-cus) or Kitti’s hog-nosed bat (Craseonycteris thonglongyai) havea body length of just 1.2–1.6 in (3–4 cm) and weigh only 0.05-0.07 oz (1.5–2 g).

Mammals colonized almost all habitats and regions on theEarth. They now feed on flying insects hundreds of metersabove the ground; jump through foliage in the canopy of atropical forest; graze in lowland savannas and high mountainalpine meadows; hunt for fish under the ice cover of arcticseas; burrow the underground labyrinths to feed on diverseplant roots, bulbs, or insects; cruise the world’s oceans, ordive there to depths of 1.8 mi (3 km) in the hunt for giantsquid. Some even sit by a computer and write articles likethis.

About 4,600 species of mammals are arranged in approxi-mately 1,300 genera, 135 families, and 25 orders. Rodents with1,820 species, 426 genera and 29 families are far the largestorder, while in contrast, 8 orders include less than 10 species,and four of them are even monotypic (Microbiotheria, Noto-ryctemorphia, Tubulidentata, Dermoptera). Although inter-relationship among individual orders is still the subject of avivid debate, three major clades of mammals are quite clear:monotremes (2 families, 3 genera, 3 species), marsupials (7 or-ders, 16 families, 78 genera and 280 spp.), and eutherian orplacentals (17 orders, 117 families, 1,220 genera, 4,300 spp.),the latter two clades are together denoted as Theria.

The essential differences among the three major clades ofmammals are in mode of their reproduction and patterns ofembryonic development. Monotremes (platypus and echid-nas), restricted to the Australian region, show only little dif-ference from their ancestral amniote conditions. They delivereggs rich in yolk, and incubate them for 10 to 11 days. Younghatch from the egg in a manner similar to birds. Monotremesalso retain the reptile conditions in the morphology of the re-productive system: the ovary is large and short oviducts comevia paired uteri to a broad vagina, which opens with the uri-nary bladder and rectum into a common cloaca. Except formonotremes, all mammals are viviparous with intrauterineembryonic development and have quite small eggs, poor inyolk (particularly in eutherians).

There are essential differences between marsupials andeutherians in the earliest stages of embryonic development,as well as in many other characteristics. The reproductivetract in a female marsupial is bifurcated (with two vaginas),and also the tip of the penis in a male marsupial is bifurcated.Many marsupials have a marsupium, the abdominal pouch

for rearing young, supported with the marsupial epipubicbones that are present in both sexes. The marsupial in-trauterine development is very short and the embryo is at-tached to the uterine endometrium by the choriovitelline(yolk) placenta that lacks the villi penetrating deeper in thewall of uterus (except in bandicoots). The marsupial new-borns are very small and little developed, and birth is non-traumatic. In contrast, the lactation period is much longerthan in eutherians (only bats and some primates have pro-portionally long lactation periods). Nevertheless, themother’s total investment by the time of weaning young isroughly equal in both clades, but its distribution is different.The marsupial strategy is much less stressful for a motherand allows an extensive variation in tactics of reproduction.For instance, in the kangaroo, a mother can have three gen-erations of young at one time: the young baby returning todrink low-protein but high-fat milk, the embryo-like youngattached to a nipple nourished with high-protein but low-fatmilk, and an embryo in the uterus for which development isdelayed until the second-stage young is released.

A key agent of eutherian reproduction is the highly spe-cialized organ supporting a prolonged embryonic develop-ment—the chorioallantoic placenta. Eutherian newborns arelarge and despite considerable variation over particular clades,are potentially capable of an independent life soon after birth.Large herbivores such as elephants, perissodactyls, and artio-dactyls, as well as cetaceans, sirenians, hyraxes, and some pri-mates, deliver single, fully developed newborns with openeyes, ears, and even the ability to walk immediately after birth.Such a newborn is called precocial in contrast to the altricialnewborns of insectivores, bats, rodents, or carnivores, whichare hairless, blind, and fully dependent on intensive mother’scare. Both developmental strategies may, of course, appearwithin one clade as in lagomorphs (large litters and altricialyoung in a rabbit versus small litters and precocial young ina hare). Variations in reproductive strategies are closely in-terconnected with numerous behavioral adaptations and adap-tations in social organization and population dynamics, all ofwhich contribute significantly to mammalian diversity.

Recent molecular data strongly support the essential roleof geographic factors in phylogenetic history and in taxo-nomic diversity of mammals. Thus, there is very strong sup-port for the African clade Afrotheria, which is composed ofthe tenrecid and potamogalid insectivores, golden moles,macroscelids, aardvark, hyraxes, proboscideans, and sirenia.Also, the extensive covergences between Australian marsupi-als and particular eutherian clades and/or the paleontologicaldata on mammalian evolution on particular continents sug-gest that on each continent, the adaptive radiation producedquite similar life forms: small to medium sized insectivores,rodent-like herbivores, large herbivores, and their predators.The niche of large herbivores seems to be particularly attrac-tive (at least 18 different clades attained it) but at the sametime, it is perhaps the most dangerous (13 of them are extinct).

Nearly one fourth of all mammals fly. This is pertinent toa number of species, the number of genera, and perhaps forthe number of individuals as well. Bats, with more than 1,000species in 265 genera, are the most common mammals in



many tropical and subtropical habitats. Mostly active at night,bats hunt for various kinds of aerial prey (a basic strategy ofthe clade) or feed on fruit, nectar, or pollen. Some bats feedon frogs, reptiles, or other bats, and in the tropics of SouthAmerica, the total biomass of bats exceeds that of all othermammals. Several Old World bats, such as false vampires,feed on small vertebrates, while others feed on fish pluckedfrom the water surface. Frugivorous and nectarivorous batsare the essential agents for pollination and seed dispersal ofmany tropical plants, including banana and mango. Bats areoften very social and form large colonies, including the largestassemblies known in mammals, such as the maternity colonyof about 36 million Mexican free-tailed bats in Bracken Cavein Texas.

However, most of the extant mammals (nearly a half ofall genera) maintain the basic mammalian niche. They areterrestrial, mostly nocturnal or crepuscular, and forage fordifferent food resources that are available on the ground. Ina tropical forest this may be seeds and fruits falling downfrom the canopy and the invertebrate or vertebrate animalsfeeding on them. In the subtropics and temperate regions,the significance of this habitat increases as the soil surfacebecomes the most significant crossroads of ecosystem me-tabolism. In a temperate ecosystem, the soil is the major con-veyer of the energetic flow and an important source of free

energy that is available in a variety of food resources. It is nowonder that in the temperate regions terrestrial mammalsform more than half of the local mammalian taxa (while it isone third or less in the tropics) and that their densities ex-ceed those of all remaining mammalian species. Among themwe find the groups that are the most progressive and mostrapidly diversifying clades of the extant mammals (such asshrews or muroid rodents). Terrestrial mammals are, as arule, quite small animals, and are often the r-strategists. Theyhave short life spans, large litter sizes, several litters per year,and rapidly attain sexual maturity, sometimes even a fewweeks after birth. Most of the small ground mammals dig un-derground burrows for resting. This reduces not only the riskof predation, but due to stable microclimatic conditions ofthe underground habitat, it also reduces metabolic stress byambient temperature or by daytime changes in other weatherconditions. Many mammals also tend to spend a consider-able part of their active life underground, including foodgathering. Those that combine it with terrestrial foraging arecalled semifossorial—most of the 57 genera of semifossorialmammals are rodents. Those that are entirely adapted to anunderground way of life and often do not come above groundat all are called fossorial. The fossorial adaptations, whichmake them all quite similar in general appearance, are seenin 35 genera of 13 different clades and evolved convergentlyin all major geographic regions (Australian marsupial mole,



The manatee (Trichechus manatus) is primarily herbivorous. Here a mother nurses her young. (Photo by Jeff Foott. Bruce Coleman, Inc. Repro-duced by permission.)

Holoarctic true moles, the African golden moles, and 10groups of rodents in Holoarctic, Ethiopian, and Neotropicalregions). Compared to their relatives, the fossorial mammalsare all the K-strategists, some with pronounced tendenciesto complex organization (mole rats).

The mammals also evolved another way to inhabit terres-trial habitats. It is called scansorial adaptation and is typicalof large herbivores with an enormous locomotory capacity,enabling them to exploit distant patches of optimal resourcesand react actively to seasonal changes in them. In many in-stances these are social animals living in large nomadic herds.Kangaroos, the large macropodid marsupials of Australia, ex-hibit this scansorial adaptation. They move rapidly aroundtheir terrestrial habitat by hopping bipedally on their long,powerful hind legs, using their long tails for balance.

Locomotory modes are entirely different in the 156 gen-era of mammals that forage in arboreal habitats. Essentiallyarboricolous are primates, dermopterans, and tree shrews, aswell as many marsupials, rodents, bats, and some edentates andcarnivores. Typical for most of them are long forelimbs and along tail, often prehensile. Other arboricolous mammals havea haired membrane between their legs, enabling them to glidebetween tree trunks. The mammals equipped for such glidingflight include flying lemurs (Dermoptera), several groups ofrodents (flying squirels, African anomalurids), and three gen-era of marsupials.

Roughly 107 genera and 170 species are aquatic or semi-aquatic and mostly fish-eating. Three grades can be distin-guished here: (1) terrestrial animals that enter aquatic habitatsonly temporarily for feeding only (African otter shrews, OldWorld water shrews, desmans, water opossum, more cladesof rodents, including large rodents such as beaver and capy-bara, and several clades of carnivores, particularly otters); (2)marine mammals that spend most of their life in aquatic habi-tats but come to shore for breeding (all pinnipedian carni-vores, such as seals, sea lions and walruses, and sea otters);and (3) the exclusively aquatic mammals incapable of surviv-ing outside of the aquatic environment—sirenians andcetaceans. The latter group is quite diversified, and includes78 species in 41 genera that can be subdivided into two ma-jor clades: Mysticeti, whales that filter marine plankton withbaleen plates hanging from roof of the mouth cavity, andOdontoceti, dolphins and toothed whales, which echolocateand feed on fish or squid (including the giant deep-sea ar-chiteuthids as in the sperm whale). Cetaceans evolved varioussophisticated adapatations for prolonged diving into deepoceanic waters, such very economic ways of gas exchange thatinclude a reduced heart rate during diving and more oxygen-binding hemoglobin and myoglobin in blood than in othermammals. Cetaceans, though closely related to non-ruminantartiodactyls and recently included together with them in acommon order, Cetartiodactyla, diverge from the commonpicture of “what is a mammal?” perhaps most of all.

The extreme diversity in feeding adaptations is among themost prominent characteristics of mammals. Feeding special-izations such as grazing grass or herbal foliage, palynovory(eating pollen of plants), myrmecophagy (specialized feedingon ants and termites), and sanguivory (feeding on blood of

birds and mammals, in five species of true vampires) are notknown from any other vertebrates. At the same time, all thefeeding adaptations occurring in other vertebrate clades oc-cur also among mammals.

In all mammals, the efficiency of a feeding specializationdepends upon the appropriate morphological, physiological,and behavioral adaptations. First, it concerns the design of theteeth and dentition. The generalized heterodont dentition andthe tribosphenic molar teeth designed for an insectivorous diet(as retained in various marsupials, insectivores, tree shrews,prosimian primates, and bats) can be easily modified to thecarnivorous diet. A carnivorous diet further demands enlarg-ing the size of the canines and arrangements that increase theshearing effect of cheek teeth. A lower position of the jaw jointincreases the powered action of temporal muscles at the ante-rior part of dentition, and in extremely specialized carnivoressuch as cats, the dentition is then considerably shortened andreduced except for canines and the carnasial cheek teeth (thelast upper premolar and the first lower molar, generally thelargest teeth of carnivores). There is no problem with digest-ing the tissues of vertebrates and thus no special arrangementsof the alimentary tract are needed.

In contrast, herbivores, especially those specialized in feed-ing on green plant mass, require a modified jaw design. Thiskind of food is everywhere and easily accessible as a rule, butit is extremely difficult to digest for several reasons. One isthat this diet is very poor in nutritive content and must beconsumed in very large volumes; it must also be broken downmechanically into small particles. Hence, the dentition isoverburdened by wear of occluding teeth and their abrasionwith hard plant tissue. Efficiency of feeding depends directlyon the design of the tooth crown, on the size of total area foreffective occlusion, and the efficiency of masticatory action.Large teeth with flat surfaces and high crowns resistant to in-tensive wear are particularly required.

The major problem with a diet of plants is that mammals(as well as other animals) do not produce enzymes that breakdown cellulose. They must rely on symbiotic microorganismsresiding in their alimentary tract, evolve an appropriate hous-ing for them, and ensure a sufficient time for proper food fer-mentation. The mammals evolved several ways to fulfill theserequirements. One is the foregut fermentation (digastric di-gestion system) characteristic of ruminant artiodactyls (bovids,cervids), kangaroos, and colobus monkeys. The fermentationchambers are situated in spacious folds of the stomach; fromthese fermentation chambers the partially fermented food canbe regurgitated and chewed during a rest period, which alsoprolongs the movement of food through the gut. The mi-croorganisms detoxify alkaloids by which growing plants de-fend against herbivores prior to digestion, but are very sensitiveto tanins contained in the dry plant tissues. The foregut fer-menters avoid dry plants but feed on growing parts of plants,selectively cut with the tongue and lips (ruminants even lackthe upper incisors).

Perissodactyls, rodents, lagomorphs, hyraxes, and elephantsevolved hindgut fermentation (monogastric digestion system),where fermenting microorganisms are housed in the caecumand large intestine. Food is not regurgitated and all mechan-



ical disintegration of food must be performed at one mastica-tion event. Except for caeca, the passage of food through thegut is almost twice as fast as in the foregut fermenters. Hindgutfermenters can survive on a very low-quality food, if it is avail-able in large quantity. They can effectively separate the taninsand dry plant mass, both of which decrease the efficiency ofthe foregut fermenting. Correspondingly, the foregut andhindgut fermenters prefer different parts of plants and canboth forage in the same habitats without any actual competi-tion. The latter are, of course, under more intense pressure toevolve further adaptations to compensate for the energetic dis-advantages of their digestion. One of them is extreme en-largement of caeca (as in rodents); another is considerableincrease in the height of cheek teeth (maximized in severalclades of lagomorphs and rodents, in which cheek teeth arehypselodont, or permanently growing). The third way is anincrease in body size. This enlarges the length of the alimen-tary tract and prolongs the passage of food through it, whileat the same time it reduces the rate of metabolism. The be-havioral reduction of metabolic rate by a general decrease ofactivity level as in foliovore (leaf-eating) sloths or the koalaproduces the same results.

The gradual increase in body size is a feature of mam-malian evolutionary dynamics, as it was repeatedly demon-strated by the fossil record of many clades. This is seen inmost eutherians (not only in the herbivorous clades), but ismuch less apparent in marsupials. It seems that in additionto the common factors promoting a larger body size (a re-duced basal metabolic rate, smaller ratio of surface area tobody mass, and smaller heat transfer with ambient environ-ment), something else comes into play, something which hasto do with the essential differences of both the clades. Thisis the enormous stress of the eutherian way of reproduction.While intrauterine development is short and a litter weightis less than 1% of the mother body mass in a marsupial, theeutherian female must endure a very long pregnancy and thetraumatic birth of a litter that in small eutherians such as in-sectivores, rodents, or bats, may weigh 50% of the mother’sbody mass.

With enlarging body size, the stress of pregnancy and par-turition is reduced as the size of a newborn is relativelysmaller (compared with 3-5% of a mother’s mass in largemammals and 10-20% in smaller mammals). With a reduc-tion of litter size, it further provides a chance to refine thefemale investment and deliver fully developed precocialyoung, as in ungulates or cetaceans. This aspect of mam-malian adaptation and diversity should remind us that per-haps the ways in which a female does manage the stress ofeutherian reproduction (the factor that magnified thestrength of selection pressure) became the most influentialsource of viability of our clade.

Neighbors, competitors, and friendsMammals and humans have been the closest relatives and

nearest neighbors throughout the entire history of hu-mankind. Mammals contribute essentially to our diet and we

keep billions of domesticated mammals solely for that pur-pose. Hunting mammals for protein-rich meat became an es-sential background factor in human evolution several millionyears ago. More recently, the discovery of how to get suchanimal protein in another way started the Neolithic revolu-tion some 10,000 years ago. The symbiotic coexistence withherds of large herbivores—which included taking part intheir reproduction and consuming their milk and offspring—ensured the energetic base for a considerable increase in thehuman population of that time and became one of the mostimportant developments in human history. Moreover, theother essential component of the Neolithic revolution maybe related to mammals. Feeding on seeds of grass and stor-ing them in the form of a seasonal food reserve could hardlyhave been discovered without inspiration from the steppeharvesting mouse (Mus spicilegus) and its huge corn stores orkurgans, containing up to 110 lb (50 kg) of corn. The the-ory that humans borrowed the idea of grain storage from amouse is supported by the fact that the storage pits of Ne-olithic people were exact copies of the mouse kurgans. Mam-mals have even been engaged in the industrial andtechnological revolutions. Prior to the steam engine and fora long time in parallel with it, draft animals such as oxen,donkeys, and horses were a predominant source of power notonly for agriculture, transport, and trade, but also for min-ing and early industry. Indeed, our civilization arose on thebacks of an endless row of draft mammals.

At the same time, many wild mammals have been con-sidered dangerous enemies of humans: predators, sources ofepizootic infections, or competitors for the prey monopo-lized by humans. Many mammals were killed for these rea-sons, while some were killed merely because we could killthem. As a result, many species of wild mammal were dras-tically reduced in numbers leading to their local or globalextinctions. The case of the giant sea cow (Hydrodamalis stel-leri) is particularly illustrative here, but the situation withmany other large mammals, including whales, is not muchdifferent. The introduction of cats, rats, rabbits, and othercommensal species to regions colonized by humans has badlyimpacted the native fauna many times, and the industrialpollution and other impacts of recent economic activity actin a similar way on a global scale. About 20% of extant mam-malian species may be endangered by extinction, mostly dueto the destruction of tropical forest.

However, since the Paleolithic, humans also have keptmammals as pets and companions. Even now, the small car-nivores or rodents that share our houses bring us a great dealof pleasure from physical and mental contact with somethingthat, despite its apparent differences, can communicate withus and provide what often is not available from our humanneighbors—spontaneous interest and heartfelt love. Contactwith a pet mammal may remind us of something that is al-most forgotten in the modern age: that humans are not theexclusive inhabitants of this planet, and that learning from theanimals may teach us something essential about the true na-ture of the world and the deep nature of human beings aswell.





ResourcesBooksAnderson, S., and J. K. Jones, Jr., eds. Orders and Families of

Recent Mammals of the World. New York: John Wiley andSons, 1984.

Austin, C. R., and R. V. Short, eds. Reproduction in Mammals.Vols. 1, 2, 3 and 4. Cambridge, UK: Cambridge UniversityPress, 1972.

Chivers, R. E., and P. Lange. The Digestive System in Mammals:Food, Form and Function. New York: Cambridge UniversityPress, 1994.

Eisenberg, J. F. The Mammalian Radiations, an Analysis ofTrends in Evolution, Adaptation, and Behavior. Chicago:University of Chicago Press, 1981.

Feldhammer, G. A., L. C. Drickamer, A. H. Vessey, and J. F.Merritt. Mammalogy. Adaptations, Diversity, and Ecology.Boston: McGraw Hill, 1999.

Griffith, M.The Biology of Monotremes. New York: AcademicPress, 1978.

Kardong, K. V. Vertebrates. Comparative Anatomy, Function,Evolution. Dubuque, Iowa: William C. Brown Publishers,1995.

Kowalski, K. Mammals: an Outline of Theriology. Warsaw,Poland: PWN, 1976.

Kunz, T. H., ed. Ecology of Bats. New York: Plenum Press,1982.

Lillegraven, J. A., Z. Kielan-Jaworowska, and W. A. Clemens,eds. Mesozoic Mammals: The First Two-Thirds of MammalianHistory. Berkeley: University of California Press, 1979.

Macdonald, D., ed. The Encyclopedia of Mammals. New York:Facts on File Publications, 1984.

Neuweiler, G. Biologie der Fledermaeuse. Stuttgart-New York:Georg Thieme Verlag, 1993.

Nowak, R. M. Walker´s Mammals of the World. 5th ed.Baltimore and London: Johns Hopkins University Press,1991.

Pivetau, J., ed. Traité de paléontologie, Tome VII Mammiferes.Paris: Masson et Cie, 1958.

Pough, F. H., J. B. Heiser, and W. N. McFarland. VertebrateLife. 4th ed. London: Prentice Hall Int., 1996.

Ridgway, S. H., and R. Harrison, eds. Handbook of MarineMammals. New York: Academic Press, 1985.

Savage, R. J. G., and M. R. Long. Mammal Evolution, anIllustrated Guide. New York: Facts on File Publications,1986.

Starck, D. Lehrbuch der Speziellen Zoologie. Band II: Wirbeltiere.5. Teil: Säugetiere. Jena-Stuttgart-New York: Gustav FischerVerlag, 1995.

Szalay, F. S., M. J. Novacek, and M. C. McKenna, eds.Mammalian Phylogeny. New York: Springer-Verlag, 1992.

Thenius, E. Phylogenie der Mammalia. Stammesgeschichte derSäugetiere (Einschliesslich der Hominiden). Berlin: Walter deGruyter and Co, 1969.

Vaughan, T. A., J. M. Ryan, and N. Czaplewski. Mammalogy.4th ed. Belmont, CA: Brooks Cole, 1999.

Wilson, D. E., and D. M. Reeder, eds. Mammal Species of theWorld: a Taxonomic and Geographic Reference. 2nd ed.Washington, D.C.: Smithonian Institution Press, 1993.

Young, J. Z. The Life of Mammals. 2nd ed. Oxford: ClaredonPress, 1975.

OtherUniversity of Michigan Museum of Zoology. Animal Diversity

Web. <http://animaldiversity.ummz.umich.edu>

Animal Info—Information on Rare, Threatened andEndangered Mammals. <http://www.animalinfo.org>

BIOSIS. <http://www.biosis.org.uk>

Links of Interest in Mammalogy. <http://www.il-st-acad-sci.org/mamalink.html>

The American Society of Mammalogists. <http://www.mammalsociety.org>

Smithsonian National Museum of Natural History. <http://www.nmnh.si.edu/vert/mammals>

World Wildlife Fund. <http://www.worldwildlife.org>

Ivan Horácek, PhD

During the latter half of the Ice Ages, the Pleistocene, inresponse to the slow pulsation of continental glaciers, thereevolved unique large mammals—man included. In their biol-ogy and appearance they diverged from anything seen earlierin the long Tertiary, the Age of Mammals. They did notmerely adapt to the increasingly seasonal climates and greaterextremes in temperature and moisture. Rather, in the sheerexuberance and breadth of their adaptations, they reflectedboth the new ecological riches and soil fertility generated byglacial actions as well as the long successions of biomes theyevolved in prior to life in the face of glaciers. Their noveltyresides in novel opportunities and seasonal resource abun-dance in the environments shaped by these glaciers. It is thiswhich gave rise to their oddness in shape and biological ec-centricity, which shaped many into giants, and which usheredin the Age of Man.

The Pleistocene epoch is the latter half of the Ice Ages andis characterized by major continental glaciations, which be-gan about two million years ago. There have been about 20of these. Minor glacial events building up to the major glacialperiods characterized the latter part of the Pliocene epoch.The evolutionary journey of mammalian families that suc-ceeded in adapting to the cold north began in moist tropicalforests. It proceeded stepwise into tropical savanna, dry grass-lands at low latitudes, and then either into the deserts or intotemperate zones at higher latitudes and altitudes. From thereit continued into the cold, but fertile environments formedthrough glacial action and on into the most inhospitable ofcold environments: the tundra, the alpine, and the polardeserts. Such extreme environments developed with the greatcontinental glaciations that cycled at roughly 100,000 year in-tervals between cold glacial and warm interglacial phases.There was massive ice buildup in the Northern Hemisphereduring the former with a concomitant shrinkage of oceansand severe drop in ocean shorelines. During inter-glacialsthere was glacial melt-off, followed by a re-flooding of theocean to roughly the current level. We live today towards theend of an interglacial period. The well-differentiated latitu-dinal climatic zones we take for granted are a characteristicof the Ice Ages we live in; during the preceding Tertiary pe-riod there were tropical forests in what are today polar deserts.Consequently, adaptations to the extreme environments ofthe Ice Ages are relatively new.

Species adapted to cold and glacial conditions are new be-cause the environments generated by huge continental glac-iers became extensive only in the Pleistocene. That was new.Habitats formed by small mountain glacier are, of course, old,but large glaciations allowed the spread of what once wererare ecosystems. Also new is a sharp climatic gradient betweenequator and poles, generating latitudinal successions of bio-mes with increasing seasonality, terminating in landscapes ofglaciers and snow.

Glaciers are “rock-eaters” that grind rock into fine pow-der. This ground rock is spewed out by the glacier with meltwater and flows away from glacial margins as silt. When theseasonal glacial melting declines and the freshly deposited siltdries under the sun’s rays, it turns to fine dust which the windsblowing off the glaciers carry far, far away. Glacial times aredusty times. In the ice cores from Greenland glaciers, theglacial periods are characterized by their dust deposits. Thiswind-born dust is called by the German term “loess.” Theecological significance of glacial dust lies first and foremostin its fertility. Loess has high pH levels. Where it falls day af-ter day it forms into the fertile loess-steppe. Silt and loess aredeposited in lakes and deltas. After the lakes drain, there re-main fertile deep-soils deposits. These Pleistocene loess andsilt deposits in Eurasia and North America, as well as the on-going deposition of glacier-ground silt along major rivers suchas the Nile, Mekong, or Yellow River, are not merely today’sgrain baskets, but the very foundations of great civilizations.The silt and loess deposits form rich virgin soils, unleachedand undepleted of their soluble mineral wealth. These young,fertile soils foster rich plant growth wherever there is sun-shine and moisture.

Glaciers generate their own climates. They foster kata-batic, that is, warm winds blowing away from the glacier. Onthe melt-off edges they foster clear skies and sunshine. Westill see such climates along the ice fronts of the large moun-tain glaciations in the western Yukon and Alaska, along withabundant, diverse, and productive flora and fauna. Glaciersare not hostile to life.

Along these ice fronts we also see that when melt-waterretreats, lenses of alkali mineral salts form in the silt depres-sions due to evaporation. These “saltlicks,” composed largelyof sulfate salts, are avidly visited by large herbivores and


• • • • •

Ice Age giants

carnivores. The inorganic sulfur is converted in the gut bybacteria into sulfur bearing amino acids, cysteine and me-thionine, the primary amino acids for the growth of connec-tive tissues, body hair, hooves, claws, horns, and antlers. Saltlicks are avidly visited by lactating females and by all duringthe shedding and re-growth of a new coat of hair. They areessential for the growth of luxurious hair patterns and hugehorns and antlers. These “evaporite lenses” are covered bymore and more loess, becoming part of deep loess deposits.When water cuts through such deposits forming steep loesscliffs, these evaporates attract big game which gradually digdeep holes into loess cliffs.

The Pleistocene loess steppe is a haven for large grazersdue to its fertility. It has been called the “mammoth steppe”based on remains of woolly mammoth associated with it, aswell as an “Artemisia steppe” based on the fact that manyspecies of sage thrive here. This fertile steppe was also hometo wild horses, long-horned bison, camels, reindeer, saiga an-telopes, giant deer, and wapiti, as well as wolves, hyenas, li-ons, saber-toothed cats of two species, and several species ofbears. We may also call it the “periglacial” environment. Itwas extensive during glaciations. During the interglacial warmperiods, without the fertilizing effect of glacial silt and loess,the acid tundra, alpine, polar deserts, and boreal forest were

prevalent. Thus the development of diverse cold environ-ments, some greatly affected by glacial actions and seasonallyquite productive, invited the colonization by new types ofmammals able to cope with the biological riches and the cli-matic hardships.

The evolutionary progression towards Ice Age giants be-gins in the tropical forests with old, primitive parent speciesthat are, invariably, defenders of resource territories. Theyare recognizable as such by their weapons, which are special-ized for injurious combat: long, sharp canines or dagger-like,short horns. Property defense is based on expelling intrudersby inflicting painful injuries that also expose the intruder togreater risk of predation. Both males and females may bearmed and aggressive. They escape predators by taking ad-vantage of the vegetation for hiding or climbing and are ex-cellent jumpers that can cross high hurdles.

In the subsequent savanna species the “selfish herd” be-comes prominent as a primary security adaptation against pre-dation. This is associated with a dramatic switch in weaponsystems and mode of combat. That is, as individuals becomegregarious, they fight mainly via wrestling or head-butting,and minimize cuts to the body that could attract predators.They also evolve “sporting” modes of combat, sparring


Vol. 12: Mammals IIce Age giants

A skeletal comparison of a mastodon (left), modern elephant (center), and a woolly mammoth (right). (Photo by © David Worbel/Visuals Unlim-ited, Inc. Reproduced by permission.)

matches, in which there are no winners or losers. This is anovelty permitted by the new mode of combat. Moreover, rel-ative brain size increases, probably as a response to more com-plex social life. With adaptation to greater seasonality thespecies evolves the capacity to store surpluses from seasons ofabundance into seasons of scarcity. That is, individuals de-velop the capacity to store significant amounts of body fat.Their reproduction tracks the seasonal growth of plants,whether triggered by rain falls or seasonal temperatures.Their mode of locomotion changes to deal with the preda-tors of the open plains. They may evolve fast running, with-out giving up their ancestral ability to jump and hide inthickets.

As evolution progresses to the wide-open, grassy steppe,the plains-adapted species evolves capabilities to deal with lowtemperatures. Seasonal hair coats evolve. Because of the richseasonal growth of forage, individuals experienced a “vaca-tion” from want and from competition for food, evolving or-nate hair coats and luxurious secondary sexual organs. Thistended to go along with an increase in body size. Conse-quently, by the time species evolve in the cold environmentsclose to continental glaciers, they may be giants of their re-spective families as well as their most ornate, brainy, and fatmembers. We may call these new Ice Age species “grotesquegiants.” They are exemplified by woolly mammoth and woollyrhino, the giant stag or Irish elk, the moose, caribou or rein-deer, Przewalski’s horse, Bactrian camels, the extinct cave bearand giant short-faced bear, and extant Kodiak and polar bear,and, of course, our own species, Homo sapiens. Compared toother species within our family or tribe, we are indeed agrotesque Ice Age giant. Indeed, two human species adaptedto the glacial environments—the extinct Neanderthals andourselves. Note: every Ice Age giant is the product of suc-cessful adaptations to a succession of climates and environ-ments from tropical to arctic. Thus, they have a wide rangeof abilities built into their genomes.

The progression of species from primitive tropical formsto highly evolved arctic ones is well illustrated in the deerfamily, as is the varied nature of gigantism. Moreover, in thedeer family both subfamilies of deer follow the very same evo-lutionary pattern. In the Old World deer it begins with themuntjacs, small tropical deer from southern Asia with one ortwo pronged antlers and long upper combat canines. Theyare largely solitary territory-defenders that escape predatorsby rapid bounding (saltatorial running) followed by hiding indense cover. They are a very old group dating back to themid-Tertiary.

The second step in the evolutionary progression is repre-sented by species of tropical three-pronged deer. These areadapted to savanna, open wetlands and dry forest. They in-clude the highly gregarious axis deer, hog deer, rusa and sam-bar, as well as the swamp-adapted Eld’s deer and barasingha.These deer too are largely saltatorial runners and hiders, al-though they favor some open spaces. All have gregariousphases. All have antlers evolved for locking heads in wrestlingmatches. The upper canines are reduced or absent in adults.There is a split into more gregarious, showy meadow-speciesand more solitary forest-edge species. Although these species

differ in external appearance, nevertheless the identity of theirbody plan is readily apparent. The most gregarious forms haveprominent visual and vocal rutting displays.

The third step in the progression is represented by thefour-pronged deer. These are adapted to temperate climateswith a short, mild winter. Only two species are alive today,the fallow deer and the sika deer. Besides the increased com-plexity of antlers, there is a stronger differentiation and showi-ness of the rear pole. While the three-pronged deer have ashowy tail, the four-pronged deer have a rump patch in ad-dition. That of the sika deer consists of erectable hair thatmay be flared during alarm and flight. These are highly gre-garious deer with very showy vocal and visual displays.

The fourth step is represented by the five-pronged deer,all of which are primitive Asiatic subspecies of the red deer.They are found in regions with a distinctly harsher, colder,and more seasonal climate than the preceding four-prongeddeer, including in high mountain areas of central Asia. Thesedeer have progressed still further in the differentiation of theantlers, body markings, and rump patch and tail configura-tions. They are also much larger in body size. An evolu-tionarily advanced branch of red deer of some antiquity isthe European red deer. These feature complex five-prongedantlers, a neck mane, and larger and more colorful rumppatches.

The fifth step is represented by the six-pronged deer—theadvanced wapiti-like red deer of northeastern Asia and NorthAmerica. These are the ornate giants among Old World deer.They are much more cold-adapted and extend on both con-tinents beyond 60°N. They occupy periglacial and cold mon-tane, sub-alpine habitats, are more adapted to grazing thanother red deer, and have a body structure similar to plainsrunners. They have the largest rump patch and the shortesttail, the greatest sexual body color dimorphism, and the mostcomplex rutting vocalizations.


Ice Age giantsVol. 12: Mammals I

A life-sized woolly mammoth (Mammuthus primigenius) model. (Photoby Stephen J. Krasemann/Photo Researchers, Inc. Reproduced by per-mission.)

Of the same evolutionary rank as the six-pronged wapitiwas the now extinct giant stag or Irish elk. It grew the largestantlers ever and was also the most highly evolved runneramong the deer. Besides the enormous antlers, it had a humpover the shoulders, a tiny tail, and probably had prominentbody markings judging from cave paintings. It was a residentof the fertile glacial loess steppe and proglacial lakes. Of thesame evolutionary rank among the New World deer are themoose and the reindeer, both found in extremely cold cli-mates. In South America, in the cold southern pampas formedfrom loess, cold and plains adapted deer also evolved enor-mous reindeer-like antlers. They are now extinct.

Among the primates only the hominids leading to Nean-derthals and modern humans have gone through a similarmode of evolution. Humans are the only primate that hasbeen able to penetrate the severe ecological barriers posed bythe dry, treeless steppe. That is what allowed them to spreadinto and adapt to northern landscapes. To conquer the tree-less steppe humans had to be able to escape predation at nighton the ground. They had to provide continually high qualityfood to gestating and lactating females irrespective of the sea-son. Besides evolving the capacity to store very large quanti-ties of body fat, which became a prerequisite of reproduction,they developed means to access the subterranean vegetation

food stores encased in hard soils during the dry season. Theysuccessfully exploited the rich food resources of the inter-tidalzones and estuaries. Through hunting, they tapped into therich protein and fat stores of the large mammals on the steppe.As the capacity to kill large mammals evolved, weapons de-veloped that could stun opponents rendering them unable toretaliate, and cultural controls over killing augmented ancientbiological inhibitions. This is a profound adaptation, and isthus biologically unique and not found among other mam-mals. The distinction between doing what is right and wrongmust thus go back to the roots of tool and weapon use abouttwo million years ago.

Here there is the familiar, step-wise progression from atropical, forest-adapted, resource-defending ancestor similarto a chimp; to the savanna-adapted australopithecines whogreatly reduced the canines—ancestral weapons of territor-ial defense; to the steppe-adapted Homo erectus, our parentspecies. Homo erectus appeared at the beginning of the ma-jor glaciations almost two million years ago and spread intocold-temperate zones in Eurasia. Unlike the deer family,however, which skipped past deserts and went directly intoperiglacial, arctic, and alpine environments, human evolu-tion did not bypass deserts. It appears that with the massivePenultimate Glaciation beginning about 225,000 years ago,



The Moreno glacier rises 197 ft (60 m) above Lago Argentino’s water level in the National Park of Los Glaciares in Patagonia, Argentina. (Photoby Andre Jenny/Alamy Images. Reproduced by permission.)

which must have led to a maximum spread of deserts inAfrica, Homo sapiens arose out of Homo erectus by adapting todeserts. Two branches survived to invade and thrive in theperiglacial zones of Eurasia, the enigmatic Neanderthals andthe modern Homo sapiens species. We can thus trace the riseof a “grotesque giant” primate—ourselves. Man is large inbody, ornate in hair pattern and secondary sexual organs, andevolved a very large brain. Our reproductive biology dependson large stores of body fat, and we evolved highly sophisti-cated displays based on vocal and visual mimicry. Finally, wedeveloped an insatiable urge to artistically modify everythingwe were able to modify, which led to culture. We are thuspart and parcel of a greater evolutionary phenomenon, thatof the Ice Age giants.

However, the tropics too produce giants, representedamong primates by the larger of the great apes, foremost bythe gorilla and orangutan. Tropical giants built on primitivebody plans are, invariably, “coarse food” giants. Small-bod-ied mammals have a high metabolic rate per unit of masscompared to large-bodied mammals. This is related to thefact that to keep a constant core-temperature of about 98.6°F(37°C), which is essential for optimum enzyme functioning,small mammals must burn more fuel per unit of mass thando large mammals. Small mammals, because of the very largesurface to mass ratio, lose heat rapidly compared to largemammals with their low surface to mass ratio. Consequently,a mouse must metabolize per unit of mass much more foodthan an elephant. In order to maintain the high metabolicrate required the mouse needs to digest its food very rapidly,compared to an elephant, and must consequently select onlyrich, highly digestible food. Elephants, by comparison, canfeed on very coarse, fibrous food that may remain for sometime in their huge digestive tracts. The same principle ap-plies to tiny and gigantic tropical primates. The former feed

on buds, flowers, fruit, insects, etc., while the gorilla feedson fibrous, much more difficult to digest vegetation. Thechimpanzee, which stands so close to our ancestral origins,is somewhere in between large and small, and its omnivorousfood habits reflect that fact.

Ice Age giants reflect totally different conditions. Theirsize depends, in part, on the large seasonal surpluses of highquality food during spring and summer. Large size, however,is also an option in insuring minimum predation. That is, ahigh diversity and density of predators, such as those thatcharacterized North America’s Pleistocene, generates gigan-tic herbivores with highly specialized anti-predator adapta-tions. Conversely, herbivores stranded on a predator-freeoceanic island decline rapidly in size and loose their securityadaptations. They become highly vulnerable “island dwarfs”.Elephants for instance have shrunk to 3 ft (0.9 m) in shoul-der height on islands. Oddly enough, large body size is notrelated to ambient temperatures in winter, despite the factthat the surface to mass ratio declines with body size, favor-ing heat conservation. This is the principle behind the fa-mous, but invalid Bergmann’s Rule. Contrary to itspredictions, body size in the same species does not increasesteadily with latitude. Rather, body size increases only toabout 60-63°N and then reverses rapidly. That is, individu-als of a species beyond 63°N become rapidly smaller with lat-itude, some, such as caribou and musk oxen reaching dwarfproportions closest to the North Pole. Lowering the surfaceto mass ratio as an adaptation to cold is so inefficient that theabsolute metabolic costs of maintaining ballooning bodiesoutstrips whatever metabolic savings might be gained by thereduction in surface relative to mass. Bergmann’s Rule hasthus neither empirical nor theoretical validity. That preda-tion plays a role in driving up body size is not only indicatedby North America’s Pleistocene fauna of gigantic predatorsand prey or the biology of island dwarfs, but also by the factthat the largest deer, the Irish elk, was also the most highlyevolved runner among deer. For humans adapting to the drysteppe, hunting must have played a role in increasing bodysize, while periods of low food abundance favored a reduc-tion in body size.



Mountain goats (Oreamnos americanus) at a salt lick at Jasper Na-tional Park, Alberta, Canada. (Photo by © Raymond Gehman/Corbis.Reproduced by permission.)

A woolly mammoth (Mammuthus primigenius) skeleton. (Photo by JohnCancalosi/OKAPIA/Photo Researchers, Inc. Reproduced by permission.)

However, by far the most striking attributes of thegrotesque Ice Age giants are their showy, luxurious hair coats,secondary sexual organs and weapons, and their showy socialdisplays. The enormous tusks of mammoths and their longhair coats; the huge antlers of Irish elk, moose, and caribou aswell as their striking hair coats; the enormous horn-curls ofgiant sheep and bighorns; the beards, pantaloons, and hair-mops of bison and mountain goats; and the sharply discon-tinuous hair patterns and large fat-filled breast and buttocksin our species all stand in sharp contrast to comparable organsin tropical relatives. The great surpluses of food in summerdo permit the very costly storage of fat as well as horn, tusk,and antler growth. However, seasonally abundant food is onlya necessary condition for “luxury organs” to evolve, but not asufficient one. The rise of animal behavior as a science has in-formed us about these luxury organs. Their size, structure, anddistribution over the body, as well as the manner in which theyare displayed during social interactions indicate that they are

signaling structures evolved under sexual selection. Predationlurks in the background in some lineages, as illustrated by theway in which the gigantic antlers, horns, and tusks of north-ern plains-dwelling herbivores have evolved.

Envision a deer moving from tree and bush-studded sa-vanna to open grasslands void of cover. The more open thelandscape, the more difficult it is to hide a newborn ade-quately, particularly in already large-bodied species. Also, hid-ing becomes increasingly more risky, as visits by the femaleto suckle and clean her young are now quite readily observedas they are out in the open. Predators can thus find newbornsin the open terrain. The way out of this dilemma is to bearyoung that can quickly get to their legs and follow their moth-ers at high speed. This must be followed by nursing the youngwith milk exceptionally rich in fat and protein. Then theyoung are able to grow rapidly to “survivable size,” at whichendurance as well as speed can match that of adults. This,however, places a great burden on the female. In order to be



A man stands next to a life-sized woolly mammoth model in the Royal British Columbia Museum. (Photo by © Jonathan Blair/Corbis. Reproducedby permission.)

well developed and quick to rise and run, a newborn needs tobe born large in body and advanced in development. That,and the subsequent production of rich milk requires that thefemale not only have a high food intake, but take risks feed-ing in dangerous areas just to maintain a high food intake.She must also spare nutrients and energy from her bodygrowth in favor of that of her child. What father must sucha female choose so that her daughters may have the highestgenetic potential to grow large babies and rich milk?

Since the fathers contribute only their genes to the wel-fare of their children, they must—somehow—advertise theirsuccess at foraging and escaping predators. In the case of deer,any energy and nutrients ingested above the need of the bodyfor maintenance and growth are automatically diverted intoantler growth. Therefore, the better a male is at finding highquality food, the better its antler growth and the larger itsantlers. However, high quality, uncontested food may be ininsecure areas favoring predators. Therefore, the larger theantlers the more daring the male and the more able it is atdetecting and escaping predators. The symmetry of the antlersis also a factor. Symmetry is a proxy for health. Therefore,

the female should choose as a father for her daughters a malewith very large, symmetrical antlers. If so, then the larger theantlers, the more males ought to advertise with their antlersduring courtship. Therefore, the larger the antlers of aspecies, the larger and more advanced the newborn, the richerthe milk, the better the parents are at high-speed running,and the more males flout their antlers in courtship. All ofthese expected correlations are found.

What antlers do for deer, horns or tusks and elaborate haircoats do for other species that are associated with wide-open,cold, but productive Ice Age landscapes. These luxury organsevolve in relation to the security of newborns. Therefore, se-vere predation pressures ought to enhance the evolution ofthese luxury organs in plains dwellers. It is not surprising,therefore, that in Pleistocene North America, the large num-ber of specialized predator species are associated not only withvery large-bodied prey, but also with body structures in preythat enable speedy running, as well as immense tusks in mam-moth, enormous horns in long-horned bison, and huge, com-plex antlers in the stag-moose and caribou.

In the hominid line leading to our species, the highly de-veloped luxury organs are also related to reproduction andsexual selection. Not only need females have an exceptionallyhigh body fat content for mammals before conception andpregnancy is possible, but the female’s “hour glass” distribu-



A saber-toothed cat (Smilodon californicus) skeleton taken from theRancho La Brea tar pits. (Photo by Tom McHugh/Photo Researchers,Inc. Reproduced by permission.)

The grizzly bear (Ursus arctos), standing in a meadow at StrawberryValley, Utah, USA, evolved a thick coat to deal with its cold environ-ment close to continental glaciers. (Photo by © Galen Rowell/Corbis.Reproduced by permission.)

tion of fat over her body signals her fertility and health. Inaddition to breast and buttocks, which are shaped largelythrough triglyceride (fat) deposits, the density and quality ofhair acts as sexual signals. Hair is formed from sulfur-bearingamino acids such as cysteine and methionine, which are rareand cannot be readily synthesized in our bodies in adequateamounts. Luxurious hair growth, formed from rare aminoacids signals, therefore, biological success as it is based on theintake of high quality food. Our notion of beauty and gracerests in the first instance on symmetry of body features andfunction. Symmetry is a function of good nutrition. Our brainconsists largely of fat. Its superior function depends on a richand balanced intake of essential fatty acids. Even mother’smilk reflects this demand as, compared to other species, it isexceptionally rich in brain-building omega-3 and omega-6fatty acids. For superior growth and development, humansthus require omnivorous food sources fairly rich in fats thatcontain these essential fatty acids, such as the fat of wild game,fish, and seafood. In the Upper Paleolithic of Europe humansreach exceptional physical development and brain sizes; thearcheological record indicates that their food was primarilyreindeer and salmon. Neanderthal, the human super-predator,reached earlier comparable brain sizes living off the largest ofperiglacial herbivores, woolly mammoth, woolly rhino, giantdeer, horses, and steppe bison. The cerebral cortex is a tissue

of low growth priority. That is, it grows to maximum sizeonly under exceptionally favorable food intake, provided ofcourse that it is also well stimulated daily through an activesocial life and adventures.

There were many Ice Age giants in the periglacial envi-ronment: huge beavers; enormous bears such as the carnivo-rous short-faced bear of North America or the cave bear ofEurope or the current Kodiak brown bear and the polar bear.Northern cave-lions and cave-hyenas reached body sizes twicethe mass of their African relatives, as did the American Pleis-tocene cheetah compared to the African or Near East forms.And, of course, humans reached maximum body and brain di-mensions in the periglacial landscapes. Why then did theselarge-bodied forms not grow larger still? We get a glimpse ofthe answer for our own species by looking at what Nean-derthals did.

Neanderthals, exceptionally robust and powerful, with hugejoints in arms and legs and massive bones, approached us in height and were probably equal in body mass. As super-carnivores they specialized in the largest and hairiest herbi-vores, which were brought down apparently by one hunterskillfully tackling and attaching himself to the hairy exteriorof his prey, while a second hunter jumped in to disable or killthe distracted beast. The tackled beast, however, must have



A recreation of how Megantereon, a species of saber-toothed cat, may have looked. (Photo by Tom McHugh/Photo Researchers, Inc. Reproducedby permission.)

gone through some violent rodeo-like bucking and jumpingto dislodge the attached first hunter. Consequently, dislodgedhunters would have been catapulted through the air followedby harsh landings, often on frozen ground. Not too surpris-ingly, Neanderthal skeletons reveal frequent bone breaks andthe pattern of bone breaks resembles that of rodeo cowboys.Neanderthal hunters did not enjoy a long life expectancy, un-like the modern humans in the Upper Paleolithic that followedthem. A body size larger than that attained would have placedthe hunters at a disadvantage as it would have been more dif-ficult to hold on, while falling off would have generated harderimpacts and generated even more bone breaks. That is, as bodysize increases, it reduces mobility and acceleration, but in-creases muscular strength and impact force during a fall. Ifagility and acceleration are compromised at large body size,then the ability of hunters to evade attacks by large prey theyantagonized or wounded is compromised. Furthermore,should there be periods of food shortage that strike during thegrowth and development of an individual, then the smaller-bodied individual has a better chance of growing brain tissuethan a large individual. Small body size, while excelling atagility and acceleration, suffers from lower strength, maximumrunning speed, and endurance. Body mass is thus based on acompromise of factors that allow optimum performance in thetasks demanded by adaptation.

The evolutionary road to periglacial environments is vir-tually a one-way road to herbivores and omnivores. There ispractically no return of Ice Age species to habitats at lowerelevation and in more benign climates, with a few exceptions.Ice Age herbivores must be generalists that can deal with agreat diversity of seasonal temperatures and foraging condi-tions. They cannot compete against the food-specialists atlower elevations. These evolved to deal with the myriad ofchemical and structural defenses of plants against being eatenby herbivores. Cold climate vegetation, by comparison, ismuch less defended in large part because much of it may be

hidden under a long-lasting snow-blanket and unavailable forgrazing. Moreover, Ice Age species are exposed to fewer par-asites and pathogens than are species in warmer climates.Consequently, the diseases and parasites of more primitivewarm-climate species can be devastating to Ice Age mammals.The tropics in particular are characterized by an abundanceof microorganisms and parasites against which northernspecies have little or no immunity. Nevertheless, some specieshave succeeded in re-invading warm climates, humans in par-ticular. That humans from high latitudes do have significantproblems in the tropics is attested to by medical history.

With the rise of humans to ecological dominance their fel-low Ice Age giants did not fare well. Most went extinct, andthough their passing is shrouded in controversy, the weightof opinion points to humans as the cause of their extinction.Human capabilities improved sharply between 60,000 to40,000 years ago and the largest of the Ice Age giants beganto fade then. Massive extinctions of the megafauns followedthe last retreat of the glaciers. However, that was also a timeof great hardships for humans, followed by the rise of agri-culture, which brought some relief. Most of the Ice Age gi-ants must have become victims of very hungry and very ablehuman hunters.

The Ice Ages generated new, increasingly seasonal and cli-matically harsh environments from the equator to the poles.Each Ice Age giant is thus the product of successive adapta-tions to ever more challenging landscapes. Each has the genomeof ancestors that were highly successful in the tropics, in thesavanna, in the steppe, in deserts, in cold-temperate zones aswell as in the climatically extreme periglacial, arctic, and alpinehabitats. They were thus constructed genetically with more andmore abilities to cope with more and more challenges. Thatmay be the reason why in the Pleistocene, and not earlier, thereevolved the most uniquely gifted Ice Age giant of all: the mod-ern human.



ResourcesBooksBonnichsen, Robson, and Karen L. Turnmire, eds. Ice Age

People of North America. Corvallis: Oregon State UniversityPress. 1999.

Geist, Valerius. Life Strategies, Human Evolution, EnvironmentalDesign. New York: Springer Verlag, 1978.

Geist, Valerius. Deer of the World. Mechanicsburg, PA:Stackpole Books. 1998.

Guthrie, Dale R. Frozen Fauna of the Mammoth Steppe.Chicago: University of Chicago Press. 1990.

Martin, Paul S., and Richard G. Klein. Quaternary Extinctions.Tucson: University of Arizona Press, 1984.

Nilsson, Tage. The Pleistocene. Stuttgart: Ferdinand EmkeVerlag, 1983.

Valerius Geist, PhD

IntroductionTraditional studies of evolutionary relationships among

living organisms (phylogenetics) relied predominantly oncomparisons of morphological characters. However, phylo-genetic studies have increasingly benefited from additional in-puts from molecular genetics. Reconstruction of evolutionaryrelationships among mammals provides a prime example ofsuch benefits, and the broad outlines of the phylogenetic treeof mammals have now been convincingly established. For in-stance, it has proved possible to identify four major clusters(superorders) of placental mammals: (1) Afrotheria—ele-phants, manatees, hyraxes, tenrecs, golden moles, elephantshrews, and the aardvark; (2) Xenarthra—sloths, anteaters,and armadillos; (3) Euarchontoglires—rodents, lagomorphs,primates, dermopterans, and tree shrews; (4) Laurasiatheria—artiodactyls (including cetaceans), perissodactyls, carnivores,pangolins, bats, and most insectivores (“eulipotyphlans”:hedgehogs, shrews, and moles).

All phylogenetic reconstructions based on molecular datadepend on studies of the genetic material DNA or of pro-teins, whose synthesis is governed by individual DNA se-quences. The primary components of the double-strandedDNA molecule are nucleotide bases, sugar groups, and phos-phate groups. There are four nucleotide bases (adenine, cy-tosine, guanine, and thymine), and specific chemical bondsbetween pairs of these (adenine with thymine; cytosine withguanine) provide the backbone for DNA’s double helix struc-ture. These specific bonds between pairs of bases also ensurethat, if one strand is separated, the missing strand will be faith-fully replicated. Because the basic unit in the double-strandedDNA molecule is hence a bonded pair of bases (one base ineach strand), the length of a DNA sequence is measured inbase pairs (bp). The sequence of nucleotide bases in the DNAmolecule provides the basis for protein synthesis through thegenetic code, with a group of three bases (“triplet”) in theDNA sequence corresponding to one amino acid in the pro-tein sequence. Protein sequences hence depend directly uponDNA sequences, and a score of different amino acids are com-bined into chains of specific composition through translationof sequences of nucleotide bases in DNA, assisted by twokinds of RNA (messenger RNA and transfer RNAs). How-ever, the original simple concept of “one gene, one protein”has needed modification. One major reason for this is that a

DNA sequence corresponding to a particular protein se-quence often contains non-coding regions (introns) betweenthe coding regions (exons). Only the exons are ultimately re-flected in the amino acid sequence of the corresponding pro-tein. Furthermore, the products of individual DNA sequencescan be spliced together to produce a protein.

Both DNA sequences and protein sequences are particu-larly suitable for phylogenetic reconstruction because theyconsist of relatively simple components arranged in linear se-ries (nucleotide bases and amino acids, respectively) that canbe easily compared between species. Initially, comparisons be-tween species were based on laborious step-by-step determi-nation of the amino acid sequences of proteins, as there wasno straightforward technique for studying DNA sequencesthemselves. The first phylogenetic trees derived from mole-cular genetics were therefore based on amino acid sequencesof proteins, and relatively few species were included in com-parisons because of the time-consuming procedure involvedin protein sequencing. At first, it was also technically very dif-ficult to determine DNA sequences. However, a major break-through came with development of the capacity for generatinglarge quantities of individual DNA sequences through ampli-fication using the polymerase chain reaction (PCR). Thisopened the way to relatively straightforward and rapid directdetermination of DNA sequences, and heralded the transi-tion from studies of gene products (proteins) to studies of thegenes themselves (DNA sequences). In fact, because it becameeasier and faster to determine DNA sequences directly, a pro-tein sequence is now commonly inferred from the DNA se-quence of the corresponding gene rather than from sequencingof the protein.

It is important to note that there are two different sets ofgenetic material (genomes) in mammalian cells, as in animalsgenerally. The primary genome is contained in the chromo-somes in the nucleus (nuclear DNA), but each mitochondrionin the cell cytoplasm also contains a number of copies of aseparate small genome (mitochondrial DNA). As several mi-tochondria are present in each cell, there are numerous copiesof the mitochondrial genome, whereas there is only one nu-clear genome per cell. However, the basic structure of DNAis the same for nuclear DNA (nDNA) and mitochondrialDNA (mtDNA), with chains of nucleotide bases, althoughmtDNA is organized in a ring whereas nDNA exists as lin-


• • • • •

Contributions of molecular genetics to phylogenetics

ear sequences within chromosomes. The mitochondrion is arespiratory power plant found in all organisms with a cell nu-cleus (eukaryotes). It is, in fact, derived from a free-living bac-terium that took up residence in the cell cytoplasm in anancestral eukaryote more than a billion years ago, in anarrangement that was of mutual benefit (symbiosis). Origi-nally, the mitochondrial genome contained many more genesthan are now present in mammals, whose mitichondria retainonly a small number of protein-coding genes that are all con-nected with respiration.

Reconstruction of phylogenetic treesRegardless of whether morphological or molecular data are

analyzed, reconstruction of phylogenetic relationships be-tween species depends on interpretation of shared similari-ties. In principle, it is relatively easy to survey similaritiesbetween species for individual characters. This task is partic-ularly straightforward with molecular data because the indi-vidual components at defined positions in sequences of DNA(nucleotide bases) or proteins (amino acids) are relatively sim-ple and directly comparable. Furthermore, because the pri-mary process underlying evolutionary change is pointmutation (random replacement of one nucleotide base by an-other in a DNA sequence), comparison of DNA sequencesdirectly reveals basic evolutionary steps. Most changes inDNA sequences lead to changes in corresponding protein se-quences, but there is some degree of redundancy in the ge-netic code, because up to six different triplet sequences ofnucleotides can correspond to a single amino acid. For thisreason, about 25% of point mutations in DNA are “silent”and do not lead to a change in protein sequences. Such re-dundancy applies particularly to the third base position inDNA triplets.

Analysis of similarities between species to construct phy-logenetic trees is more difficult than it seems at first sight. Inthe first place, similarities can arise independently throughconvergent evolution at any time after the separation betweentwo lineages. For instance, rodent-like incisor teeth have de-veloped several times independently during the evolution ofmammals. But reconstruction of the relationships betweenspecies depends on exclusion of convergent similarities andidentification of homologous similarities that have been in-herited through descent from a common ancestor. In the caseof morphological characters, it is often possible to identifyconvergent similarities directly because development of sim-ilar characters is typically driven by similar functional re-quirements. For example, rodent-like incisors develop inresponse to selection pressure for gnawing behavior. For com-plex morphological characters, convergent similarity is typi-cally only superficial because it merely needs to meet aparticular functional requirement. Hence, detailed examina-tion of such characters commonly reveals fundamental dif-ferences. With incisors, for instance, a rodent-like pattern candevelop without altering the structure of enamel that charac-terizes a particular group of mammals. With molecular char-acters, by contrast, each type of nucleotide base or amino acidshows complete chemical identity, so it is impossible to de-termine from direct examination whether convergent evolu-tion has occurred. Instead, convergence in molecular

evolution is recognizable only from the phylogenetic tree af-ter it has been generated on the assumption that the tree re-quiring the smallest total amount of change (the mostparsimonious solution) is the correct one. Because there areso few possibilities for evolutionary change at the molecularlevel (4 nucleotide bases; 20 amino acids), convergent evolu-tion is very common. As a rule, about half of the similaritiesbetween species recorded in any tree that is generated musthave arisen independently through convergent evolution.Convergence is therefore a major problem with any tree de-rived from molecular data, particularly because functional as-pects of changes in nucleotide bases and amino acids are rarelyconsidered (thus excluding any possibility of identifying func-tional convergence). Moreover, precisely because there are sofew possibilities for change in DNA base sequences, repeatedpoint mutation at a given site will mask previous changes andcan easily lead to chance return to the original condition. Al-though it is now standard practice to make a global correc-tion for repeated mutation at a given site in molecular trees,it is virtually impossible to reconstruct the mutational historyof individual sites if repeated change has occurred.

In fact, there is a further problem in interpreting similar-ities for the reconstruction of phylogenetic trees. Even if it ispossible to exclude certain cases of convergent evolution, asis often true with complex morphological similarities, an im-portant distinction remains with respect to inherited homol-ogous similarities. For any group of species considered, aparticular set of features will be present in the initial commonancestor. If such a primitive feature is retained as a homolo-gous similarity in any descendants, it reveals nothing about


Contributions of molecular genetics to phylogeneticsVol. 12: Mammals I

Due to DNA evidence, cetaceans like the bottlenosed dolphin (Tur-siops truncatus) have been linked to hippopotamuses (Hippopota-mus amphibius). (Photo by © Tom Brakefield/Corbis. Reproduced bypermission.)

branching relationships within the tree. The only homolo-gous features that provide information about branchingwithin a tree are novel features that arise at some point andare subsequently retained by descendants as shared derivedsimilarities. This crucial distinction between primitive and de-rived homologous similarities is particularly relevant if thereare marked differences between lineages in the rate of evolu-tionary change. For instance, members of two slowly evolv-ing lineages can retain many primitive similarities and wouldthus be grouped together on grounds of overall homologoussimilarity if no special attempt were made to identify derivedsimilarities. It was once believed that rates of change are rea-sonably constant at the molecular level, thus reducing theneed to distinguish between primitive and derived homolo-gous similarities, but the availability of large molecular datasets has revealed that there can be major differences in ratesbetween lineages.

In conclusion, the increasing availability of molecular datahas provided a major benefit for the reconstruction of phylo-genetic trees. The large numbers of directly comparable char-acters included in molecular data sets provide a highlyinformative basis for quantitative comparisons. On the otherhand, because the methods used do not explicitly tackle thecrucial distinction between convergent, primitive, and derived

similarities, the results are subject to error. Accordingly, ifthere is a conflict between a tree based on molecular data andone based on morphological data, it should not be automat-ically assumed that the latter is necessarily incorrect. After all,there is quite often a similar conflict between trees based ontwo different molecular data sets. The safest procedure istherefore to take a balanced approach that gives due consid-eration to both morphological and molecular evidence. Com-bined studies that do precisely this with comprehensive datasets are becoming increasingly common.

Mitochondrial DNAThe ring-shaped, double-stranded mtDNA molecule has

the same basic structure in all mammals. It is approximately16,500 bp in length and contains coding sequences for 13genes, 2 ribosomal RNA molecules (12S and 16S), and 22transfer RNA molecules, together with a non-coding con-trol region (D-loop). In contrast to nuclear genes, there areno introns in mtDNA. Furthermore, mtDNA differs fromnDNA in another crucial respect that simplifies analysis ofits evolution. In mammals, mtDNA is exclusively or almostexclusively inherited maternally (i.e., from the mother), andthere is no recombination of genes when the mitochondrion


Vol. 12: Mammals IContributions of molecular genetics to phylogenetics

The red panda (Ailurus fulgens) is very hard to classify, but was placed with the other Ursidae species due to similar DNA. (Photo by Tim Davis/PhotoResearchers, Inc. Reproduced by permission.)

divides. Phylogenetic reconstructions may be based on partof mtDNA (e.g. using an individual gene, such as cy-tochrome b) or on the entire molecule, and many completemtDNA sequences are now available for analysis. Overall,mtDNA tends to accumulate changes more rapidly thannDNA (about five times faster overall), and for this reasonit is more suitable for analyses of relatively recent changesin the evolutionary tree of mammals. Because rapidly evolv-ing DNA sequences become saturated with changes at anearlier stage, they are unsuitable for probing early parts ofthe tree. However, there are differences in rate of evolutionbetween individual parts of the mtDNA molecule, so it ispossible to select regions that are suitable for particularstages of mammalian evolution. Mitochondrial DNA se-quences can be crudely divided into those that evolve rela-tively rapidly, hence being useful for comparisons of quiteclosely related species (e.g. control region, ATPase gene)and those that evolve relatively slowly, thus being useful forcomparisons of more distantly related species (e.g. riboso-mal genes, tRNA genes, cytochrome b gene). For example,golden moles are of presumed African origin. This impliesthat there was an extensive African radiation from a singlecommon ancestor that gave rise to ecologically divergentadaptive types. DNA studies suggest that the base of this ra-diation occurred during Africa’s isolation in the Cretaceousperiod before land connections were developed with Europein the early Cenozoic era. In another study, scientists ex-amined the mtDNA of 654 domestic dogs, looking for vari-ations. They were trying to determine whether dogs weredomesticated in one or several places, and then attemptingto identify the place and time that such domestication oc-curred. Their results show that our common domestic dogpopulation originated from at least five female wolf lines.They went on to speculate that while the archaeologicalrecord cannot define the number of geographical origins ortheir locations, their own data indicate a single origin of do-mestic dogs in East Asia some 15,000 to 40,000 years ago.

Nuclear DNASurprisingly, only a small fraction of the nuclear DNA

(nDNA) contained in chromosomes consists of gene se-quences that code for production of proteins. It is estimatedthat less than 5% of human DNA consists of genes that codefor approximately 30,000 different proteins. Much of the rest(95%) has no well-established function and is often labeled“junk DNA”. A large part of this DNA consists of repetitivesequences that in some cases are present as many thousandsof copies. Such DNA sequences that have been inserted intothe genome are known as “retroposons”, but their functionremains essentially unknown.

Reconstruction of phylogenetic relationships using DNAsequences that code for protein sequences (or using the pro-tein sequences themselves) hence involves only a small partof the nuclear genome. Nevertheless, there are many differ-ent nuclear genes available for analysis, and the sequence dataset for mammals is increasing rapidly. Certainly, the poten-tial total sequence information that can be obtained from the30,000 protein-coding genes in the nuclear genome is vastlygreater than that provided by the 13 protein-coding genes inthe mitochondrial genome. As a general rule, the reliabilityof phylogenetic trees generated with molecular data increasesboth with the number of species included in comparisons andwith the number of DNA sequences analyzed. However, thereare some unresolved problems with the methods currentlyemployed for reconstruction of trees using molecular data.Furthermore, there are practical limits to the quantity of datathat can be effectively analyzed, so various short-cuts are nec-essary.

In addition to protein-coding DNA sequences, some cat-egories of retroposons (inserted sequences) are becoming in-creasingly useful as tools for reconstructing phylogeneticrelationships. This is particularly true of inserted sequencesknown as short interspersed nuclear elements (SINEs) andlong interspersed nuclear elements (LINEs), respectively.



The giant anteater (Myrmecophaga tridactyla) belongs to the Xenarthracluster of placental mammals. (Photo by © Tom Brakefield/Corbis. Re-produced by permission.)

The African elephant (Loxodonta africana) has been grouped into theAfrotheria cluster of placental mammals. (Photo by © Craig Lovell/Corbis. Reproduced by permission.)

Because SINEs and LINEs apparently arise at random andoccur widely throughout the genome, they are almost idealderived characters. Given the vast array of DNA sequencesin the nuclear genome, the probability of convergent evolu-tion in the insertion of a SINE or LINE is exceedingly small.It is highly improbable that one of these sequences will beinserted at exactly the same site in the genome in two sepa-rate lineages. Secondly, because each insertion is a uniqueevent that is unlikely to be reversed, SINEs and LINEs pro-vide excellent markers for the recognition of groups of re-lated organisms descended from ancestors possessing specificinsertions. A very good example of the use of such evidencecomes from discussion of the relationships between cetaceans(dolphins and whales) and artiodactyls (even-toed hoofedmammals). It has been accepted for some time that cetaceansare in some way related to artiodactyls. However, accumu-lating evidence from DNA sequences (both mtDNA andnDNA) indicated that cetaceans are, in fact, specifically re-lated to hippopotamuses and thus nested within the artio-dactyl group. This interpretation conflicts with the standardinterpretation of the morphological evidence, according to

which cetaceans constitute the sister-group to all artiodactyls.Certain fossil forms (mesonychians) that were regarded asrelatives of whales and dolphins lacked a characteristic dou-ble-pulley adaptation of the ankle joint that is found in allartiodactyls (and was most probably present in their commonancestor). It had therefore been concluded that cetaceansbranched away before the emergence of ancestral artio-dactyls. This conflict of evidence was convincingly resolvedby the discovery that cetaceans and hippopotamuses share anumber of SINEs that are not found in any other mammals.Subsequently, early whale fossils possessing the typical ar-tiodactyl ankle joint were discovered. Hence, it is now wellestablished that cetaceans and hippopotamuses are sister-groups and that mesonychians are not direct relatives of thecetaceans after all.

Gene duplicationStudies of the evolution of DNA and protein sequences

have generally concentrated on changes arising through pointmutations of individual nucleotide bases. Indeed, molecularevolution has often been portrayed essentially as the pro-gressive accumulation of point mutations in genes. However,evolution of DNA can also take place in other ways. One ofthe most important changes that can occur is tandem dupli-cation of genes. This arises through slippage during the repli-cation of DNA during cell division. Once a gene has beenduplicated, the way is open for divergent evolution of the orig-inal and its copy. Indeed, over long periods of evolutionarytime, gene duplication can occur repeatedly, such that quitelarge families of genes can result. A prime example is pro-vided by globin genes, which are thought to have arisen froman original single gene through repeated duplication. The he-moglobin molecule, which plays a vital role in respiration,consists of four globin chains. In the blood of adult humans,the hemoglobin molecule contains two alpha-chains and twobeta-chains. Sequence comparisons indicate that the beta-chain arose from the alpha-chain through an ancient dupli-cation. There are also special hemoglobins that aretemporarily present during the embryonic and fetal stages.Embryonic hemoglobin contains two epsilon-chains, while fe-tal hemoglobin contains two gamma chains. Both the epsilon-chains and the gamma chains also arose from the beta-chainthrough relatively recent duplications that took place duringthe evolutionary radiation of the placental mammals. This il-lustrates how gene duplication can provide an alternativeroute for the evolution of new functional properties of genes.

During the long history of evolution of living organismswith a cell nucleus containing chromosomes (eukaryotes),there have also been cases where the entire set of chromo-somes has been multiplied (ploidy), for example through dou-bling of their number. Once sex chromosomes becameestablished, as is the case with all living mammals (XX for fe-males and XY for males), such doubling of the entire set ofchromosomes became virtually impossible. Doubling of amale set of chromosomes (to XXYY) would result in the pres-ence of two X chromosomes, thus disrupting the normalprocess of sex determination in which males have only a sin-gle X chromosome. However, at an earlier stage of evolution,



Four phylogenetic mammal trees have been established. The branchLaurasiatheria includes carnivores such as the gray wolf (Canis lu-pus). (Photo by Tom Brakefield/Bruce Coleman, Inc. Reproduced bypermission.)

prior to the development of typical mammalian sex chromo-somes, multiplication of chromosome sets would still havebeen possible. Although the evidence is controversial, thereis a strong possibility that two successive duplications of theentire chromosome set took place during vertebrate evolu-tion leading up to the emergence of the mammals. For ex-ample, two successive doublings of an original set of 12chromosomes could have let to a set of 48 chromosomes,which is the modal condition found in placental mammals.Although duplications of an entire chromosome set can, ofcourse, be subsequently masked by secondary modificationsof individual chromosomes, quadrupling of the chromosomesprior to the emergence of the ancestral placental mammalsshould still be reflected in the presence of four copies of manyindividual genes. This does, indeed, seem to be the case formany sets of genes, such as the homeobox genes that play animportant part in development.

Duplication of individual genes or entire chromosomes infact poses an additional problem for reconstruction of phylo-genetic trees using molecular data sets. When a tree is basedon nucleotide sequences for any individual gene, care mustbe taken to ensure that it is really the same gene that is be-ing compared between species. If there are multiple copies ofa particular gene in the genome, there is always the dangerthat comparisons between species might involve differentcopies. A striking example of this danger is provided by mi-tochondrial genes. Although gene duplication has never beenrecorded within the mitochondrial genome, individual mito-chondrial genes have been repeatedly copied into the nucleargenome, where they generally remain functionless. Inadver-tent inclusion of such redundant nuclear copies in compar-isons of mitochondrial genes between species has led toserious errors in interpretation. For instance, a supposed mi-tochondrial gene sequence reported for a dinosaur turned outto be an aberrant nuclear copy of that sequence in humanDNA.

The molecular clockIn addition to permitting reconstruction of relationships

among species to generate a phylogenetic tree, molecular ge-netics can also yield valuable information with respect to thetimescale for that tree. With the very first reconstructionsconducted using molecular data, it was observed that the rateof change in amino acid sequences of particular proteins (andhence in the DNA sequences of the genes responsible) seemedto be relatively constant along different lineages. This led onto the notion of the “molecular clock”, according to whichthe degree of difference between DNA sequences or aminoacid sequences in any two species can provide an indicationof the time elapsed since their separation. However, it shouldbe noted that accumulating evidence has indicated that therate of molecular change is in fact quite variable. In the firstplace, it was obvious from the outset that some genes evolvefaster than others, and it was then shown that the overall rateof change in mtDNA is considerably greater than that innDNA. Moreover, it also became clear that rates of changediffer markedly even within individual genes. Some of thisvariation in rate of change within genes is to be expected. For



A mounted specimen of the now-extinct thylacine, or Tasmanian wolf(Thylacinus cynocephalus). (Photo by Tom McHugh/Photo Researchers,Inc. Reproduced by permission.)

The Euarchontoglires grouping of placental mammals is represented bymammals such as the woodchuck (Marmota monax). (Photo by © JohnConrad/Corbis. Reproduced by permission.)


whale

Cetartiodactyla

Laurasiatheria

Boreoeutheria

dolphin

PerissodactylaEuarchontoglires

hippo

Carnivora

Xenarthra

ruminant

Pholidota

Afrotheria

pig

Chiroptera

Marsupialia

llama

Eulipotyphla

rhino

Rodentia

tapir

Lagomorpha

horse

Dermoptera

cat

Scandentia

caniform

Primates

pangolin

Pilosa

flying fox

Cingulata

rousette fruit bat

Afrosoricida

rhinolophoid bat

Macroscelidea

phyllostomid microbat

Tubulidentata

free-tailed bat

Sirenia

hedgehog

Hyracoidea

shrew

Proboscidea

mole

mouse

rat

hystricid

caviomorph

sciurid

rabbit

pika

flying lemur

tree shrew

strepsirrhine

human

sloth

anteater

armadillo

tenrec

golden mole

s.e.elephant shrew

l.e.elephant shrew

aardvark

sirenian

hyrax

elephant

opossum

diprotodontian

Phylogeny of living placental mammals, based on a large molecular data set (16,397 base pairs) including 19 nuclear genes and 3 mitochondr-ial genes. Based on Murphy et al. 2001. (Illustration by GGS. Courtesy of Gale.)

example, “silent mutations” (notably in third base positions)and mutations within non-coding regions of genes (introns)are inherently likely to accumulate faster because they do notlead to changes in amino acid sequences and are hence notsubject to natural selection. In sum, it is now widely recog-nized that the concept of the “molecular clock” must be usedwith caution and that there may be quite marked differencesbetween lineages in the rates of molecular change. Methodshave therefore been developed to identify differences in ratesof change between lineages and to apply the notion of “localclocks”.

It should be noted that molecular data cannot directly yieldinformation on elapsed time and that phylogenetic trees pro-duced with such data always require calibration using infor-mation from the fossil record. Once a tree that is characterizedby relatively uniform rates of change has been calibrated withat least one date from the fossil record, it is possible to con-vert genetic distances into time differences. However, con-version of genetic distances into time differences requires thatgenetic change should be linearly related to time. This gen-erally seems to be the case once a global correction has beenmade for repeated mutation at a given site. Unfortunately,even if rates of molecular change along lineages are approx-imately linear (as is required for reliable application of a clockmodel), calibration dates derived from paleontological evi-dence introduce an additional source of error. The problemis that the fossil record can only yield a minimum date for thetime of emergence of a particular lineage, by taking the ageof the earliest known member of that lineage. The lineagemay have existed for some considerable period of time priorto the earliest known fossil representative. Clearly, the size ofthe gap between the actual date of emergence of a lineage andthe age of the earliest known representative of that lineagewill vary according to the quality of the fossil record. If thefossil record is relatively well documented, as is probably thecase with large-bodied hoofed mammals, the earliest knownfossil representative may be quite close to the time of origin.In other cases, however, use of the age of the earliest knownfossil to calibrate a phylogenetic tree may lead to consider-able underestimation of dates of divergence. For instance, theearliest known undoubted primates are about 55 million yearsold, but statistical modeling indicates that we have so far dis-covered less than 5% of extinct fossil primate species. Cor-rection for the numerous gaps in the primate fossil recordindicates that the common ancestor of living primates existedabout 85 million years ago (mya), rather than 60–65 mya asis commonly assumed. Molecular evolutionary phylogenetictrees have also been accurately determined for the commonchimpanzee, pygmy chimpanzee, gorilla, and orangutan.

Overall molecular trees for mammalsLarge-scale combined studies of nDNA and mtDNA have

yielded phylogenetic trees for mammals that generally fit the

conclusions derived from traditional morphological compar-isons, but also show some differences in detail. For instance,molecular data have generally confirmed that the monotremesbranched away first in the mammalian tree and that there wasa subsequent division between marsupials and placentals. In-terestingly, however, comparisons of complete mtDNA se-quences have suggested that the monotremes and marsupialsform a group separate from the placentals (Marsupiontia). Asthis aberrant result conflicts with other molecular evidence aswell as with a well-established body of morphological evi-dence, it probably reflects an artifact of some kind. Indeed, itis noteworthy that the main points of conflict between dif-ferent molecular trees involve relatively deep branches in themammalian tree, which are precisely the branches that haveposed the greatest challenges in morphological studies. Nev-ertheless, there is a gathering consensus from broad-basedmolecular studies that there are four major groups of placen-tal mammals (Afrotheria, Xenarthra, Euarchontoglires andLaurasiatheria). As there are a number of consistent novel fea-tures of these groups, some modifications of conclusions basedon morphological studies are undoubtedly required. For in-stance, the existence of the assemblage “Afrotheria” had notbeen identified from morphological comparisons and was firstrevealed by molecular studies. Moreover, it would seem thatthe order Insectivora is not only an artificial grouping of rel-atively primitive mammals (as has long been expected) but infact includes widely separate lineages that belong either inAfrotheria (tenrecs, golden moles) or in Laurasiatheria(hedgehogs, shrews, and moles).

Overall phylogenetic trees for mammals based on molec-ular data have been calibrated in a variety of ways, and a fairlyconsistent picture has emerged. This conflicts with the long-accepted interpretation, according to which the evolutionaryradiation of modern mammals did not begin until the di-nosaurs died out at the end of the Cretaceous, 65 mya. In-stead, it would seem that the four major groups of placentalmammals began to diverge over 100 mya and that many (ifnot all) modern orders of placental mammals had become es-tablished by the end of the Cretaceous. For instance, numer-ous lines of evidence indicate that primates diverged fromother placental mammals about 90 mya. This revised inter-pretation of the timing of mammalian evolution is significantnot only because it indicates that dinosaurs and early relativesof modern placental mammals were contemporaries, but alsobecause it suggests that continental drift may have played amajor part in the early evolution of mammals. Contrary tothe long-accepted interpretation that the evolutionary radia-tion of modern mammals began after the end of the Creta-ceous, the new interpretation based on molecular dataindicates that the early evolution of both placental mammalsand marsupials took place at a time when the southern su-percontinent Gondwana was undergoing active subdivision.As one outcome of this process, it seems that the endemicgroup Afrotheria became isolated in Africa.





ResourcesBooksAvise, J. C. Molecular Markers, Natural History and Evolution.

London: Chapman & Hall, 1994.

Easteal, Simon, C. Collett, and D. Betty. The MammalianMolecular Clock. Austin: Texas, R.G. Landes, 1995.

Gillespie, J. H. The Causes of Molecular Evolution. Oxford:Oxford University Press, 1992.

Givnish, T. I., and K. Sytsma. Molecular Evolution and AdaptiveRadiations. Cambridge: Cambridge University Press, 1997.

Hennig, W. Phylogenetic Systematics. (Reprint of 1966 edition witha foreword by Donn E. Rosen, Gareth Nelson, and ColinPatterson) Urbana: University of Illinois Press, 1979.

Hillis, David M., and Craig Moritz. Molecular Systematics.Sunderland: MA, Sinauer Associates, 1990.

Kimura, M. The Neutral Theory of Molecular Evolution.Cambridge: Cambridge University Press, 1983.

Lewin, Roger. Patterns in Evolution: The New Molecular View.San Francisco: W. H. Freeman, 1997.

Li, W.-H. Molecular Evolution. Sunderland: MA, SinauerAssociates, 1997.

Li, W.-H., and D. Graur. Fundamentals of Molecular Evolution.Sunderland: MA, Sinauer Associates, 1991.

Nei, M. Molecular Evolutionary Genetics. New York: ColumbiaUniversity Press, 1987.

Ohno, S. Evolution by Gene Duplication. Berlin: Springer Verlag,1970.

Scheffler, I. E. Mitochondria. New York: Wiley-Liss, 1999.

PeriodicalsAllard, Mark W., R. L. Honeycutt, and M. J. Novacek.

“Advances in higher level mammalian relationships.”Cladistics 15 (1999): 213–219.

Anderson, S., M. H. L. de Bruijn, A. R. Coulson, I. C. Eperon,F. Sanger, and I. G. Young. “Complete sequence of bovinemitochondrial DNA: Conserved features of the mammalianmitochondrial genome.” Journal of Molecular Biology 156(1982): 683–717.

Arnason, Ulfur, Anette Gullberg, S. Gratarsdottir, B. Ursing,and A. Janke. “The mitochondrial genome of the spermwhale and a new molecular reference for estimatingeutherian divergence dates.” Journal of Molecular Evolution50 (2000): 569–578.

Bromham, L., M. J. Phillips, and D. Penny. “Growing up withdinosaurs; molecular dates and the mammalian radiation.”Trends in Ecological Evolution 14 (1999): 113–118.

Cao, Y., J. Adachi, Axel Janke, Svante Pääbo, and M.Hasegawa. “Phylogenetic relationships among eutherianorders estimated from inferred sequences of mitochondrialproteins: instability of a tree based on a single gene.”Journal of Molecular Evolution 39 (1994): 519–527.

Gatesy, Y., C. Hayashi, M. A. Cronin, and P. Arctander.“Evidence from milk casein genes that cetaceans are closerelatives of hippopotamid artiodactyls.” Molecular Biology andEvolution 13 (1996): 954–963.

Gray, M. W. “Origin and evolution of mitochondrial DNA.”Annual Review of Cell Biology 5 (1989): 25–50.

Hedges, S. Blair, Patrick H. Parker, Charles G. Sibley, and S.Kumar. “Continental breakup and the ordinal diversificationof birds and mammals.” Nature 381 (1996): 226–229.

Janke, Axel, X. Xu, and U. Arnason. “The completemitochondrial genome of the wallaroo (Macropus robustus)and the phylogenetic relationship among Monotremata,Marsupialia and Eutheria.” Proceedings of the NationalAcademy of Sciences, USA 94 (1997): 1276-1281.

Kumar, Sudhir, and S. B. Hedges. “A molecular timescale forvertebrate evolution.” Nature 392 (1998): 917–920.

Li, W.-H., M. Gouy, P. M. Sharp, C. O’hUigin, and Y.-W.Yang. “Molecular phylogeny of Rodentia, Lagomorpha,Primates, Artiodactyla, and Carnivora and molecularclocks.” Proceedings of the National Academy of Sciences, USA87 (1990): 6703–6707.

Li, W.-H., M. Tanimura, and P. M. Sharp. “An evaluation ofthe molecular clock hypothesis using mammalian DNAsequences.” Journal of Molecular Evolution 25 (1987):330–432.

Madsen, Ole, et al. “Parallel adaptive radiations in two majorclades of placental mammals.” Nature 409 (2001): 610–614.

Miyamoto, M. M. “A congruence study of molecular andmorphological data for eutherian mammals.” MolecularPhylological Evolution 6 (1996): 373-390.

Murphy, William J., et al. “Molecular phylogenetics and theorigins of placental mammals.” Nature 409 (2001): 614–618.

Murphy, William J., et al. “Resolution of the early placentalmammal radiation using Bayesian phylogenetics.” Science294 (2001): 2348–2351.

Nikaido, M., A. P. Rooney, and N. Okada. “Phylogeneticrelationships among certartiodactyls based on insertions ofshort and long interspersed elements: Hippopotamuses arethe closest extant relatives of whales.” Proceedings of theNational Academy of Sciences, USA 96 (1999): 10261–10266.

Rambaut, A., and L. Bromham. “Estimating dates ofdivergence from molecular sequences.” Molecular BiologicalEvolution 15 (1998): 442–448.

Schmitz, Jürgen, Martina Ohme, and H. Zischler. “Thecomplete mitochondrial genome of Tupaia belangeri and thephylogenetic affiliation of Scandentia to other eutherianorders.” Molecular Biological Evolution 17 (2000): 1334–1343.

Shedlock, A. M., and N. Okada. “SINE insertions: powerfultools for molecular systematics.” BioEssays 22 (2000):148–160.

Shimamura, Mitsuru, et al. “Molecular evidence fromretroposons that whales form a clade within even-toedungulates.” Nature 388 (1997): 666–670.

Springer, Mark S., et al. “Endemic African mammals shake thephylogenetic tree.” Nature 388 (1997): 61–64.

Tavaré, Simon, Charles R. Marshall, Oliver Will, ChristopheSoligo, and R. D. Martin. “Using the fossil record toestimate the age of the last common ancestor of extantprimates.” Nature 416 (2002): 726–729.



ResourcesUrsing, B. M., and U. Arnason. “Analyses of mitochondrial

genomes strongly support a hippopotamus-whale clade.”Proceedings of the Royal Society, London B 265 (1998):2251–2255.

Waddell, P. J., Y. Cao, M. Hasegawa, and D. P. Mindell.“Assessing the Cretaceous superordinal divergence times

within birds and placental mammals by using wholemitochondrial protein sequences and an extended statisticalframework.” Systemic Biology 48 (1999): 119–137.

Robert D. Martin, PhD

IntroductionMammalian evolutionary history goes back 230 million

years. The earliest mammals occupied a nocturnal niche anddeveloped a suite of traits that allowed them to adapt to thecooler temperatures of the night. Mammals are endothermic(able to produce their own heat) and most are homeothermic(able to maintain their body temperature within a particularrange). Many mammalian structures and their functions areinvolved with maintaining body temperature, which requiresefficient generation and conservation of heat.

Modern mammals evolved from early mammal-like rep-tiles called therapsids, which had a mosaic of reptile and mam-malian traits. In defining what a mammal is, we must utilizecharacteristics that are preserved in the fossil record, whichare largely skeletal. When a transitional fossil species has amammal trait it is usually accompanied by a reptile trait. Con-sequently, there is controversy as to when the actual mam-mal-reptile division occurred.

The key identifier in mammalian fossils is found in thedentary-squamosal articulation because the mammalian lowerjaw (the mandible) is unique. It consists of two bones, thedentaries, which articulate directly with the cranium. This isthe key criterion that defines mammals. And there is a rela-tionship between the repitian jaw and the mammalian ear.The reptilian jaw consists of two bones, the articular and thequadrate. In mammals, these were modified to become themalleus and the incus bones of the ear, which, along with thestapes (called the columella in reptiles), form the auditory os-sicles in the mammalian skull. Thus, mammals have threebones in their middle ears (malleus, incus, and stapes), andreptiles have only one (the columella).

Living mammals also have many soft anatomy traits that fur-ther define them as mammals. For example, at some stage oftheir lives, all mammals have hair. (However, it has been sug-gested that the reptilian flying pterosaurs had fur, so we mustbe cautious about saying that hair is exclusive to mammals). Onthe other hand, mammary glands are unique to mammals amongthe living vertebrates. Another structure unique to mammals isthe respiratory diaphragm that separates the thoracic and ab-dominal cavities. Only mammals possess this structure as a mus-cle, whereas other vertebrates have either a membranousdiaphragm or no diaphragm at all. The mature red blood cellsof mammals are enucleated (without a nucleus), whereas the red

blood cells of other vertebrates contain a nucleus. The mam-malian heart differs from other vertebrates in that only the leftaortic arch is developed in adult mammals. In mammal brains,the neopallium (neocortex) is elaborated and expanded com-pared to reptile brains. Each of these unique mammal structuresare discussed in context in the rest of this entry.

Integumentary form and functionThe integumentary system is composed of the skin and its

accessory organs. The mammalian integument has many ofthe characteristics that we consider mammalian. Generallymammalian skin is thicker than the skin of other vertebratesbecause of its function in retarding heat and water loss. Theintegument consists of two major regions, the epidermis anddermis. Squamous cells are produced by a basal (or germina-tive) layer on the border of the epidermis and dermis. As cellsare produced at the basal layer they push the cells above themtoward the surface of the epidermis. As they move toward thesurface the squamous cells fill with the protein keratin andproduce the corneum, a tough waterproof layer of dead cellson the outermost layer of the epidermis. Epidermal cells arecontinuously shed and replaced as they serve as mechanicalprotection against environmental insults.

The dermis is mainly a supportive layer for the epidermisand binds it to underlying tissues. Blood vessels in the dermispass near the basal layer of the epidermis and provide the cellsof the avascular epidermis with nutrients. The dermis also con-tains muscle fibers, associated with hair follicles, and nervoustissue that provides assessment of the environment. A subcu-taneous layer lies below the dermis and is a site of adipose (fat)deposition, which serves as both insulation and energy storage.

Mammals have a number of skin glands that are found in noother vertebrate. Mammals have two types of coiled, tubularsweat glands, apocrine (or sudoriferous) and eccrine. Apocrinesweat glands are usually associated with a hair follicle, and se-crete the odorous component of sweat. Eccrine sweat glands se-crete sweat onto the surface of the skin to remove heat throughevaporative cooling. Most mammals have both these glands inthe foot pads. They are more widely distributed on a few mam-mals, including humans. Those species with a limited distribu-tion often use a supplementary method for cooling such aspanting by dogs or immersion into cool mud or water by mem-bers of the pig family. Some small mammals such as insectivores


• • • • •

Structure and function

and small rodents, bats, and aquatic mammals, do not experi-ence heat loading and therefore do not have sweat glands.

Most mammals also have sebaceous glands distributedwidely throughout the integument. Sebaceous glands consist ofspecialized groups of epithelial cells that produce an oily sub-stance, sebum, that keeps hair and skin pliable, waterproof, andsoft. These glands are usually associated with hair follicles. Insome marine mammals such as otters and sea lions sebum is es-pecially important in waterproofing the pelage and keeping coldwater from contacting the skin, thereby preventing heat loss.

Scent glands are odoriferous glands used for social inter-actions, territory marking, and defense. One type of secretionis a pheromone, which elicits a behavioral or physiological ef-fect on a conspecific (member of the same species). During

the breeding season it may advertise the sexual receptivity ofthe individual. Pheromones in the urine of some rodentspecies is even believed to induce estrus. Scent glands are usedto delineate territory (i.e., marking). The distribution of scentglands is highly variable; they may be located on the wrists(carpal glands), throat region, muzzle, the chest (sternalglands), on the head, or the back, but most commonly scentglands are found in the urogenital area (anal glands). Amongthe mustelids (weasel family including skunks and minks),modified anal glands are able to squirt a smelly irritant sev-eral feet (or meters) when the animal is threatened.

Ceruminous glands are the wax-producing glands locatedin the skin of the ear canal. They help to prevent the tym-panic membrane from drying out and losing its flexibility.Ceruminous glands are modified apocrine sweat glands.


Structure and functionVol. 12: Mammals I

Mammals have different tooth shapes for different functions. Herbivores typically have large, flattened teeth for chewing plants. Rodents’ ever-growing incisors are used for gnawing. Carnivores have teeth for holding and efficiently dismembering their prey. (Illustration by Jacqueline Mahannah)

molars

premolars

canine

incisorsUnspecialized(omnivore)

Grinding (herbivores)

Tearing (carnivores)

molars andpremolars withsharp cusps large

caninesbroad, ridgedmolars

Gnawing (rodents)

Continuouslygrowing incisors

Mammary glands (mammae) are also generally believed tobe modified apocrine sweat glands, although it has been sug-gested that they could have been derived from sebaceousglands. Mammae secrete milk that is used to feed the new-born mammal. The mammary glands in most mammals con-sist of a system of ducts that culminate in a nipple or teat.The one exception is found in the monotremes (egg-layingmammals). In monotremes, the mammary glands secrete milkonto hair associated with the glands and the hatchlings suckmilk from these hairs. The number and location of mammaeis variable among mammal species and is related to the nor-mal size of the litter. The fewest number of mammae is two,but up to 27 are found in some marsupials. Mammae are usu-ally on the ventral surface of placental mammals; in the mar-supials they may be located in the pouch.

Hair is often described as a unique mammalian character-istic that has no structural homologue in any other vertebrate.Its distribution varies from heavy, thick pelages (fur coats) onmany mammals to just a few sensory bristles (e.g., on the snoutof whales or seacows). Mammalian hair originates in the epi-dermis, although it grows out of a tubular follicle that pro-trudes into the dermis. Growth occurs by rapid replication ofcells in the follicle. As the shaft pushes toward the surface thecells fill with keratin and die. Each hair is composed of anouter scaly layer called the cuticle, a middle layer of densecells called the cortex, and (in most hair shafts) an inner layerof cuboidal cells called the medulla. Each hair is associatedwith a sebaceous gland and a muscle (called the arrector pili)that raises the hair. Raising hair serves as a threat signal insocial interactions but also increases insulation properties.The evolution of hair is part of the suite of adaptations thatenabled mammals to be active at night. It served to retardheat loss by insulating the body. There are two layers of hairthat form the pelage. The dense and soft underfur functionsprimarily as insulation by trapping a layer of air. The coarseand longer guard hair serves to shelter the underfur, keepingit dry in aquatic mammals, and to provide coloration.

Although the primary purpose of hair is insulation it hasassumed other roles in living mammals. Color in hair comesfrom the pigments melanin and phaedomelanin. The mainfunction of coloration appears to be camouflage, which helpsthe animal blend in with its surroundings. Mammals tend tohave pelage colors that match their environment. One exam-

ple of this is countershading. The pelage tends to be darkeron the top and sides of the animal and lighter below and un-derneath, which under normal lighting conditions functionsto obscure the form of the animal. In addition, there are var-ious patterns on the pelage. Patterns on predators such as atiger’s stripes (Panthera tigris) help to conceal the predator.Stripes found on prey tend to confuse predators. Eye spots lo-cated above the eyes (e.g., Masoala fork-marked lemurs[Phaner furcifer] or four-eyed possums) may divert attentionfrom the eye, confusing predators. Such patterns are called dis-ruptive coloration. Another functional pattern is the whiterump patch of the tail in mule deer (Odocioleus hemionus), whichmay serve as a silent alarm signal to conspecifics. But, whenthe tail is lowered, a predator whose eyes are fixed on the whitepatch might lose sight of the deer. Coloration may also iden-tify conspecifics in visually oriented species. Blue monkeys(Cercopithecus mitis) and red-tailed monkeys (Cercopithecus asca-nius) are sympatric (live in the same geographic location) andclosely related, but they normally do not mate. It is believedthat their distingushing facial patterns are the reason. Colorpatterns may also differ within a species. Often sexual dimor-phism is expressed in color differences between males and fe-males. Infants and juveniles may have different pelage colorsor patterns from adults. In monkeys—one of the most visuallyoriented species—pelage patterns on the face, rump, or tail areused to communicate with one another. Another function ofpelage patterns is that of warning potential enemies, e.g., thewhite stripe found on skunks might be a signal that it is wellarmed and can defend itself. Color changes can occur over amammal’s lifetime because hair, like skin, is replaced over time.Most mammals have two annual molts, usually correlated withthe seasons. Yet others, such as humans, have hairs that growto a particular length and then are shed. Some populations ofsnowshoe hares undergo three seaonal molts: a brownish-graysummer coat, a gray autumn coat, and a white winter coat.

Hair has undergone other modifications in addition tocolor. The guard hairs of some species have been modifiedfor specific functions. For example, spines (or quills) are en-larged stiff hairs that are used for defense. In North Ameri-can porcupines these quills have barbs that work their wayinto the flesh of an attacker. Vibrissae (or whiskers) are an-other modification of hair. These are supplied with nerves toprovide tactile (touch) sensory information. These hairs arecommonly found on the muzzles of many mammals such as


Vol. 12: Mammals IStructure and function

Mammal foot diversity: A. Hominid; B. Bat; C. Pinniped; D. Elephant; E. Equid; F. Odd-toed ungulate; G. Two-toed ungulate; H. Four-toed ungulate.(Illustration by Patricia Ferrer)

A C

B

D E F G H

arm (leg) bones

carpals (tarsals)

metapodials

phalanges

fat pad

hoof

cats and mice, but they can be found in other body locationsas well. For example, tactile hairs may be located on the wrists,above the eyes, or on the back of the neck. These hairs allowmammals to sense objects around them when low-light con-ditions do not allow them to see well.

Claws, nails, and hoovesThe distal ends of mammal digits possess keratinized

sheaths or plates that are epidermal derivatives forming claws,nails, or hooves. Only the members of the whale and sirenia(seacows) families lack these structures. Claws are usuallysharp, curved, and pointed. In many cases mammal claws are

very similar to the claws found in other vertebrates. A clawconsists of a dorsal plate called the unguis and a ventral platecalled the subunguis. The unguis is curved both in length andwidth and encloses the subunguis, which is connected to thedigital pad at the distal end of the digit. In addition to pro-tection, claws assist predator species, such as lions and tigers,in holding their prey. They provide traction for some arbo-real species (e.g., squirrels) when scampering on branches.Sloths have long curved claws that serve as hooks for hang-ing. Digging mammals, such as anteaters and moles, have longclaws that help them dig.

Nails are modified claws found on the first digit of somearboreal mammals and on all the digits of some primates.Nails cover only the dorsal part of digits. The unguis (calleda nail plate in human anatomy) is broad and flat, and the sub-unguis is vestigial. It has been suggested that nails evolved inprimates to prevent rolling and provide flat support for thelarge pad of tactile sensory tissue found on the underside ofthe digit. Thus nails allow both increased tactile perceptionand enhanced manipulative abilities. The Callitrichidae (smallmonkeys found in South and Central America) have second-arily evolved claws, which are not true claws because they arederived from the laterally compressed nails of their ancestors.Nails and claws may be found on the same mammal (e.g.,hyraxes).



Foot structure of mammals: plantigrade (bear); digitigrade (dog); un-guligrade (horse). (Illustration by Jacqueline Mahannah)

Plantigrade

Digitigrade

Unguligrade

calcaneum

calcaneum

calcaneum

metapodial

metapodial

metapodial

digits

digits

singledigit

Cross section of mammal skin. (Illustration by Patricia Ferrer)

epid

erm

isde

rmis

sweat gland

sweat duct

arrectorpilimuscle

hair follicle

sebaceous gland

fatvein

artery

hair

Hooves are constructed of a prominent unguis that curvesaround the digit and encloses the subunguis. The well-devel-oped unguis has lent its name to the group that have hooves:the ungulates (although this is not a true taxonomic group).For ungulates, the unguis is much harder than the subunguisand does not wear away as quickly, thus developing a sharpedge.

Horns and antlersHorns and antlers are found in the order Artiodactyla (cat-

tle, sheep, deer, giraffes, and their relatives). Several othertypes of mammals have similar head structures, but true horns,originating from the frontal bone of the skull and found onlyamong the Bovidae (cattle, antelopes, buffalo), consist of abony core enclosed by a tough keratinized epidermal cover-ing or sheath. True horns are not branched, although theymay be curved. Horns grow throughout the life of the animaland are used for defense, display, and intraspecies combat (e.g.,contests between males for mates). A variation of the true hornis the pronghorn, found on the North American pronghorn(Antilocapra americana) in the artiodactyl family Antilocapri-dae. A pronghorn branches and its epidermal sheath is shedon an annual basis; the sheath on a true horn is not shed.Antlers are found among the Cervidae (deer, caribou, moose,and their relatives). Mature antlers are entirely made of boneand are branched. They develop from buds covered by in-

tegument that is richly innervated and vascularized, called vel-vet. As the antlers grow the velvet dies and the animal usuallyrubs it off on tree trunks. Antlers are used for combat betweenmales for mates. After the breeding season they are shed andreplaced by a larger pair the next year; this continues until theyreach their full growth. The small bony horns of giraffes (Gi-raffa camelopardalis) originate from the anterior portion of theparietal bones. Because they do not arise from the frontal bonesthey are not considered true horns. Giraffe horns are coveredby furred skin and persist throughout life. Another type ofhorn is found on the rhinoceroses of the order Perissodactyla,the only living mammals outside the artiodactyls with a horn.The rhinoceros horn is centered over elongated nasal bones,but it lacks a bony core. It is a solid mass composed of dermalcells interspersed with tough epidermal cells.

Body design and skeletal systemAs endotherms, mammals require more energy than ec-

tothermic animals. Consequently, many mammal traitsevolved to conserve energy. This is particularly true of themammal skeleton. Mammals differ as a group from other liv-ing quadrupedal vertebrates in that their limbs are positioneddirectly below the body, allowing more energy-efficient lo-comotion. The lateral placement of the limbs on reptiles andamphibians requires them to spend considerable energykeeping their bodies lifted off of the ground while they un-



Gas exchange between the air and bloodstream takes place in the capillaries of the lungs’ alveoli. (Illustration by Wendy Baker)

Oxygen fromthe alveolidiffuses into thearterial blood andis circulated bythe heart

CO2

Carbon dioxide from the venous blood diffuses to the alveoli and is exhaled through the lungs

02

C02 and O2

exchange in the alveoli

CO2

02

dulate laterally (rather than moving straight forward as mam-mals do). The vertical limb placement in mammals also al-lows removal of size constraints so that mammals maybecome much larger than amphibians or reptiles. (The largeMesozoic reptiles actually had limbs placed under the bodyalso.) Another difference in the mammal skeleton is that itceases growth in the adult, saving metabolic energy. Mam-mal long bones grow from bands of cartilage positioned be-tween the diaphysis (shaft) and epiphyses (the ends). Thisallows permanent articulations between bones and formswell-established joints. The mammal skeleton has been sim-plified in that many bones have fused, decreasing the num-ber of growth surfaces overall, and saving metabolic energythat would be used for maintenance. An example is the mam-mal skull, which is more ossified and simpler than those ofother vertebrates. Bones that are fused in mammal skulls areseparated by cartilage in reptiles. Ossification provides moresurface area on bones with larger sites available for muscleattachments. Exceptions to many of these mammalian char-acteristics are found among the living monotremes. Somemammalogists actually believe that monotremes should beclassified as therapsid reptiles because they have laterallyplaced forelimbs and their skeletons contain separated bonesthat are fused in other mammals, and, like reptiles, they re-tain cervical ribs. Ribs in most mammals are attached to thevertebral column only in the thoracic region; reptiles have

ribs attached to cervical, thoracic, and lumbar vertebrae. Thisrib arrangement allows mammals to lie on their sides for rest-ing or to suckle their young.

The bones that make up the limbs in mammals are part ofthe appendicular skeleton. The forelimbs of mammals are at-tached to the pectoral girdle, consisting of a scapula and aclavicle (collar bone). The scapula is held in place by muscu-lature, which provides the high mobility important in manylocomotor modifications. The pectoral girdle articulates withthe axial skeleton (skull, vertebral column, thoracic cage) onlythrough sternal bones, which allows a large range of motionin the shoulder. The pelvic girdle supports the hind limbs andconsists of a coxal bone (the fusion of three different elementsfrom the reptile condition) that attaches to the axial skeletonat the sacrum.

Locomotor adaptationsThe musculoskeletal design of the mammalian body has

accomodated many diverse means of locomotion, not only interrestrial environments but also in aquatic and aerial niches.Many mammal species are capable of using several differentmeans of locomotion, but much of the body configuration isdetermined by the dominant mode of locomotion used by aparticular species.



Jaw and ear structure in mammals. Mammals have only one bone in the lower jaw, not several as reptiles do. However, the bones of the formerreptilian jaw are now part of the mammalian inner ear structure. (Illustration by Jacqueline Mahannah)

Early reptile Triassic mammal

Modern mammalMiddle ear bones

of modern mammal

Incus

Malleus

A B

CDentary

Angular

Ar ticular

Quadrate

Squamosal

Jugular

Stapes

Most mammals that are ambulatory (walking) do so on allfour limbs, i.e., they are quadrupedal. Most ambulators arepentadactyl (possessing five digits) and plantigrade (walkingon the soles, or plantar surface, of their feet). Pentadactyly isthe primitive condition in mammals, although many lineageshave reduced this number. Ambulators include bears and ba-boons. Some ambulators are large. As they approach a ton(0.9 tonne) in weight, adaptations for their large size are a ne-cessity. Such animals are said to be graviportal. They have arigid backbone and their limbs take on the appearance of acolumn with each element directly above the one below it.They retain all five digits in a pad that provides cushioning.Elephants are an example of a graviportal mammal. Elephantsare not able to run, instead they trot, increasing their speedby walking quickly.

Cursorial locomotion (running) is accomplished in diverseways. Among mammals there is a range of adaptations andabilities for this way of moving. Many cursors are digitigrade,i.e., their metacarpals and metatarsals are permanently raisedabove the substrate with only the phalanges in contact withthe ground. Often the metacarpals and metatarsals are elon-gated and the number of digits reduced. For example, in

equids (horses), the leg is supported on a single central digitof their mesaxonic foot. Other mammals, such as deer andhyenas, have legs with a paraxonic foot with two toes con-tacting the ground. Some mammals have one set of limbs thatare paraxonic and another set that are mesaxonic.

A number of characteristics allow the generation of highspeed in cursory locomotion. Reduction or loss of the clavi-cle that would impede forelimb movement is one adaptation.In addition, most of the musculature has shifted to the upperlimb, and the lower limb has become thinner and elongated.In many cases it is the metacarpals and metatarsals that arethe most elongated. In hoofed mammals the number of dig-its is reduced. The horse is the most extreme example withonly a single digit. The elongation of the leg relative to bodylength produces a longer stride, thereby increasing the speed,which is equal to the length of the stride multiplied by striderate. Another trait that increases speed is a pliant vertebralcolumn that enables the mammal to place the hind feet infront of the fore feet when running at full clip. At very highspeed, all four feet may be simultaneously off the ground. Thisis seen in horses, greyhounds, gazelles, and cheetahs. Chee-tahs can cover a fixed distance faster than any other mammal.They are able to sprint at over 60 mph (97 kph).



Mammal tail diversity reflects different functions. 1. A jerboa’s tail is used as a counterweight and balance; 2. A spider monkey’s tail is pre-hensile and used in locomotion; 3. A narwhal’s tail propels it through the water; 4. A mule deer’s tail can communicate an alarm; 5. A red kan-garoo uses its tail as a support while upright; 6. A northern flying squirrel uses its tail as a rudder. (Illustration by Gillian Harris)

1

23

4

5

6

GH2003

Saltatory mammals use hopping as a means of locomotion.Some are quadrupedal, such as hares, using all four limbs tomake their leaps. Others use another form of hopping calledricochet saltation. This is a bipedal locomotion in which onlythe two hind legs are involved in propulsion. Ricochet salta-tors have a long tail (often tufted at the end) that is used forcounterbalance. In the case of the macropods (kangaroos) itis also used as a support during rest. Other ricochet saltatorsinclude kangaroo rats, jerboas, springhares, and tarsiers. Inmost cases ricochet saltators have reduced forelegs, long hindlegs, and elongated feet. Generally it is the metatarsals havethat been the most elongated. One exception is the tarsier, asmall primate that retains longer forelimbs. It is the tarsalbones in the hind foot that are elongated, rather than themetatarsals. This leaves the tarsier with grasping ability in itshind paws. It is a ricochet saltator on a horizontal substrate,but in the shrub layer it employs vertical clinging and leap-ing, i.e., it pushes off vertical supports with its powerful hindlegs and grasps a branch with its forelimbs and the upper partof its hind legs.

Arboreal mammals have many adaptations to life in thetrees. One is stereoscopic vision (depth perception) in leapers

and gliders. Grasping paws and opposable thumbs are oftenfound, but they are not required. Squirrels scamper about onbranches using sharp claws that provide traction. Sloths haveelongated curved claws from which they hang under branches.Gibbons (small apes) have long fingers that serve as hooks, areduced thumb, and a more dorsal scapula that allow them toswing underneath branches in the manner that children doon “monkey bars” at playgrounds. Prehensile tails are foundin many arboreal mammals ranging from marsupials to pri-mates. These tails are capable of wrapping around branchesand serving as a “fifth limb.” An arboreal adaptation amonggliders (e.g., flying squirrels and colugos) is a ventral mem-brane, called the patagium, that can be spread out to gener-ate lift for gliding. Except in the colugo, the tail is free of thepatagium and is used for maneuvering. Gliders cannot ascendin flight, so they must climb before they launch. Despite thatlimitation, gliding can be very efficient. Colugos are able tocover over 400 ft (122 m) with a loss of only 40 ft (12 m) inaltitude.

Among mammals, powered flight has evolved only in thebats, which are nocturnal fliers. In the order Chiroptera (lit-erally “handwing”) the mammalian forelimb has been modi-



A. Cross section of a hair. B. Hairs may provide insulation and waterproofing. Specialized hair includes quills, whiskers (C), and horns (D). (Illus-tration by Patricia Ferrer)

A

B

C

D

cuticle

cortex

medullasecondary hairs

sebaceous glands

whiskers

quills

fied to form a wing with the main portion composed of theelongated bones of the hand. Bat hind limbs have been mod-ified to help control the rear portion of the flight membrane.In addition, the feet have curved claws that enable these an-imals to hang in an upside down position. Flight requires awhole suite of characteristics including circulatory and ther-moregulatory adaptations, and echolocation for flight in adark environment. Most of the Old World fruit bats do nothave echolocation and do not fly in complete darkness.

Some mammals have successfully adapted to aquatic envi-ronments. Semiaquatic mammals spend some time on land(e.g., yapoks [or water opossums], beavers, otters, and duck-

billed platypuses). Their locomotor adaptations include a bodyapproaching a fusiform (torpedo) shape, webbed feet (at leaston the hind leg), and valvular openings to the nose and earthat can be closed to keep out water. Seals, sea lions, and wal-ruses are more aquatic and have evolved flippers that provideefficient propulsion in water, although they still retain somelocomotive ability on land. Seals propel themselves mainly byundulation of the flexible vertebral column assisted by the hindlimbs. Completely aquatic mammals include the Cetacea(whales, dolphins, and porpoises) and the seacows (dugongsand manatees). The body is more fusiform than other marinemammals. The skeletal elements of the hind limbs have beenlost, having been replaced by soft tissue forming a fluke that



A. Mammary glands are commonly on the ventral surface of the abdomen; B. Cross section through a typical mammary gland. Numbers and lo-cation of teats may be due to litter size and life style of the mammal, as shown by C. Killer whales; D. Domestic cat; E. Orangutan. (Illustrationby Jacqueline Mahannah)

gland cistern

teat cisternteat

glandulartissue

ductsA

B

C

D

E

propels the animal in concert with undulation of the posteriorvertebral column. The forelimbs are flippers used for maneu-vering. The cervical vertebrae of completely aquatic mammalsare short, and they have completely lost their pinnae.

Cardiovascular and respiratory systemsIn order to distribute nutrients and oxygen needed for me-

tabolism, mammals need a highly efficient circulatory system.The main differences in circulatory structure between mam-mals and most other vertebrates are in the heart and in thered blood cells. The mammalian heart has four chambers (asdo birds and crocodilian reptiles) compared to the three chambers found in the reptiles (except the crocodilians). Theadditional chamber is the result of a muscular wall (or sep-tum) that divides the ventricle (lower half of the heart) intotwo chambers. In reptiles there is a single ventricle in whichdeoxygenated blood from the right atrium mixes with oxy-genated blood from the left atrium. In mammals deoxy-genated blood enters the right ventricle only and is thenpumped to the lungs. Oxygenated blood returns from the

lungs to the left atrium and then enters the left ventricle fromwhich it is sent to the systemic circuit and the rest of the body.Thus, mammals have separated the pulmonary and systemiccircuits with the result that mammalian blood is more fullyoxygenated than the blood of terrestrial vertebrates withthree-chambered hearts. Additionally, mature mammalian redblood cells (erythrocytes) are enucleated, i.e., they lack a nu-cleus, and are concave in shape. Space saved by the lack of anucleus leaves room for additional hemoglobin molecules, theoxygen-binding molecule. The concave shape also increasessurface area and places the membrane surface closer to thehemoglobin molecules facilitating gas diffusion. Thus, mam-malian blood is capable of carrying more oxygen than reptil-ian blood.

The mammal heart is large, as are the lungs, and togetherthese organs occupy most of the thoracic cavity. In certain taxa,these organs may be even bigger. Bats, for example, have a heartthat is three times larger than the average terrestrial mammalof the same size. The mammal lung is sponge-like and consistsof branched airways that terminate in microscopic sacs called



A. The horse has a stiffer spine, making it better suited for endurance. B. The cheetah is the fastest land mammal; flexibility in its spine allowsfor longer strides. C. The kangaroo has more upward movement with each leap, and does not move forward as quickly as the horse or cheetah.(Illustration by Patricia Ferrer)

A. Horse - 43 mph (70 km/h)

B. Cheetah - 62 mph (99 km/h)

C. Kangaroo - 35 mph (55 km/h)

vertical fulcrum

alveoli. The alveoli walls consist of epithelial tissue throughwhich gas exchange occurs. This structural arrangement ofsmaller and smaller tubes and saccules increases the surface areaavailable for respiration. For example, the respiratory mem-brane of human lungs is between 750 and 860 ft2 (70–80 m2),which is about 40 times the surface area of the skin.

Mammals have a layer of muscle that separates the tho-racic cavity from the abdominal cavity. This is called the res-piratory (or muscular) diaphragm. When this muscle isrelaxed its domed shape forms the floor of the thoracic cav-ity. When it contracts it moves towards the abdominal cav-ity, increasing the volume of the thoracic cavity, which drawsair in from the external environment.

Digestive systemTo fuel endothermy, mammals require more calories per

ounce (or gram) of tissue than do ectothermic vertebrates suchas reptiles. This is accomplished by more efficient digestion offood stuffs and more efficient absorption of nutrients. This ef-ficiency begins with specialization of the teeth. Mammals havefour different kinds of teeth (heterodonty) that are ideallyshaped to cut, slice, grind, and crush food. An exception is thetoothed whales in which all the teeth are similar (homodonty).The four types of teeth are incisors for slicing, canines for pierc-

ing, premolars for crushing or slicing, and molars for crushing.They are commonly represented by a notation called a dentalformula, e.g., I2/2 C1/1 P3/3 M2/3, the dental formula for theEgyptian fruit bat (Rousettus aegyptiacus). The first in each groupof two numbers represents the teeth in the upper jaw and thesecond is the number of teeth in the lower jaw. Multiplyingthe dental formula by 2 gives the total number of teeth, 34.The Egyptian fruit bat’s dental formula indicates that the fullset of teeth for the upper jaw is four upper incisors, two uppercanines, six upper premolars, and four molars. There is a greatdeal of variation in the number and type of teeth present. Forexample, the prosimian primate, the aye-aye (Daubentoniamadagascariensis), has a dental formula of I1/1 C0/0 P1/0 M3/3,which illustrates a reduction in number of some teeth and thecomplete loss of others. In the case of some herbivorous mam-mals the upper incisors are either reduced in number or com-pletely replaced by a hard dental or gummy pad that functionsas a cutting board for the lower incisors. In some gnawing mam-mals, such as rodents and rabbits, the upper and lower incisorsgrow throughout the entire life span and the canines have beenlost. Modification of teeth may be extreme, such as completeloss in most anteaters, or the formation of large tusks, derivedfrom the second upper incisors in elephants, or from the ca-nines in walruses (Odobenus rosmarus).

The relationship between dental structure and function isso precise that the diets of long-extinct mammals can be de-



The mammalian heart is four-chambered, and separates oxygenated and deoxygenated blood. Oxygenated blood flows from the lungs, throughthe heart, to the body. Deoxygenated blood flows from the body, through the heart, to the lungs, where it is reoxygenated. The smaller heart onthe left belongs to a cat. (Illustration by Wendy Baker)

The mammalian heart has four chambers

RightAtrium

Left Atrium

RightVentricle

LeftVentricle

To Lungs

FromLungs

duced from their teeth. The teeth are often the only fossil re-mains recovered from paleontological sites. Teeth performmechanical (or physical) digestion by breaking down a foodmorsel into smaller pieces, providing additional surface areafor action by digestive enzymes. Premolars in herbivorousmammals usually have ridges for grinding. In some carnivoressuch as wolves, the last upper premolar has a blade that shearsagainst the first lower molar. Fruit-eating mammals such asflying foxes often have flattened premolars and molars.

Other modifications for efficient digestion occur in thestomach, a portion of the gastrointestinal tract. The stomachserves as a storage receptacle in most mammals and as a siteof protein breakdown. A simple stomach is found in mostmammal species, including some that consume fibrous plantmaterial. In other mammals that consume a high fiber dietthe stomach has become enlarged and modified to handlemore difficult digestion. These modifications comprise aforegut digestive strategy, for which the stomach containscompartments where symbiotic microbes break down cellu-lose and produce volatile fatty acids (VFA) that can be uti-lized by the mammal. Foregut fermentation has beendeveloped to the greatest degree among the mammal orderArtiodactyla, which includes pigs, peccaries, camels, llamas,giraffes, deer, cattle, goats, and sheep. Rumination, repro-cessing of partially digested food, is accomplished by the four-compartment stomachs of giraffes, deer, cattle, and sheep.Less complex tubular and sacculated stomachs are found inkangaroos, colobus monkeys, and sloths. Stomachs in foregutfermenting species are neutral or only slightly acidic, aroundpH 6.7, to provide a favorable environment for symbionts.

Food moves from the stomach to the intestines; which con-sist of the small intestine, where most digestion and absorp-tion occurs, and the large intestine. The wall of the small

intestine contains epithelial tissue with small finger-like pro-jections called villi. In turn, each villus has smaller extensionscalled microvilli. The villi secrete enzymes for further carbo-hydrate and protein digestion. The microvilli absorb the di-gested nutrients. The presence of the villi and microvilli inthe mammal small intestine increases the absorptive surfacearea by at least 600 times that of a straight smooth tube. The



A longtail weasel (Mustela frenata) in its summer coat. (Photo by TomBrakefield. Bruce Coleman, Inc. Reproduced by permission.)

Black rhinoceros (Diceros bicornis) profile showing its horns used forprotection and fighting for supremacy and social heirarchy. (Photo byLeonard Lee Rue III. Bruce Coleman, Inc. Reproduced by permission.)

A longtail weasel (Mustela frenata) in winter coat. (Photo by Bob andClara Calhoun. Bruce Coleman, Inc. Reproduced by permission.)

villi of the human small intestine, for example, provide 3,230ft2 (300 m2) of surface area whereas the surface area of asmooth tube of the same size as the small intestine is about5.4 ft2 (0.5 m2). Nutrient absorption occurs through the mem-branes of the microvilli of each intestinal epithelial cell. Alsodistributed throughout the small intestine are glands that se-crete special enzymes for further digestion of proteins, car-bohydrates, and lipids.

For mammals, diet and the length of the small intestineare closely correlated. Mammals that consume a diet that iseither digested in the stomach (such as animal protein con-sumed by faunivores) or easily absorbed (such as nectar con-sumed by nectarivores) have a shorter small intestine than

other mammals. Herbivores that eat very fibrous plant mat-ter tend to have the longest small intestine. The small in-testines of fruit-eaters tend to be intermediate in length.

The foregut fermentation strategy of herbivores requires amedium or large body size to accommodate the necessarilylarge stomach. A strategy generally used by smaller herbivoresis hindgut fermentation (although there are large hindgut fer-menters such as horses, elephants, and howler monkeys). Thehindgut, also called the large intestine, consists of the cecumand the colon. The cecum is a blind pouch that serves as theprincipal fermentation chamber in the hindgut strategy. As inthe stomach of foregut herbivores, colonies of symbionts inthe cecum of hindgut fermenters break down cellulose and ex-crete products advantageous to the mammal. Nutrients appearto be absorbed through the wall of both the cecum and colon,especially in the larger mammals.

Small hindgut fermenters, such as many rodents and rab-bits, have the problem that food can only be retained in thegut for a short time. As it leaves the hindgut, digestion is in-complete and many valuable nutrients may be left unabsorbed.This problem is solved by a behavioral adaptation: a soft pel-let is produced in the cecum, defecated, and immediately



A free-ranging yak (Bos grunniens) exhibits the rare golden color phase.(Photo by Harald Schütz. Reproduced by permission.)

An aardvark (Orycteropus afer) unearths the subterrranean nests ofants and termites through active digging using powerful and well-adapted claws. (Photo by Rudi van Aarde. Reproduced by permission.)

An elephant can reach a long way up for a meal using its trunk. (Photoby K & K Ammann. Bruce Coleman, Inc. Reproduced by permission.)

picked up by the animal and reingested. This reingestation offeces is called coprophagy. The soft pellet then goes throughthe digestive process a second time and the end product is ahard fecal pellet devoid of nutrients. Many owners of pet rab-bits are familiar with the hard pellet, often called a “raisin.”The softer pellet is usually consumed at night (when co-prophagy goes unobserved by the pet owner) and is called the“midnight pellet.” Coprophagy is efficient; voles are able toextract 67–75% of the energy contained in their food.

Nervous system and sensory organsMammals have relatively larger brains than other verte-

brates. From monotremes to marsupials to eutherians, themammal brain increases in size and complexity, primarily bythe expansion of the neopallium. The neopallium (or neo-cortex) is a mantle of gray matter that first appeared as a smallregion between the olfactory bulb and the larger archipallium.The neopallium in mammals has expanded over the primitiveparts of the vertebrate brain, dominating it as the cerebralcortex. The cerebral cortex is a thin laminar structure con-sisting of six sheets of neurons. In order to increase the num-

ber of neurons in the neocortex it must be folded to fit withinthe skull of a mammal. For example, the surface area of thehuman neocortex is about 1.5 ft2 (0.14 m2). With this area, itcould not be simply laid over the deeper parts of the brain;folding produces gyri and sulci (folds and grooves, respec-tively), which gives the eutherian brain a convoluted appear-ance. Small mammals do not usually have convolutions, butthey are almost always found once a species has reached a par-ticular body size. Some researchers believe that the convolu-tions simply serve to increase the number of neurons in theneocortex, while others propose that the primary purpose ofthe convolutions is to increase surface area for heat dissipa-tion. The brain produces a large amount of metabolic heatand must be cooled. Increasing the surface area provides morearea for heat transfer (radiation) to occur; i.e., the convolu-tions produce a “radiator” for the brain.

The neocortex may be more developed or less developeddepending on the mammalian species. In echolocating bats,for example, it comprises less than 50% of the brain surfacebecause most of the bat brain is devoted to the auditory cen-ters. Specific regions of the neocortex are specialized for par-



A barbary ape (Macaca sylvanus) juvenile in a female’s arms. (Photoby Animals Animals ©J. & P. Wegner. Reproduced by permission.)

A Bengal tiger’s (Panthera tigris) stripes make it stand out on a beach,but keep the tiger well camouflaged as it hunts from thickets, longgrasses, or shrubs along riverbanks. (Photo by Jeff Lepore/Photo Re-searchers, Inc. Reproduced by permission.)

ticular functions. For example, the occipital region is a visualcenter, the temporal region is involved with hearing, and theparietal lobe interprets touch. A structure found only in theeutherian brain is the corpus callosum, a concentration ofnerve fibers that connect the two cerebral hemispheres andserve as a communication conduit between them.

Brain structure accounts for mammals’ great ability to learnfrom their experiences. Their brain structure, combined withother neural characteristics, also accounts for mammals’ acutesensory abilities. For example, mammalian smell is very acute.In some mammals, it is the most developed sense. Mammalshave an elongated palate and, consequently, the nasal cavity iselongated as well. A structure in the palate of many mammals,the vomeronasal organ, detects smells from food. The devel-opment of turbinal bones covered by sensory mucosa in thenasal cavities has allowed more efficient detection of odors.Even so, some mammals have a poorer sense of smell than oth-ers, e.g., insectivorous bats, higher primates, and whales. In fact,dolphins and porpoises completely lack the olfactory appara-tus. The receptors for taste are located on the tongue. Taste,interpreted in the brain in conjunction with olfactory stimuli,helps mammals identify whether food is safe to eat or not.

Mammal hearing is highly developed. In mammals, the ar-ticular and quadrate bones of the reptilian jaw were modifiedto become the malleus and incus bones, which, along with thestapes, form the auditory ossicles in the mammal skull. Theauditory ossicles conduct vibrations to the inner ear. Anothermammal modification is the evolution of a pinna, an externalflap that directs sound waves into the ear canal (externalacoustic meatus). Many mammal species have mobil pinnaethat enable them to pinpoint the location of the sound source.Pinnae are most elaborate in the insectivorous bats, but com-pletely lacking in most marine and subterranean species.

The mammal eye is based on the reptilian eye. Many mam-mals are able to see very well in low-light conditions becauseof a reflective mirror-like layer (tapetum lucidum) in thechoroid coat beneath the retina. The tapetum lucidum pro-duces “eyeshine,” such as seen in the eyes of deer staring intoautomobile headlights. Vision is improved as light is reflectedback across the retina so that photoreceptors can interact withthe light multiple times. Some mammals have an abundanceof cones in the retina providing for color vision. This is es-pecially true of the anthropoid primates, but this is also foundin other mammals, e.g., Old World fruit bats. Aquatic speciesusually have a nictitating membrane that covers the eye, pro-viding protection in the underwater environment.

ThermoregulationMammals produce their own body heat (endothermy) as

opposed to absorbing energy from the outside environment.This metabolic heat is produced mainly in their mitochon-dria. Internal organs such as the heart, kidney, and brain arelarger in mammals than reptiles and the corresponding in-crease in mitochondrial membrane surface area adds to their



The bison’s heavy coat helps it to survive winter blizzards in Wyoming,USA. (Photo by © Jeff Vanuga/Corbis. Reproduced by permission.)

An agile bobcat (Lynx rufus) leaps across rocks. (Photo by Hans Rein-hard. Bruce Coleman, Inc. Reproduced by permission.)



ResourcesBooksFeldhamer, G. A., ed. Mammalogy: Adaptation, Diversity, and

Ecology. San Francisco: McGraw-Hill, 2003.

Hildebrand, M. Analysis of Vertebrate Structure. 4th ed. NewYork: John Wiley & Sons, 1994.

MacDonald, D., ed. The Encyclopedia of Mammals. New York:Facts on File, 2001.

Martin, R. E., R. H. Pine, and A. F. DeBlase. A Manual ofMammalogy. 3rd ed. San Francisco: McGraw-Hill, 2001.

Neuweiler, G. The Biology of Bats. New York: OxfordUniversity Press, 2000.

Novak, R. M. Walker’s Mammals of the World. 6th ed.Baltimore: John Hopkins University Press, 1999.

Pough, F. H., C. M. Janis, and J. B. Heiser. Vertebrate Life. 6thed. Upper Saddle River, NJ: Prentice Hall, 2001.

Romer, A. S. and T. S. Parson. The Vertebrate Body. 6th ed.San Francisco: Saunders College Publishing, 1985.

Welty, J. C., L. Baptista, and C. Welty. The Life of Birds. 5thed. New York: Saunders College Publishing, 1997.

Vauhan, T. A., James M. Ryan, and Nicholas Czaplewski.Mammalogy. 5th ed. Philadelphia: Saunders CollegePublishing, 1999.

PeriodicalsYoung Owl, M., and G. O. Batzli. “The Integrated Processing

Response of Voles to Fibre Content of Natural Diets.”Functional Ecology 11 (1998): 4–13.

Marcus Young Owl, PhD

heat production. Mammals also regulate their body tempera-ture within a stable range, generally between 87 and 103°F(30–39° C). This is called homeothermy. Having a constanttemperature allows mammals to maintain warm muscles,which gives them the ability to react quickly, either to securefood or to escape predation. They can also maintain the op-timum operating temperature for many enzymes, providing amore effective physiology. Some mammals are heterothermic(able to alter their body temperature voluntarily). Many in-sectivorous bats are heterothermic. When in torpor they lowertheir body temperature to the ambient temperature, conserv-ing calories that would otherwise be used for heat production.

To regulate body temperature, mammals must also havethe means to retain a certain amount of the heat they pro-duce. Small mammals lose heat more rapidly than larger mam-mals because they have a greater proportion of surface areato volume (or, equivalently, to their body mass). Heat is lostthrough surface area. The higher the surface area–to-mass ra-tio, the greater the rate of heat loss. Fur helps to insulate asmall mammal to some degree, but often it is not enough toprevent the high rate of heat loss. Small mammals often com-pensate by obtaining more calories per unit of time by con-tinuously eating foods that are quickly digested and absorbed.Larger mammals’ surface area–to-mass ratio decreases as theirmass increases, and they lose heat at a lower rate.

Reproductive systemThere are three different modes of reproduction used by

mammals. The monotremes, whose extant members are theechidnas and duck-billed platypuses, lay eggs. The therians (mar-supial and placental mammals) give birth to live young. Marsu-pial newborns are undeveloped (some mammalogists call themembryos). After only a short gestation period they must maketheir way to a teat outside the mother’s body (a teat that may bein a pouch in species that have pouches) to finish development.The embryos of placental mammals remain in the uterus dur-ing development, and they have a nutritive connection with themother through the placenta. The young of placental mammalsare born more mature than the young of the other two groups.

The female reproductive tract in monotremes is very muchlike a reptile’s. A cloaca (also found in amphibians, reptiles,and birds) is a common chamber for the digestive, urinary,and reproductive system. The eggs are conveyed from theovaries through the oviducts where fertilization occurs. Afterfertilization the eggs are covered with albumen and a leath-ery shell produced by the shell gland. In therian females thereproductive organs are separate from the urinary and diges-tive systems. The marsupial female has two uteri, each withits own vagina. Eutherian females may have either a singleuterus or paired uteri, but always a single vagina. The pla-cental embryo implants and develops in the uterine wall.

In all therians, the male urinary and reproductive systemsshare a common tract, the urethra. A problem for endother-mic mammals is that their body temperature may be too highto sustain viable sperm. This is not a problem for monotrememales because their body temperature is lower than that oftherians, and their testes are contained in the abdominal cav-ity. The testes of therian males are typically contained in ascrotum, a sac-like structure that lies outside the body cavity.The testes may descend into the scrotum from the abdomi-nal cavity only during breeding season or they may be per-manently descended. The penis differs in the three maingroups of mammals. The monotreme penis is attached to theventral wall of the cloaca. The marsupial penis is directed pos-teriorly, contained in a sheath, and the glan penis (tip) is bi-fid, which accommodates the two vaginas in the marsupialfemales. The eutherian penis is directed forward. It may hangfreely or be contained in an external sheath. In many species,including most primates, a bone called the baculum supportsthe penis.

Mammary glands (see also the discussion under integu-ment) provide nourishment for the young mammal. Whilemilk requires energy to produce, it also conserves energy forthe mother: Mammals do not have to make numerous tripsto find food and return with it to feed their offspring. Ob-servations of bird parents making trip after trip in order tofeed insatiable hungry mouths at the nest illustrate this point.A mammal mother obtains her food, returns to the nest orden, and can feed her young in comparative safety.

Adaptation for flight in bats

Bats, and an uneasy creeping in one’s scalp As the batsswoop overhead! Flying madly. Pipistrello! Black piper onan infinitesimal pipe. Little lumps that fly in air and havevoices indefinite, wildly vindictive; Wings like bits of um-brella. Bats!

The poet, D. H. Lawrence, seemed to find bats disgust-ing, but these creatures of the night are the only mammals tohave evolved powered flight. Occupying the nocturnal flierniche has been extremely successful—so successful that oneout of every four mammal species is a bat.

Three vertebrate taxa have evolved lineages capable ofpowered flight: the pterosaurs (Reptilia), birds (Aves), andbats (Mammalia). In all three cases, the forelimbs of thesevertebrates were modified over time to form wings. This isan example of convergence, the independent evolution of acommon structure that performs a similar function amongunrelated species. The pterosaurs, the only reptiles to evolvetrue flight, were the first vertebrates to develop poweredflight. Pterosaurs (order Pterosauria) appeared about 225million years ago and lasted about 130 million years untilthey became extinct at the end of the Mesozoic era. The mostdiverse lineage of flying vertebrates is the birds (class Aves),which underwent extremely rapid evolution during the Cre-taceous period, approximately 150 million years ago (mya).Bats (order Chiroptera) appear to be the most recent flyinglineage among vertebrates, although precisely how recent isuncertain because only a few examples are represented in thefossil record. The oldest unquestioned fossil bat dates backto the early Eocene (about 50 mya) and is already a well-de-veloped bat. Fossils from the early Paleocene (65–60 mya)attributable to bats consist mainly of teeth and jaws. Theyare often disputed as belonging to the order Primates.

Advantages to flightFlight in a vertebrate provides several advantages. First,

the flying animal has access to food sources unavailable toterrestrial species. This includes insects flying above theground level that cannot be reached by earthbound animalsas well as fruits and flowers on the terminal ends of thin

branches. Second, the flier has a ready means of escape fromnon-flying (or non-volant) predators and can rest in placesthat are not accessible to earthbound predators. Third, flightgives a species great mobility and the ability to cover largeexpanses rapidly and cheaply. Although the amount of en-ergy required to initiate flight is great, once the animal isairborne, flying is the most economical form of locomotionper distance traveled in a terrestrial environment. In addi-tion to daily foraging advantages, flight provides the meansto compensate for seasonal changes in climate and food avail-ability. A fourth advantage is at the evolutionary level. Flierscan overcome geographic barriers such as large bodies of wa-ter and, consequently, can disperse to locations not easilytraversed by non-volant terrestrial animals. For example, batsare the only mammals native to New Zealand, to many re-mote Pacific Islands, and to the Azores in the Atlantic. Be-fore humans arrived on Australia with dogs, bats and a fewrodents (apparently arriving from New Guinea) were theonly eutherian mammals among all the terrestrial fauna onthe continent.

Nocturnal flight adaptationsThe focus of this entry will be the adaptation for flight

among bats, the only mammals to evolve structures for pow-ered flight. Bats are not just fliers, they are mammalian, noc-turnal fliers. Consequently, their adaptation to flight involvesmore than just the evolution of wings, but also requires solu-tions to nocturnal navigation, thermoregulatory problems,and energy considerations.

Over a span of 65 million years of evolutionary history,natural selection acted to balance several physical considera-tions to accommodate demands of flight: body mass andshape, wing morphology, flying style (i.e., control of wingshape, orientation, and motion), and physiology (to meet theenergy requirements for flight). To understand flight adapta-tion, it is useful to gain an understanding of the forces ex-erted on the animal in powered flight. Adaptation for flightof bats is guided by the need to generate and withstand, orminimize, these forces during flight. However, before look-ing at flight it is imperative to look at a prerequisite for noc-turnal flight: some way to navigate in darkened space. Beforeflight could evolve in bats, a bat ancestor must have devel-


• • • • •

Adaptations for flight

oped echolocation. There is more to being a flying bat thanjust having wings.

EcholocationBefore there could be nighttime fliers, there had to a way

to navigate in the dark. Bats are active at night and they of-ten inhabit darkened areas such as caves or the inside of hol-low trees.

Echolocation is an adaptation for navigating in visuallylimited environments. There are other mammals that employecholocation, including various marine mammals and possi-bly members of the order Insectivora such as shrews. Thereis also some suggestive evidence that the colugo, a nocturnalglider, has some form of echolocation. Marine mammals suchas whales and dolphins move through a medium that trans-mits light very poorly. The water they swim in is often ob-scured by murkiness from plankton and other suspendedparticles. At depths greater than 656 ft (200 m), a routine div-ing depth for marine mammals, the surroundings becomecompletely dark. The shrew is a terrestrial mammal with tinyeyes and presumably poor vision. They are active at night.Shrews are fossorial, i.e., they burrow, dig, and forage in theleaf litter of wooded areas. Consequently, they also occupy a

visually limited environment. It should also be pointed outthat only two bird species are known to echolocate. Oilbirdsare nocturnal and inhabit caves. The other, the Asiatic caveswiftlets, frequently fly in dark caves.

Birds have been part of the terrestrial fauna for at least 150million years. They fill the available diurnal (daytime) flyingniches. By the time bats appeared in the Eocene, birds werecompletely developed and no latecomer mammal would havebeen able to out-compete them in the daytime. Bats mostlikely descended from small nocturnal insectivorous mam-mals. Therefore, protobats were already in the nocturnalniche when there was an opening for a nocturnal flier. How-ever, flying in the dark can be dangerous. In addition to theopen nighttime environment, most bats roost in caves or in-side hollow trees, which are darker environments than out-side. There is also the danger of mid-air collisions with otherbats. Consequently, before nocturnal flying could be feasible,some way of avoiding obstacles had to evolve. Of course, thereis no way to know when echolocation actually evolved in bats.However, it had to be very early in their development. Asmentioned previously, shrews have a crude form of echolo-cation, and shrews and other insectivores are often cited as amammalian rootstock. If so, it is not unreasonable to suggestthat echolocation developed sometime before flight.


Adaptations for flightVol. 12: Mammals I

The bulldog bat (Noctilio albiventris) uses its claws to swoop in and grab prey while in flight. (Photo by T. E. Lee Jr./Mammal Images Library ofthe American Society of Mammalogists.)

It was the Italian physiologist Lazzaro Spallanzani who firstexperimented with obstacle avoidance in bats and owls in theeighteenth century. He discovered that owls would not fly incomplete darkness, but this did not deter bats. He hung wiresfrom his ceiling with small bells attached. Bats could flythroughout his study and never jingle the bells. When heblinded the bats, again they did not touch the wires. He fi-nally inserted brass tubes into their ear canals. This was ob-served to impair the bats ability to avoid the wires. Spallanzaniwas still baffled. No sound came from the wires while theywere simply hanging. Nevertheless, he attributed the bats’ability to avoid the wires to keen hearing. Of course, he wasnot able to hear the high-pitched sounds that the bats wereactually emitting.

In the 1930s, the first microphone capable of detecting ul-trasound (beyond the hearing of humans) was produced.American zoology and comparative psychology student, Don-ald Griffin, prominent in the 1980s for his work on animalcognition, found that placing one of these microphones in themiddle of a group of quiet bats suddenly changed these rela-tively quiet animals into loud chatterboxes. At about the sametime, the Dutch zoologist, Sven Dijkgraf, who had very keenhearing, discovered that he could hear sounds coming fromGeoffroy’s bat. When he placed muzzles over their jaws, pre-venting the emission of the sounds, these bats became dis-

oriented and crashed into objects. From these discoveries,early researchers were able to gain some understanding of themechanisms of echolocation. However, to date, the details ofdetection and interpretation of these signals by the bat arestill a very active area of research (e.g., the bat project at theAuditory Neuroethology Lab at the University of Maryland,College Park).

Echolocation in bats results from the production of a high-pitched sound by the larynx and emitted through either themouth or the nostrils. Often, the nose has been modified intoa nose leaf, a fleshy process on the upper snout, which helpsdirect these sounds. Sound waves travel until hitting an ob-ject and bouncing back. The pinnae (external ears) of bats arelarge, highly modified structures designed to receive the re-turning signal of the bounced sound. The tragus is a smallflap located in front of the ear canal. It acts as an antenna andallows the bat to discern the direction from which the soundis coming. Different species of bats utilize different frequen-cies. Individuals of the same species will alter their frequen-cies slightly to prevent confusion of signals that could lead tomid-air collisions.

Echolocation is also used for foraging. In fact, echoloca-tion may have originally developed in a bat ancestor that wasforaging in the forest litter. Bats can catch insects “on the fly,”


Vol. 12: Mammals IAdaptations for flight

The flying fox (Pteropus sp.) can have a wingspan of up to 6.6 ft (2 m). (Photo by © W. Perry Conway/Corbis. Reproduced by permission.)

part of what makes them successful as nocturnal fliers. How-ever, an evolutionary arms race exists because some mothshave developed a defense against bat echolocation. They pos-sess sound sensors on their thorax that enable them to detectthe ultrasonic pulses being aimed at them by the bats. Theythen engage in erratic flight patterns in an attempt to evadethe foraging bats. Some moths have even developed counter-measures. They produce sounds directed at the bats that seemto deter them. It is possible that these sounds are jammingthe bats’ echolocation in the way that aluminum foil was usedto jam radar signals during World War II.

One group of bats is notable for not having echolocation.These are the large flying foxes and fruit bats (Megachi-roptera). These bats depend on vision during activity underlow-light conditions at dusk and dawn, a cycle referred to asa crepuscular activity cycle. They are also active during allmoon phases, except the new moon when there is no moon-light. Megachiroptera lack the large pinnae and elaborate noseleafs found on the echolocating insectivorous bats (Microchi-roptera). There is one exception: rousette bats that roost indark caves (which is unusual for a megachiropteran) use a formof echolocation in which they produce sounds by slowly click-

ing their tongue. This is different from microchiropteranecholocation. Although echolocation is not necessary forflight in itself, it is a required adaptation for fliers who travelin pitch-black darkness.

The physics of powered flightOnce a means for detecting and avoiding obstacles was de-

veloped in a bat ancestor, the lineage was free to expand intothe nocturnal flier niche. Powered flight allows access to fly-ing insects. Because gliders do not have the maneuverabilityto pursue flying insects, this feeding niche was wide open dur-ing early bat evolution. The difference between poweredflight and other modes of traveling through the air is ma-neuverability. Gliders such as the colugo have extra skin atthe body’s sides, which can both stretch out and change an-gle during flight to control both the rate and the angle of de-scent. Therefore, gliding has both a downward and ahorizontal component of motion. However, the starting pointis always higher than the final position of the animal. This isbecause gravitational potential (the energy determined by abody’s position in a gravity field) is the only source of kineticenergy (energy of motion) in this mode of traveling throughthe air. To obtain a greater height above the starting posi-tion, gliders must utilize other means (e.g., tree climbing).Power flyers can oppose the force of gravity and increase theirheight above the ground by using wings and the power gen-erated by their own muscles. They are also capable of con-trolling the magnitude and direction of their forward speedwithout depending on gravity or air currents.



Bats have adapted to flight by developing extremely light and slenderbones. (Photo by Barbara Strnadova/Photo Researchers, Inc. Repro-duced by permission.)

The southern flying squirrel (Glaucomys volans) uses a thin membranethat extends from its hands to its feet to glide up to 80 yd (73 m).(Photo by © Joe McDonald/Corbis. Reproduced by permission.)

Powered flight is possible because air is a fluid. In every-day usage, the word “fluid” brings to mind a liquid such aswater or gasoline. But technically, a fluid obeys the law thatthe faster an object moves through it, the greater the forceexerted on the object. In the terminology of fluid mechanics,the force exerted on an object in a direction perpendicular tothe direction in which the object moves through a fluid iscalled dynamic lift, which is generated when an object mov-ing through a fluid changes the direction of the fluid flow.

Another fluid force exerted on an object is dependent onthe shape of the object. This is called Bernoulli lift, whichmay be involved in natural selection pressure for the wing andbody shape of the bat. The Bernoulli principle in fluid me-chanics states that the faster a fluid flows over a surface, thelower the pressure on that surface perpendicular to the fluidflow. Therefore, the pressure is lower on the top than it is onthe bottom. This pressure difference results in Bernoulli liftupward. Experimentally it has been determined that Bernoullilift alone is not sufficient for power flying, but most likelyprovides a selection pressure favoring a particular wing shape,body streamlining, and flight style.

In summary, the forces that must be overcome in poweredflight are inertia (the resistance to change in motion that is a

property of all masses), weight (the force exerted on the massby gravity), and drag (the fluid force exerted by air on any ob-ject moving through it). To change the height from the groundand the speed and direction of forward motion, the bat has touse its wings to manipulate the airflow to generate the forcesof lift and thrust. The wing structures themselves must alsobe able to withstand the stresses of moving through the air.

Bat wing morphology and its role in poweredflight

Chief among the many adaptations of the bat for poweredflight is the bat wing, and the flapping flight style that usesmuscle power to generate lift and thrust. The bat wing evolvedfrom the forelimbs of a terrestrial mammalian ancestor. Themammalian forelimb is exceedingly mobile because the shoul-der joint between the scapula (shoulder bone) and thehumerus (upper forelimb bone) is loosely held together withmuscles. This allows for actual rotation of the arm around theshoulder joint in many species. Primates have this mobility,and so do bats.

The taxonomic name of the bats, order Chiroptera (mean-ing, “hand-wing”), perfectly describes the morphology of thebat wing. The skeletal structure of the bat wing consists ofthe humerus, a well-developed radius, and a much-reducedulna. In humans, the ulna is a major bone of the forearm andforms a hinge joint in the elbow region with the humerus.The highly elongated hand (metacarpal) and finger (pha-langes) bones form the rest of the bat wing skeleton. Onlythe pollex (or thumb) retains the claw of the mammal ances-tor, although on fruit bats and flying foxes the second digitalso retains a claw. The bones of the wing provide a segmentedskeletal frame for support and control of the flight membrane.

The flight membrane (called a patagium) is a flexible dou-ble-layered structure consisting of skin, muscle, and connec-tive tissue. It is richly supplied with blood vessels. The regionof the patagium that stretches from the sides of the body andthe hind limbs to the arm and the fifth digit is called the pla-giopatagium. Other portions of membrane extend from theshoulder to the pollex (first digit) along the anterior portionof the wing (propatagium), between the fingers (the chi-ropatagium), and from the hind limbs to the tail (theuropatagium, also called the interfemoral membrane). Thewing operates on an airfoil design, with the flexible membranesegments changing shape to produce variable pressure gradi-ents along the wing surface that results in variable amountsof lift and thrust. The bats’ fine control of the shape of thepatagium gives them a maneuverability that cannot bematched by birds.

Bat flight is controlled by seventeen different pairs of mus-cles. Three different muscles provide power for the down-stroke. Another three muscles execute the upstroke. This isvery unlike birds, where two pairs of muscles provide thepower for the depression and elevation of the wings. The ster-num (breastbone) in bats is not particularly well developed,while in birds it is very prominent with a well-developed keel.The pectoralis muscle that originates from the sternum is thelargest bat flight muscle and it has the richest supply of blood



These little red flying foxes (Pteropus scapulatus) hang upside downand as soon as they drop, they are in flight. (Photo by B. G. Thom-son/Photo Researchers, Inc. Reproduced by permission.)

vessels known for any mammal. Other muscles that originatefrom along the vertebral column (backbone) and the scapulahelp to provide tension to the membrane and adjust the po-sition of the wing. Muscles fibers embedded in the membraneassist in regulation of the tension of the patagium. Many mus-cles that exist in terrestrial mammals have been slightly repo-sitioned, while others unique to bats assist in keeping thepatagium taut. The wing operates on an airfoil design, withthe flexible patagium segments changing shape to providevariable amounts of lift and thrust.

The hind limb possesses a bony spur unique to bats calleda calcar that projects inwardly from the tibia. This bone at-taches to the uropatagium and functions to keeps the tail por-tion from flapping during flight. The legs can also form apouch out of the uropatagium used for catching insects. Inmost bats, the hind limbs have rotated 90° outwardly and as-sumed a reptilian-like position. The legs are used to controlthe uropatagium during flight. Another important adaptationof the hind legs is as a hook, an adaptation for hanging upsidedown. Bats are able to hook the claws of their hind paws ontohorizontal supports or rough edges on walls or on ceilings ofcaves. The claws have developed a locking mechanism that al-lows them to hold without any muscular involvement. Hang-ing upside down allows bats to occupy areas unavailable tobirds and allows a bat to use gravity to initiate flight by drop-ping. It is often believed that bats are completely helpless onthe ground because of the arrangement of their legs; this isnot true. Some species hop while others move quadrupedally.If a bat falls in water, it can swim to land. However, they donot use these forms of locomotion habitually. The arrange-ment of the bat hind limbs has probably constrained the batlineage to being flyers. There are no flightless bats nor arethere swimming bats comparable to those found among thebirds (e.g., ostriches and penguins, respectively).

Bat flightThe superior aerobatic ability of the bat in flight is due to

the wing segmentation provided by the skeletal frame, theflexibility of the membrane segments, and the very fine con-trols provided by the wing musculature. To date, the best an-alytical theory of animal flight is the vortex theory firstintroduced by Ellington in 1978 and further developed byRayner in 1979. According to vortex theory, bats fly by gen-erating volumes of circulating air (called vortices, singularvortex) that create pressure differences on different parts ofthe bat’s wing. The resulting fluid forces push the animal inthe direction it wants to go, at the speed it wants to go. Thebats’ flight motions are similar to the motions of a humanswimmer doing the butterfly stroke. During the downstroke,the wing is fully extended. It envelops the maximum possiblevolume of air and pushes it down, generating a region of highpressure beneath the wing and low pressure above the wing.The pressure differences add up to a resultant force that hastwo components: a thrust component that opposes the dragexerted on the animal by its motion through the air, and a liftcomponent perpendicular to the drag that opposes the actionof gravity on the mass of the animal (the animal’s weight).The numerical value of each component depends on the an-

gle of attack. The steeper the angle, the higher the lift andlower the thrust. During steep-angle ascent, the bat increasesthe curvature of the propatagium to prevent stalling. To max-imize lift, the uropatagium is curved downward. During theupstroke, the bat flexes the wing and extends the legs to de-crease drag by decreasing the surface area perpendicular tothe airflow. Each wing segment contributes different relativeamounts of lift and thrust. The wing segments closest to thesides of the body, the plagiopatagium, generate mostly lift,and the distal wing segments (the chiropatagium) providemost of the thrust. The exact pattern of airflow over differ-ent wing segments is not yet known, however, computer sim-ulations of the aerodynamics of the bat in flight are an areaof very vigorous research. For example, a project to simulatethe airflow around the changing geometry of the bat wing inflight is under way at Brown University. Preliminary resultswere published by Watts in 2001.

Wing form and flying strategiesThe wing forms of bats are highly variable from species to

species. A particular form (e.g., either long and narrow orshort and broad) may reveal a relationship between flight styleand foraging habits because it is likely that selection pressurefavors the evolution of the best wing form for a particularfeeding style. The two primary quantities used for compar-ing wing morphology to flight style are wing loading (WL)and aspect ratio (AR). WL is the ratio of body weight to thesurface area of the wing, which demonstrates the size of thewing relative to the size of the bat. In general, the higher theWL, the faster the bat has to fly to generate sufficient lift withrelatively small wings. One calculates AR by squaring thewingspan and dividing that number by the wing’s surface area.AR measures the broadness of the wing. The higher the AR,the narrower and more aerodynamically efficient (lower drag)



is the wing. Bats with high-AR wing morphology are fasterflyers, but lack the agility of bats with low AR. The surfaceareas of the uropatagium and the plagiopatagium are large inslow, agile flyers because these areas provide most of the liftduring flight. The propatagium alters the leading edge cur-vature of the wing, and prevents stalling during steep-angleflying. If the surface areas of these regions are large comparedto the wingspan, giving a low AR, the agility of the bat is veryhigh. Examining the wing form can provide clues about thebat’s specialization in foraging. There are no exact correla-tions because bats are very adaptable and highly flexible intheir foraging habits. Also, the wing form suitable for a cer-tain foraging style may be a disadvantage in other aspects ofbat behavior. Generalizations must be made with caution.With that in mind, observers have noted that some tenden-cies do emerge. In general, bats with wings having high WLand high AR are bats that fly fast and forage in open air abovevegetation. These bats regularly fly long distances in a shortamount of time, feeding on insects while in flight. Bats withwings having low WL and low AR are able to fly slowly with-out stalling and can make tight maneuvers. They are glean-ers and hoverers, able to navigate in heavy vegetation and totake off from the ground while carrying heavy prey. Fruit-eating bats that forage among vegetation and carnivorous batsthat catch prey from the ground both fit in this category.High-WL and low-AR wings tend to belong to bats that flyfast, but have short, broad wings and are capable of maneu-vering in cluttered spaces. They tend to be expert hoverers,and their flight speed allows them to visit among separatedpatches of vegetation in a minimum amount of time. Theyalso tend to specialize in nectar or pollen feeding. Low-WLand high-AR wings are found among fishing bats that flyslowly over open water with very little tight maneuvering re-quired. The low body weight allow these fishers to carry offthe day’s catch for later consumption.

Body designTo understand bat body adaptations for flight, it may be

instructive to examine bird bodies. Bird bodies are designedfor mass reduction. They do this in a number of ways. Theyhave lost teeth and the accompanying heavy jaws and jaw mus-culature over evolutionary time. They have thin, hollow, andstrong bones. Many bones are fused or reduced in size. Thelong bony tail of their ancestors has been greatly reduced tothe small vestigial pygostyle. Birds have a series of air sacs inthe body that serve to reduce weight. They do not have a uri-nary bladder to store urine nor do they have a urethra. Thekidneys excrete uric acid into the cloaca where it is mixed withintestinal contents to produce the white guano associated withbirds. Birds have lost one ovary, and lay eggs so they do nothave to carry a fetus. The most distinctive feature of birds istheir feathers, which provide lift, insulate them against heator cold, streamline the body, and reduce mass.

Bats, as mammals, must address these weight reduction is-sues differently. In general, bats are much smaller in size thanbirds. Most bats belong to the suborder Microchiroptera (theinsectivorous bats or microbats, also called the “true bats”) andrange from 0.07 oz (2 g) (Kitti’s hog-nosed bat, perhaps thesmallest mammal) to 8.1 oz (230 g), but fewer than 50 speciesweigh more than 1.8 oz (50 g). The larger flying foxes(Megachiroptera) may reach 56.4 oz (1,600 g) with wingspansof 6.5 ft (2 m), but they are never as large as the largest birds.Bat bones are thinner and lighter than those of most mam-mals, but not as light as bird bones. Bat bones have marrowin the shafts, whereas bird bones are hollow. Several bones inthe bat skeleton (ulna, caudal [or tail] vertebrae) have been re-duced, while several have been lost altogether (fibula, caudalvertebrae in fruit bats). The distal phalanges have less miner-alization and a flatter cross-section than normally found inmammal bones, which provides more flexibility in the wing



Multi-image of bat (Pipistrellus pipistrellus) in flight. (Photo by Kim Taylor. Bruce Coleman, Inc. Reproduced by permission.)

frame. Birds, on the other hand, have more mineralized bonesthat are somewhat more brittle. If present in the bat wing,these could actually break under the stresses on the wing frameduring flight. Bats have not lost any organs as birds have. Batsstill retain teeth. To compensate for the extra skull mass, theyhave a short neck that helps to keep the center of gravity inthe middle of the torso. The bat body as a whole has beenshortened and some of the vertebrae have fused, making for astiff backbone. The diets of bats are high-energy foods, suchas insects, fruit, or nectar, that pass through the gut quicklyso as not to load the animal down with bulky fiber. This high-energy diet also meets the energy requirements for flight. Bats,because they are mammals, have fur instead of feathers. Furhas some limited lifting properties, produces rough surfacesthat change airflow, and has some malleability for streamlin-ing, but it is inferior in those properties to feathers. Fur doesinsulate, but not as efficiently as feathers.

The most important difference between bats and birds isthat birds are daytime flyers and bats are nighttime flyers.As nocturnal flyers, bats face problems not faced by birds.The first problem they had to solve is navigation in a visu-ally limited environment. Other problems bats must solveare getting sufficient oxygen and nutrients to tissues andthermoregulation. Bats have dealt with these problems verysuccessfully.

EnergyPowered flight has enormous energy costs. Flight is ener-

getically cheaper than walking or running once the bat is upin the air. However, it takes a considerable amount of caloriesto get airborne. Flying is very demanding on bat physiology.In some species, the heart rate may rise to approximately 1,000beats per minute in order to supply oxygen to the tissues dur-ing flight. Because of these demands, the heart and lungs arelarger in bats than in comparably sized mammals.

Bats do not consume fibrous plant material. Such a dietsimply would not supply enough calories. Also, the gut pas-sage time and the gut modifications needed to digest high-fiber material would increase the weight of the animal. Batsconsume easily digestible, high-calorie items such as insects,fruit, or nectar. Some species also eat small vertebrates likefish, frogs, mice, or even other smaller bats.

ThermoregulationAssociated with the metabolic costs of flight is ther-

moregulation. Bats have unusual problems to solve in this re-gard. Bats probably have the most complex thermoregulatoryproblems to solve of any mammal. Most bats are small. Smallmammals must overcome heat loss problems because theyhave a greater proportion of surface area in relation to theirvolume (or equivalently, their body mass). Heat is lost throughsurface area. The higher the surface area–to-mass ratio, thegreater is the rate of heat loss. For this reason, small mam-mals have higher rates of heat loss than larger mammals. Furhelps to insulate a small mammal to some degree, but oftenit is not enough to prevent the high rate of heat loss. Small

mammals need to obtain more calories per unit time to pro-duce heat (via muscles) by continuously eating foods that arequickly digested and absorbed. This is quite the opposite oflarger mammals. As mammals get larger, their surface area–to-mass ratio decreases as the mass increases. Elephants havea heat load problem, not a heat conservation problem. Be-sides being a small mammal, bats also have additional surfacearea from their wing membranes. Therefore, this flight adap-tation results in about six times greater surface area than thatpresent in non-volant mammals of comparable size, which in-creases the heat loss rate many fold.

Bats solve these extreme heat loss problems through het-erothermy, a temporary reduction in body temperature to con-serve calories. Mammals are endothermic (“warm-blooded”),i.e., they generate internal heat. Most mammals are alsohomeothermic, which means that they regulate their bodytemperature within a particular range (generally, 95–102°F[35–39°C]). Bats, however, can reduce their body temperatureto conserve energy. This strategy is called heterothermy andresults in torpor. Bats can lower their body temperature to theenvironmental (or ambient) temperature and therefore do not



Gould’s wattled bat (Chalinolobus gouldii) echolocating from a branchon Mt. Isa, Queensland, Australia. (Photo by B. G. Thomson/Photo Re-searchers, Inc. Reproduced by permission.)

have to devote calories to produce heat, much of which wouldbe lost to the environment. Additionally, bats are able to re-duce blood flow to the extremities and to the wing membranethat reduces heat loss through these surface areas.

During flight, the bat’s thermoregulatory problems are re-versed. The problem becomes how to dissipate the heat gen-erated from the flight muscles. Bat wings have a rich supplyof blood vessels. Heat is transferred from the blood to thewing membrane and is radiated off the surface. Bats do nothave sweat glands, but a small amount of water vapor passesthrough the skin onto the membrane surface. As water evap-orates off the surface of the wing, it also carries away someheat. Another area where the echolocating bats lose heat isfrom the blood vessels of the large external ear. Breathingalso helps remove heat. Water vapor is one of the byprod-ucts of respiration and, when the animal exhales, more heatis dissipated.

Some species can build up a heat load while they are rest-ing during the day. This is more likely to occur among thelarger bats, but some smaller bats that roost in sunny loca-tions face this problem as well. In these situations, tempera-ture can be regulated through behavior by moving to a shadierlocation. Some bats will also use their wings to fan themselves.Sometimes, they also lick themselves to promote evaporativecooling from the saliva.

Cardiovascular and respiratory adaptationsLike birds, bats have hearts that are about three times big-

ger than those of comparably sized mammals. The heart mus-cle fibers (or cells) in bats possess higher concentrations ofATP (the molecule that is utilized for energy by cells) thanobserved in any other mammal. These adaptations enablesbats to pump more blood during a flight, a period of peak de-mand for oxygen. Resting bats may have heart rates as low as20 beats per minute. Within minutes of initiating flight, theheart rate may rise to between 400 and 1,000 beats per minute.Bats also have relatively larger lungs than most mammals, pro-viding a larger respiratory membrane for gas exchange. Thisis in response to the demands for oxygen required for mus-cle metabolism during flying.

Bats have highly vascularized wings (i.e., rich in blood ves-sels) that supply the wing membrane with oxygen and othernutrients. Because of this circulation, damage to the wingmembrane can heal very quickly. An unusual feature of thebat wing circulation is sphincters (muscular valves) that canclose off blood flow to the capillaries and shunt blood directlyfrom the arteries to the veins. It is not exactly known whenand why this is done. Some biologists believe that the sphinc-ters are closed and blood flows through the shunts duringflight. The sphincters may open during rest to allow blood to

flow into the capillaries and nourish the wing membrane. Aproblem that exists for wing circulation is that the flappingof the wings creates a centrifugal force that impedes the flowof blood back to the heart, causing pooling in the extremeends of the wings. To compensate for this, the veins of thewings have regions in between venous valves that contractrhythmically. These have been referred to as “venous hearts.”When venous hearts contract, the vein is constricted andpushes venous blood back towards the heart. The valves inmammalian veins prevent back flow, ensuring that blood willonly travel in one direction. Bat blood is capable of carryingmore oxygen per fl oz (ml) than other mammals. In fact, itcarries more oxygen than bird blood. It appears that this isaccomplished by increasing the concentration of red bloodcells (RBC), which contain the iron pigment heme that bindsto oxygen. Bat blood has smaller individual RBCs than nor-mally found in mammals and a larger number of RBCs withinthe same circulating blood volume. These smaller cells alsoprovide a relatively larger surface area for gas exchange to oc-cur. The actual mechanism of bat circulation is still not com-pletely understood. For budding bat biologists, the batcirculatory system offers many research possibilities becauselittle experimentation has been done on many aspects of thissystem.

Bat lungs are larger than the lungs of terrestrial mammals,but they do not contain the respiratory volume found in birds.The alveoli, the tiny sacs that help form the respiratory mem-brane, are smaller in the bat lungs than in the lungs of othermammals. The smaller the alveoli are, the greater the func-tional surface area for gas exchange. In addition, the alveoliare richly endowed with capillaries that bring a rich flow ofblood for gas exchange. Bats are superior to other mammalsat extracting oxygen from the environment, approaching thecapability of birds. Bats do not have the lung volume of birds,but they have high respiratory rates that facilitate aeration.The high respiratory rates are also believed to be associatedwith heat removal via water vapor.

Bats own the night skyBats are extremely successful nocturnal mammal fliers.

Their anatomy, physiology, and ecology are a finely tuned in-tegration of many different body organs and organ systemsthat enable these animals to dominate the night sky. Bat adap-tations for flight include more than just wings. The diet con-sists of high-calorie food that is easy to digest, assimilate, andpass quickly through the gut. They have solved thermoregu-latory problems ranging from the heat loss due to small sizeto the heat load of flight metabolism. The cardiovascular andrespiratory systems are highly adapted for efficient distribu-tion. All of these adaptations work together efficiently to makethe bat a well-integrated nighttime flying machine.





ResourcesBooksAltringham, J. D. Bats: Biology and Behaviour. New York:

Oxford University Press, 2001.

Anderson, D. F., and S. Eberhardt. Understanding Flight. NewYork: McGraw-Hill, 2001.

Fenton, M. Bats. New York: Checkmark Books, 2001.

Fenton, M. Just Bats. Toronto: University of Toronto Press,1983.

Hall, L., and G. Richards. Flying Foxes: Fruit and Blossom Bats ofAustralia. Malabar, FL: Krieger Publishing Company, 2000.

Hildebrand, M. Analysis of Vertebrate Structure, 4th edition.New York: John Wiley & Sons, Inc., 1995.

Hill, J. E., and J. D. Smith. Bats: A Natural History, 1st edition.Austin: University of Texas Press, 1984.

Neuweiler, G. The Biology of Bats. New York: OxfordUniversity Press, 2002.

Norberg, U. “Flying, Gliding and Soaring.” In FunctionalVertebrate Morphology, edited by M. Hildebrand, D.Bramble, K. Liem, and D. Wake. Cambridge, MA: BelknapPress, 1985.

Norberg, U. “Wing Form and Flight Mode in Bats.” In RecentAdvances in the Study of Bats, edited by M. B. Fenton, P.Racey, and J. Rayner. London: Cambridge University Press,1987.

Vaughan, T., J. Ryan, and N. Czaplewski. Mammalogy, 5thedition. Philadelphia: Saunders College Publishing, 1999.

Welty, J., L. Baptista, and C. Welty. The Life of Birds, 5thedition. New York: Saunders College Publishing, 1997.

PeriodicalsCarpenter, R. E. “Flight Physiology of Australian Flying Foxes,

Pteropus poliocephalus.” Journal of Experimental Biology, 114(1984): 619–647.

Maina, J. N. “What It Takes to Fly: The Structural andFunctional Respiratory Refinements in Birds and Bats.”Journal of Experimental Biology, 203 (2000): 3045–3064.

Morris, S., A. Curtin, and M. Thompson. “Heterothermy,Torpor, Respiratory Gas Exchange, Water Balance and theEffect of Feeding in Gould’s Long-eared Bat (Nyctophilusgouldi).” Journal of Experimental Biology, 197 (1994):309–335.

Padian, K. “The Origins and Aerodynamics of Flight inExtinct Vertebrates.” Palaeontology 28 (1985): 4132–433.

van Aardt, J., G. Bronner, and M. de Necker. “OxygenDissociation Curves of Whole Blood from the EgyptianFree-tailed Bat, Tadarida aegyptiaca E. Geoffroy, Using aThin-layer Optical Cell.” African Zoology, 37, no. 1 (April2002): 109–113.

Watts, P., E. Mitchell, and S. Swartz. “A ComputationalModel for Estimating the Mechanics of HorizontalFlapping Flight in Bats: Model Description and Validation.”Journal of Experimental Biology, 204 (2001): 2873–2898.

OtherAuditory Neuroethology Lab Webpage. University of Maryland,

College Park. 2002.<http://www.bsos.umd.edu/psych/batlab>.

Swartz Lab Webpage. Brown University, Providence, RI. 2003.<http://www.brown.edu/Departments/EEB/EML/about/about.html>.

Vertebrate Flight Exhibit Webpage. University of California,Berkeley. January 11, 1996. <http://www.ucmp.berkeley.edu/vertebrates/flight/enter.html>.

Weinstein, R. Simulation and Visualization of Airflow aroundChiroptera Wings during Flight. Brown University,Providence, RI. May 1, 2002. <http://www.cs.brown.edu/rlweinst/bat.pdf>.

Marcus Young Owl, PhD

Life in waterIn the beginning, all life on Earth was aquatic. Although

water covers over two-thirds of our planet, precisely how lifein the oceans came to be is one of our unanswered questions.Many of these animals have been around for millions of years.Over time, they have adapted in such a way that allows themto live and reproduce in water. One unusual example of long-

term ocean survival is that of the coelacanth. Fossils of thisarmored fish dating back more than 75 million years havebeen discovered, and it was thought to have been extinct. In1938, however, one was caught off the coast of South Africa.Since then, more than 100 of these prehistoric, deep-dwellingfish have been examined. They have no scales or eyelids, asdo “modern” fish, and have quietly kept to themselves in thedeepest areas of the ocean.


• • • • •

Adaptations for aquatic life

The hippopotamus (Hippopotamus amphibius) has its nostrils on the top of its snout allowing it to spend most of its time in the water. (Photoby Alan Root/Okapia/Photo Researchers, Inc. Reproduced by permission.)

For the most part, aquatic creatures spend their entire livessubmerged. However, a few aquatic animals—those that aredescended from land animals—come all or part of the wayout of the water for one reason or another: sea turtles, pin-nipeds, and penguins come ashore to breed, for example.Mammals, such as whales and dolphins, have also acquiredsome handy adaptive techniques for life in the water, comingto the surface only to breathe.

The smallest of the marine mammals is the sea otter (En-hydra lutris), at 5 ft (1.5 m) long, including the tail, and up to70 lb (32 kg). The largest is the blue whale (Balaenoptera mus-culus)—the largest animal alive—which can be 110 ft (33.5 m)long and weigh 300,000 lb (136,000 kg). To varying degrees,these mammals that have returned to the water have retainedvestiges of their terrestrial forms, including hair, which onlymammals have. Sea otters, seals, and sea lions are thicklyfurred; manatees and dugongs have a sparse pelage, but theyhave many whiskers around their mouths. Dolphins and whalesare hairless, but in some species hairs are present at birth (theyare soon lost). Sea otters have hand-like paws on their frontlegs, but their hind feet have become webbed, so that they’realmost flippers. The four legs of pinnipeds have become flip-pers, and the sirenians have front flippers (some of them havefingernails), but no hind legs, and a flattened tail for propul-

sion. Whales and dolphins have no hind legs, flippers insteadof forelegs, and a horizontal tail (fluke) for propulsion.

Evolution of aquatic animalsMarine fossils paint an idyllic scene of aquatic animal life

in its infancy some 670 million years ago (mya): soft coralfronds arch from the ocean floor, jellyfishes undulate in thecurrents, and marine worms plow through the ooze. But a ge-ologically brief 100 million years later, at the dawn of theCambrian period, the picture suddenly changes. Animalsabruptly appear cloaked in scales and spines, tubes and shells.Seemingly out of nowhere, and in bewildering abundance andvariety, the animal skeleton emerges.

For more than a century, paleontologists have tried to ex-plain why life turned hard. Hypotheses abound, some linkingthe skeletal genesis to changing chemistries of the seas andskies. Yet a recent analysis of old fossil quarries in Canadaand new ones in Greenland is providing evidence supportingthe notion that the skeletal revolution was more than a chem-ical reaction—it was an arms race.

High in Canadian Rockies of British Columbia, in an ex-traordinary 540-million-year-old fossil deposit called the


Adaptations for aquatic lifeVol. 12: Mammals I

The Pacific white-sided dolphin’s (Lagenorhynchus obliquidens) coloring helps to act as camouflage underwater. (Photo by Phillip Colla/OceanLight.com.Reproduced by permission.)

Burgess shale, a mid-Cambrian marine community comes tolife. Like many less exceptional deposits, the Burgess harborsmollusks, trilobites (the ubiquitous, armored “cockroaches”of the Cambrian seas), and clam-like brachiopods. But otherimprints in the smooth black shale dispel any image of a peace-ful prehistoric aquarium. In these waters lurked a lethal castof predators, eyeing little shells with bad intent: Sidneyia, aflattened, ram-headed arthropod with a penchant for munch-ing on trilobites, brachiopods, and cone-shelled hyolithids;Ottoia, a chunky burrowing worm that preferred its hyolithidswhole, reaching out and swallowing them with a muscular,toothed proboscis; and even some trilobites with predatorytastes. These findings have helped resurrect the arms race hy-pothesis: the 80-year-old idea that skeletons evolved primar-ily as fortresses against an incoming wave of predators.

Take Wiwaxia, a small, slug-like beast sheathed in a chain-mail-like armor. With two rows of spikes running along itsback, Wiwaxia was the mid-Cambrian analogue to a marineporcupine. The chinks in its armor are telling. Some of Wi-waxia’s spines appear to have broken and healed. The healedwounds of trilobite and Wiwaxia specimens suggest that

predators strongly influenced the elaborate new skeletal de-signs of the mid-Cambrian.

What sort of creature could gouge such wounds in a toughtrilobite? One likely culprit is Anomalocaris, the largest of Cam-brian predators. This half-meter-long creature glided throughthe seas with ray-like fins and chomped with a ring of spikedplates that dispatched trilobite shells like a nutcracker.

From the treacherous maw of Anomalocaris to the healedwounds of Wiwaxia, much of the support for the arms raceargument hinges on the Burgess shale collection. But whatabout the small shelly fauna that emerged 30 million yearsearlier? For an arms race hypothesis to be complete, preda-tors must have roamed then, too.

New finds strengthen the case for an early Cambrian armsrace. From an extraordinary fossil bed discovered in 1984 innorth Greenland, predating the Burgess shale by perhaps asmuch as 15 million years, comes a jigsaw puzzle already as-sembled: a suspiciously familiar, slug-like beast sheathed inchain-mail armor, proposed to be the long-sought ancestorof the armored slug Wiwaxia.

The creature sports a disproportionately large, saucer-likeshell at each end of its elongated body. From another fossildiscovery at a quarry in south China, which appears even olderthan the Greenland site, emerges the bizarre Microdictyon. Un-veiled in 1989 by Chinese paleontologists, Microdictyon is awormish creature with a row of pointed appendages and abody studded with oval phosphate plates. About 30 quarries


Vol. 12: Mammals IAdaptations for aquatic life

The sea otter’s (Enhydra lutris) extremely dense fur enables it to trapair bubbles which help to keep the otter afloat while sleeping. (Photoby Richard R. Hansen/Photo Researchers, Inc. Reproduced by per-mission.)

The Galápagos sea lion (Zalophus californianus wollebaecki) has welldeveloped flippers to provide locomotion both in the water and on land.(Photo by Tui De Roy/Bruce Coleman, Inc. Reproduced by permission.)

worldwide are beginning to yield Burgess-quality fossils, withperhaps many more waiting to be discovered.

Since that explosion of new forms some 530 mya, however,few new marine animals have evolved. Analysis of the evolu-tion of marine animals suggests that a sufficient variety of lifeforms in an environment suppresses further innovation. About530 mya, during the Cambrian period, after a long period inwhich animals were essentially jellyfishes or worms, marineanimal life exploded into a variety of fundamentally new bodytypes. Arthropods turned up inside external skeletons, mol-lusks put on their calcareous shells, and seven other new anddifferent body plans appeared; an additional one showed upshortly thereafter. But since then, there’s been nothing newin terms of basic body types, which form the basis of the top-level classification of the animal kingdom called phyla.

Research presented at a 1994 meeting of the GeologicalSociety of America lends support to the idea that once evo-lution fills the world with sufficient variety, further innova-tion may be for naught. There are only so many ways marineanimals can feed themselves—preying on others or scaveng-ing debris, for example. And there are only so many places to

do it: on the sea floor, beneath it, or some distance above it.When all the nooks and crannies of this “ecospace” are filled,latecomers never get a foot in the door.

ChallengesBecause water is so dense (up to 800 times denser than air),

it can easily support an animal’s body, eliminating the needfor weight-bearing skeletons like terrestrial animals. Water isalso more viscous than air, and this coupled with the highdensity has resulted in aquatic animals adapting a very stream-lined shape, particularly the carnivores. This makes them veryfast and powerful swimmers, enabling them to catch theirprey.

Many of the adaptations of aquatic organisms have to dowith maintaining suitable conditions inside their bodies. Theliving “machinery” inside most organisms is rather sensitiveand can only operate within a narrow range of conditions.Therefore, aquatic organisms have devised ways to keep theirinternal environments within this range no matter what ex-ternal conditions are like.

ThermoregulationMost aquatic animals are ectotherms, or poikilotherms, or

what is often referred to as “cold-blooded.” As the tempera-ture of the surrounding water rises and falls, so does theirbody temperature and, consequently, their metabolic rate.Many become quite sluggish in unusually cold water. This“slowing down” caused by cold water is a disadvantage for ac-tive swimmers. Some large fish, such as certain tunas andsharks, can maintain body temperatures that are considerably



A Galápagos sea lion (Zalophus californianus wollebaecki) showing itsstreamlined shape enabling dives to catch fish. Photo by Animals An-imals ©T. De Roi, OSF. Reproduced by permission.)

The bowhead whale (Balaena mysticetus) has developed baleen platesto filter the tiny organisms on which it feeds. (Photo by GlennWilliams/Ursus. Reproduced by permission.)

warmer than the surrounding water. They do this by retain-ing the heat produced in their large and active muscles. Thisallows them to remain active even in cold water.

Aquatic mammals are able to keep their body temperaturesmore or less constant regardless of water temperature. Ma-rine mammals deposit most of their body fat into a thick layerof blubber that lies just underneath the skin. This blubberlayer not only insulates them but also streamlines the bodyand functions as an energy reserve. The fusiform body shapeand reduced limb size of many marine mammals and organ-isms decreases the amount of surface area exposed to the ex-ternal environment. This helps conserve body heat. Aninteresting example of this body form adaptation can be seenin dolphins: those adapted to cooler, deeper water generallyhave larger bodies and smaller flippers than coastal dolphins,further reducing the surface area of their skin.

Arteries in the flippers, flukes, and dorsal fins of marinemammals are surrounded by veins. Thus, some heat from theblood traveling through the arteries is transferred to the ve-nous blood rather than the outside environment. This coun-tercurrent heat exchange also helps to conserve body heat.



The Antarctic fur seal (Arctocephalus gazella) and her pup have a thicklayer of blubber to keep them warm. (Photo by Animals Animals©Johnny Johnson. Reproduced by permission.)

The fluke of the humpback whale (Megaptera novaeangliae) has evolved to be wide with scalloped edges, which enables the mammal to reachgreat heights when breaching. (Photo by John K. B. Ford/Ursus. Reproduced by permission.)

The air-breathersSome water birds, such as cormorants and pelicans, sim-

ply hold their breath until completely out of the water. How-ever, it is not appropriate for all air breathers to leave thewater to breathe, especially if only a small portion of themcan do it. This also has two evolutionary advantages: it re-duces the amount of time at the surface of the water so theycan spend more time feeding, and it reduces the amount ofwave drag they encounter. The external nares of aquatic mam-mals, such as beavers, hippopotamuses, and dolphins, are al-ways dorsal in position, and the owner seems always to knowwhen they are barely out of water. A ridge deflects water fromthe blowhole of many whales. When underwater, the naresare automatically tightly closed. Sphincter muscles usually ac-complish this, but baleen whales use a large valve-like plug,and toothed whales add an intricate system of pneumatic sacsso that great pressure can be resisted in each direction.

To avoid inhaling water, aquatic mammals take very quickbreaths. Fin whales can empty and refill their lungs in less

than two seconds, half the time humans take, even though thewhale breathes in 3,000 times more air. Exhaling and inhal-ing takes about 0.3 seconds in bottlenosed dolphins (Tursiopstruncatus). When swimming quickly, many pinnipeds and dol-phins jump clear out of the water to take a breath. Cetaceanshave the advantage of having a blowhole on top of the head.This allows them to breathe even though most of the body isunderwater. It also means that cetaceans can eat and swallowwithout drowning.

The long, deep dives of aquatic mammals require severalcrucial adaptations. For one thing, they must be able to go along time without breathing. This involves more than justholding their breath, for they must keep their vital organs sup-plied with oxygen. To get as much oxygen as possible beforedives, pinnipeds and cetaceans hold their breath for 15 to 30seconds, then rapidly exhale and take a new breath. As muchas 90% of the oxygen contained in the lungs is exchanged dur-ing each breath, in contrast to 20% in humans. Not only dodiving mammals breathe more air faster than other mammals,they are also better at absorbing and storing the oxygen in theair. They have relatively more blood than nondiving mam-mals. Their blood also contains a higher concentration of redblood cells, and these cells carry more hemoglobin. Further-more, their muscles are extra rich in myoglobin, which meansthe muscles themselves can store a lot of oxygen. To aid indiving, marine mammals also increase buoyancy through bonereduction and the presence of a layer of lipids (fats or oils).

Aquatic mammals have adaptations that reduce oxygenconsumption in addition to increasing supply. When theydive, their heart rate slows dramatically. In the northern ele-phant seal, for example, the heart rate decreases from about85 beats per minute to about 12. A bottlenose dolphin’s av-erage respiratory rate is about two to three breaths per minute.



The bottlenosed dolphin (Tursiops truncatus), with its streamlined shapeand powerful tail, can swim at speeds of up to 33.5 mph (54 kph).(Photo by François Gohier/Photo Researchers, Inc. Reproduced by per-mission.)

A manatee’s (Trichechus manatus) heartbeat slows while diving, en-abling it to stay underwater for a longer period of time. (Photo by PhillipColla/Bruce Coleman, Inc. Reproduced by permission.)

Blood flow to nonessential parts of the body, like the ex-tremities and the gut, is reduced, but it is maintained to vitalorgans like the brain and heart. In other words, oxygen ismade available where it is needed most.

Another potential problem faced by divers results from thepresence of large amounts of nitrogen in the air. Nitrogendissolves much better at high pressures, such as those expe-rienced at great depths. When nitrogen bubbles form in theblood after diving, they can lodge in the joints or block theflow of blood to the brain and other organs. Aquatic mam-mals have adaptations that prevent nitrogen from dissolvingin the blood, whereas human lungs basically work the sameunderwater as on land. When aquatic mammals dive, theirlungs actually collapse. They have a flexible rib cage that ispushed in by the pressure of the water. This squeezes the airin the lungs out of the places where it can dissolve into theblood. Air is moved instead into central places, where littlenitrogen is absorbed. Some pinnipeds actually exhale beforethey dive, further reducing the amount of air, and thereforenitrogen, in the lungs.

BuoyancyUnlike fishes, secondary swimmers (terrestrial animals that

returned to an aquatic environment) have no such specificadaptations to the buoyancy problem. They all rely on sim-ple density adaptations to help them. For example, the bones

of diving birds are less pneumatic, and their air sacs are re-duced (loons, penguins). Mammals that dive deep may hy-perventilate before submerging, but they do not fill theirlungs. Indeed, they may exhale before diving. Deep-divingwhales have relatively small lungs. Sirenians, which may feedwhile resting on the bottom or standing on their tails, haveunusually heavy skeletons; their ribs are swollen and solid.Likewise, the skeleton of the hippopotamus is also unusuallyheavy. The presence of blubber in marine mammals also con-tributes to their overall density, and walruses (Odobenidae)have two large air pouches extending from the pharynx, whichcan be inflated to act like a life preserver to keep the animals’head above water while sleeping.

ConvergenceThe largest group of marine mammals, the cetaceans, is

also the group that has made the most complete transition toaquatic life. While most other marine mammals return to landat least part of the time, cetaceans spend their entire lives inthe water. Their bodies are streamlined and look remarkablyfish-like. Interestingly, even though all marine mammals haveevolved from very different evolutionary groups, there arecertain similarities in lifestyle and morphology, and they areconsidered good examples of the principle of convergence.Convergent evolution is the process by which creatures un-related by evolution develop similar or even identical solu-tions to a particular problem; in this case, life in water.



ResourcesBooksEllis, Richard. Aquagenesis. New York: Viking, 2001.

PeriodicalsAlexander, R. McNeill. “Size, Speed, and Buoyancy

Adaptations in Aquatic Animals.” American Zoologist 30(Spring 1990): 189–196.

Butler, Patrick J., and David R. Jones. “Physiology of DivingBirds and Mammals.” Physiological Reviews 77 (1997):837–894.

Fish, Frank E. “Transitions from Drag-based to Life-basedPropulsion in Mammalian Swimming.” American Zoologist36 (December 1996): 628–641.

Graham, Jeffrey B. “Ecological, Evolutionary, and PhysicalFactors Influencing Aquatic Animal Respiration.” AmericanZoologist 30 (Spring 1990): 137–146.

Thompson, David, and Michael Fedak. “Cardiac Responses ofGrey Seals During Diving at Sea.” Journal of ExperimentalBiology 174 (1993): 139–164.

Webb, P. M., D. E. Crocker, S. B. Blackwell, D. P. Costa, etal. “Effects of Buoyancy on the Diving Behavior ofNorthern Elephant Seals.” Journal of Experimental Biology201 (August 1998): 2349–2358.

Gretel H. Schueller

Subterranean mammalsAcross the globe, some 300 (7%) of the extant species of

mammals belonging to 54 (5%) genera and representing 10(7.5%) families of four mammalian orders spend most of theirlives in moist and dark, climatically stable, oxygen-poor andcarbon dioxide-rich, self-constructed underground burrows,deprived of most sensory cues available above ground. The sub-terranean ecotope is safe from predators, but relatively unpro-ductive and foraging is rather inefficient. These mammals arefully specialized for their unique way of life in which all theforaging, mating, and breeding takes place underground. Theseanimals are called “subterranean” (“sub” means under, and“terra” means earth or soil), whereas animals that construct ex-tensive burrow systems for shelter but search for their food(also) above ground are denoted “fossorial” (“fossor” meansdigger). Of course, there is a continuum from fossorial throughfacultative subterranean to strictly subterranean lifestyles.

The subterranean niche opened to mammals in the upperEocene (45–35 million years ago [mya]) and then extendedinto upper Tertiary (Oligocene and Miocene, i.e., 33.7–5.3mya) and Quaternary (some two mya) when in the course ofglobal cooling and aridization, steppes, savannas, semi-deserts, and deserts expanded. In seasonally dry habitats, nu-merous plants (the so-called geophytes) produce undergroundstorage organs (bulbs and tubers) that can be a substantialsource of food for herbivorous animals. (Underground stor-age organs of some plants such as potatoes, sweet potatoes,yams, cassava, etc. are among the most important human sta-ple foods.) There have been several waves of adaptive radia-tion when, independently in space and time, mammals indifferent phylogenetic lineages occupied the undergroundniche either to feed on geophytes (in the case of rodents) orto feed on invertebrates, which themselves find food and shel-ter underground (in the cases of insectivores, armadillos, andmarsupial moles). Thus, two morphological and ecologicalsubtypes of subterranean mammals have evolved. Neverthe-less, they all have been subjected to similar environmentalstresses and, as a consequence, have much in common. Al-though the subterranean ecotope is relatively simple, monot-onous, stable, and predictable in many aspects, it is veryspecialized and stressful in others. Consequently, the adap-tive evolution of subterranean mammals involves structuraland functional changes, which are both regressive (degener-

ative) and progressive (compensatory) in nature. The mosaicconvergent global evolution of subterranean mammals due tosimilar constraints and stresses is a superb example of evi-dence for evolution through natural selection, evidence ob-tained through comparative methods.

Who cares about subterranean mammals?Although at least some of the underground dwellers have

been known for many years, their biology has remained un-studied. This may be explained by the cryptic way of life of sub-terranean animals, and technical problems related with keeping,breeding, and observing them. The fact is, scientists were al-ways more fascinated by animals coping with complicated en-vironments and solving seemingly difficult and complexproblems than by those encountered by mammals underground(sensitive vision versus blindness; echolocation in a high-frequency range versus hearing in a human auditory range; navigating across hundreds or thousands of miles versus mazeorientation across tens of feet; thermoregulation in cold envi-ronments versus life in a thermally buffered burrow, etc.). In-terestingly, although many preserved specimens of moles (i.e.,insectivorous subterranean mammals) and mole-rats (subter-ranean rodents) have been collected and deposited in museums,not even the study of morphological digging specializations hasreceived the attention it has deserved. Textbooks of biology ingeneral and evolutionary biology in particular have brought di-verse examples for convergent evolution, yet one of the mostremarkable examples—convergent evolution of subterraneanmammals—has rarely been mentioned.

It may be of interest to examine the literature dealing withecology, evolution, morphological, physiological, and behav-ioral adaptations of subterranean mammals. Although thereare some relevant scientific papers published as early as at thebeginning of the nineteenth century, the real exponentialgrowth of the research and publishing activity referring to sub-terranean mammals started in the 1940s. Since then, the num-ber of publications has doubled about every 10 years. Thus,56% of about 1,300 scientific papers addressing at least partlyadaptations of subterranean mammals and published to date(March 2003) appeared after 1990, a further 25% are dated1981 to 1990, and another 11% appeared between 1971 and1980. The interest in adaptations of subterranean mammals


• • • • •

Adaptations for subterranean life

has been triggered particularly by two seminal papers on theblind mole-rat, Spalax, published in 1969, both authored orco-authored by Eviatar Nevo of the University of Haifa. In1979, a review article (which has since become a citation clas-sic) by Nevo stimulated considerable research into the phys-iology, sensory biology, communication, temporal and spatialorientation, ecology, taxonomy, and phylogeny of burrowingrodents. A second stimulus triggering the interest in subter-ranean mole-rats, particularly in their social behavior, camein 1981 with the pioneering studies of Jennifer U. M. Jarvis,when she reported on eusociality in the naked mole-rat, andin 1991, when a book was published on the evolution and be-havioral ecology of naked mole-rats and related bathyergids.Since then, several international symposia on subterraneanmammals have been convened and four books in English werepublished by renowned publishing houses within just twoyears (1999–2001).

Biased knowledgeStill, general knowledge on the subject is rather incom-

plete and heavily biased in several aspects. Most of the arti-

cles have been authored and co-authored by very few personsor research teams. Thus, 31% (410 out of 1,300) of the sci-entific papers bear a signature of one or more of just five au-thors (Bennett, Burda, Heth, Jarvis, and Nevo), while the mostinfluential of them, Eviatar Nevo, has authored or co-authored 225 of them. As a consequence—since every scien-tist observes the world through her/his own eyes and is constrained by her/his own research possibilities (professionaltraining, knowledge and experience, interests, affiliation, ge-ography, available funding, etc.)—the research has many bi-ases. Although the validity of the published data and findingsis not questioned, their interpretation may be influenced byscience’s limited knowledge and/or ideology molded by thephilosophy of the author and the world she/he lives in. How-ever, this is a general problem of scientific research.

The taxonomic treatment is uneven in that almost 85% ofall the papers on subterranean mammals and their adaptationsdeal with just a few species belonging to 10 (out of 54) genera(Arvicola, Cryptomys, Ctenomys, Geomys, Heterocephalus, Spalaco-pus, Spalax, Geomys bursarius, Talpa, and Tachyoryctes). Some ofthe species, like the mole (Talpa europaea), the northern water


Vol. 12: Mammals IAdaptations for subterranean life

The common mole-rat (Cryptomys hottentotus) has a oval-shaped bodywith short legs to enable it to move through small tunnels. (Photo by© Peter Johnson/Corbis. Reproduced by permission.)

The star-nosed mole (Condylura cristata) uses its snout and tentaclesas touch receptors. (Photo by Dwight Kuhn/Bruce Coleman, Inc. Re-produced by permission.)

vole (Arvicola terrestris), and pocket gophers (Geomyidae), havebeen studied to a much greater extent than considered here;yet most of the earlier studies on these animals have not specif-ically addressed subterranean adaptations. Usually, few specieswithin (mostly) speciose genera have been studied in only afew localities within a broader geographic and ecological rangeof distribution. Studies are biased also as to which aspect of bi-ology (and from which point of view) has been investigated.Thus, the (about 150) articles on the naked mole-rat (Hetero-cephalus glaber) primarily concentrate on the spectacular socialbehavior of this species, and some authors are prone to thinkof the naked mole-rats as if they were the only subterraneanmammals. In spite of the fact that the naked mole-rat has at-tracted such intense interest by sociobiologists, only some 7%of all studies published on this species involved field ecologi-cal research and/or investigation of wild-captured animals.Most information on (social) behavior of the naked mole-rathas been based on the study of captive colonies. Yet, as S.Braude has demonstrated recently, long-term intensive and ex-tensive field research may lead, at least in some aspects, to dif-ferent results than the short-term study of captive animals.Interestingly, the problem of why the naked mole-rat is hair-less (on both proximate and ultimate levels) has received verylittle attention from scientists. Similarly, although the questionof whether subterranean mammals are blind or not (and if so,why do they still have miniscule eyes?) has been pertinent sinceAristotle, the answer for most species is not yet known.

How to get through?The most significant challenge is a mechanical one: soil is

a dense, more or less hard and compact medium that cannot

be penetrated easily. Movement through soil is energeticallyvery costly. Vleck (1979) has estimated that a 5.3-oz (150-g)pocket gopher burrowing 3.3 ft (1 m) may expend 300–3,400times more energy than moving the same distance on the sur-face. To keep the energy costs of burrowing at the minimum,the tunnel should have a diameter as small as possible. Toachieve this, subterranean mammals have a cylindrical bodywith short limbs and no protruding appendages. Even testesof most underground dwellers are seasonally or permanentlyabdominal. Subterranean mammals are mostly small-sized an-imals weighing 3.5–7 oz (100–200 g), but ranging from 1 oz(30 g) (Namib golden mole, naked mole-rat, and mole-vole)to 8.8 lb (4 kg) (bamboo rat). In order to penetrate the me-chanically resistant medium, subterranean mammals need ef-ficient digging machinery. Subterranean rodents dig (loosensoil) primarily with their procumbent, ever-growing incisors,or use teeth and claws, whereas subterranean insectivores, ar-madillos, and the marsupial mole use only robust, heavilymuscled and large-clawed forelimbs. In teeth-diggers, thewhole skull is subservient to incisors and well-developedchewing muscles. Interestingly, subterranean rodents belong-ing to the suborder Hystricognathi (Bathyergidae, Octodon-tidae) transport loosened soil backwards by pushing or kickingthe soil with hind limbs, whereas representatives of the sub-order Sciurognatha (Muridae, Geomyidae) turn in the bur-row and push out the loosened soil with the head. Desertgolden moles as well as the marsupial mole do not dig per-manent tunnels (except for their nest burrow), but “swim”through the sand. Although sand-swimming requires less thana tenth of the energy required by mammals that dig perma-nent tunnels through compact soil, it is still much more ex-pensive than running on the surface. Sand-swimming at amean velocity of 25–97 ft/h (7.6—29.6 m/h) (as recently es-timated for the Australian marsupial mole [Notoryctes typhlops]


Adaptations for subterranean lifeVol. 12: Mammals I

The Columbian ground squirrel (Spermophilus columbianus) spendsthe majority of its time hibernating in underground burrows. (Photo byFrançois Gohier/Photo Researchers, Inc. Reproduced by permission.)

The eastern mole (Scalopus aquaticus) has no external ears and athin layer of skin protects its eyes. (Photo by Kenneth H. Thomas/PhotoResearchers, Inc. Reproduced by permission.)

and Namib desert golden mole [Eremitalpa granti], respec-tively) is also substantially slower than walking or runningabove ground (about 1,476 ft/h [450 m/h]). It would appar-ently be energetically impossible for these mammals to ob-tain enough food by foraging only underground. Indeed, inone study of free-living Namib desert golden moles, the meandaily track length was 0.87 mi (1.4 km), but only 52.5 ft (16m) of it was below the surface.

Subterranean mammals can move backwards with the sameease as forwards. The skin is usually somewhat slack, and thefur tends to be short and upright, brushing in either direction.These all may be burrowing adaptations to match frictionalresistance, to facilitate moving and turning in tunnels. The ex-tremes such as the total alopecia (hairlessness) of the nakedmole-rat or the long hairs and thick pelage of the silvery mole-rat (Heliophobius argenteocinereus) are exceptions to the rule andshould not be considered burrowing adaptations per se. Re-duction or even absence of auricles (pinnae) may be beneficialfor digging and moving in tunnels because of the reduced fric-tion. The popular assumption that auricles are reduced ormissing because, otherwise, they would have to act as shovelscollecting all the dirt cannot withstand critical comparativeanalysis. Many burrowing rodents have rather prominent au-ricles and are apparently not handicapped. Probably more im-

portant than whether auricles are an advantage or disadvan-tage for burrowing is whether they are required for sound lo-calization. If not needed for hearing, only then would they bereduced. The tail tends to be shortened in subterranean andfossorial mammals, yet there is no clear explanation as to theadaptive value of this feature. For instance, African mole-ratsof two related genera, Heterocephalus and Cryptomys, differ inthis trait markedly. Similarly, fossorial-subterranean octodon-tids have medium-sized tails, whereas related surface dwellingcavies have reduced tails. Vibrissae in subterranean mammalsare also shorter and less protruding than in many surfacedwellers. In sand-swimming golden and marsupial moles, theyare inconspicuous, sometimes even missing.

How to acquire oxygenSubterranean mammals also have to cope with problems

from the burrow atmosphere. The oxygen concentration maybe as low as 6%, compared to 21% prevailing in the ambientatmosphere at sea level altitude. This means that the oxygenconcentration even a few inches underground may be lowerthan that on Mount Everest. The carbon dioxide concentra-tion in burrows ranges between 0.5–13.5% (compared to0.03% in the above ground atmosphere). Surprisingly, some



The naked mole-rat (Heterocephalus glaber) has hair between its toes that sweeps the dirt out of the pathways in its burrow. (Photo by J.Visser/Mammal Images Library of the American Society of Mammalogists.)

recent measurements in foraging tunnels of three species ofAfrican mole-rats have revealed, however, that concentrationsof oxygen and carbon dioxide did not differ greatly from ambient values above ground. Nevertheless, gas concentra-tions may change rapidly after rains, they may differ in dif-ferent soil types and depths, and, above all, they must changedramatically in the immediate vicinity of the nose of a bur-rowing animal. Normally, there are no air currents in under-ground burrows. One can imagine that an animal movingthrough the narrow tunnel acts like a piston securing the ven-tilation of burrows, much like a train in a subway tunnel. Assuggested by Arieli, who significantly contributed to knowl-edge of respiratory physiology of mole-rats, enhanced bur-rowing activity following rains may serve as a means ofreplenishing the burrow atmosphere when the hypoxic-hy-percapnic situation becomes aggravated. Of course, workingunder such conditions becomes even more difficult.

Whereas adaptations to extreme atmospheric conditionshave been extensively studied in diving mammals and in mam-mals living at high altitudes, much less is known in this regardabout subterranean mammals. The combination of extremehypercapnia and hypoxia normally encountered and toleratedby subterranean animals is unique. Interestingly, whereas sur-face dwellers respond to hypercapnic conditions by increasingbreathing frequency, subterranean mammals display lowerventilation rates than would be expected. In fact, ventilationis not effective for releasing carbon dioxide from blood whenthere is a high concentration of it in the inspired gas. Thelungs of subterranean mammals do not show any specific mor-phological specializations—on the contrary they seem (at leastin the few species studied so far) to be rather simplified andjuvenile-like. Although the oxygen transport properties ofblood vary markedly among subterranean mammals, and nogeneralizations can be made, relatively high hemoglobin affin-ity for oxygen has been reported consistently for several speciesof subterranean rodents. Because of the higher amount of car-bon dioxide inhaled, a higher concentration of this gas in theblood and, thus, also higher blood acidity can be expected. Ithas been shown in the blind mole-rat that urine contains highvalues of bicarbonates and may serve as a pathway to bind andvoid carbon dioxide. Further adaptations to the extreme bur-row atmosphere may involve higher capillary density in mus-cles (including the heart), higher volume of musclemitochondria (found in the blind mole-rat), and, particularly,low metabolic rates and relaxed thermoregulation.

How to regulate temperatureThe microclimate of the subterranean ecotope is rather

stable. Particularly in the nest chamber, which in giant Zam-bian mole-rats (Cryptomys mechowi) is usually 23.6 in (60 cm)(in some cases, even 6.6 ft [2 m]) below ground, there areminimal daily or seasonal fluctuations in temperature and hu-midity. This constant temperature enables a lower basal rateof metabolism. In the thermally buffered environment of theunderground “incubator,” it is possible to abandon complexand complicated morphological and physiological mecha-nisms of thermoregulation. Indeed, subterranean mammalstend to hypothermia (lowering the body temperature—on av-erage 89.6–96.8°F [32–36°C]). Body temperature is partly de-

pendent upon the ambient temperature. This relaxed ther-moregulation (heterothermia) is most pronounced in thesmallest (and the only hairless representative) among the sub-terranean mammals, the naked mole-rat. High relative hu-midity (about 93%) in underground burrows results in arelatively low vapor pressure gradient and low rate of waterloss through exhalation or through the skin. This is benefi-cial for water balance as these animals do not drink free wa-ter, but instead obtain water from the food they consume.

However, high humidity and relatively high temperatures,which can occur on sunny days in shallow foraging burrows,may result in thermoregulatory problems. In the absence ofevaporative and convective cooling, overheating and thermalstress would seem to be inevitable, since burrowing is ener-getically demanding and most mammals can tolerate dry,warm climate better than humid, warm climate. Subterraneanmammals living in warmer environments have high thermalconductance, which means that the animals may exchangeheat (cool or warm themselves) relatively easily through di-rect physical contact between themselves and the soil. As inpoikilothermic reptiles, behavioral thermoregulation is of par-ticular importance in heterothermic mammals. Thus, the an-imals can adapt timing and duration of their working activityto ambient temperatures in shallow burrows. Comparativeand experimental physiological research of thermoregulationand energetics has a long tradition since McNab in 1966 firstcompared the metabolic rate of five subterranean rodentspecies and emphasized their shared adaptive convergencesyndrome: low resting metabolic rate (involving also lower



The European mole (Talpa europaea) uses its long claws to dig its bur-rows. (Photo by Hans Reinhard/OKAPIA/Photo Researchers, Inc. Re-produced by permission.)

ventilation and heart rates than would be expected on the ba-sis of body size), low body temperature, and high thermal con-ductance. Since then, additional physiological data have beenobtained on diverse species of subterranean mammals sup-porting the earlier conclusions by McNab.

How to avoid ricketsThe underground ecotope is dark. Apart from the conse-

quences for sensory orientation and communication, absenceof light also influences some physiological functions. One ofthem is mineral metabolism. On the one hand, subterraneanrodents have an especially high requirement for calcium be-cause their large teeth are constantly worn down during dig-ging. In the African mole-rat, Cryptomys, the visible part ofthe incisors regenerates completely every week. Also, calciummay be excreted in high concentrations as calcium carbonatethrough urine, a mechanism to deplete tissues of carbon diox-ide. On the other hand, it is common knowledge that vita-min D (and principally D3, cholecalciferol), which is neededfor effective absorption of calcium from the gut (its deficiencycauses rickets), is synthesized in the skin by the action of sun-light. Rochelle Buffenstein and colleagues have demonstratedthat several species of African mole-rats, although in the per-petual state of vitamin D3 deficiency due to their lightless en-vironment, have evolved other physiological mechanisms toabsorb calcium effectively (indeed, up to 91% of minerals canbe extracted) from their diet.

How to tell timeLight-dark rhythm (photoperiod) is known to regulate

production of the hormone melatonin that, in turn, regulatescircadian (meaning around a day, as in a 24-hour period)rhythms by a feedback mechanism. In surface-dwelling ver-tebrates (including human), melatonin is produced during

dark hours. It can therefore be expected that subterraneanmammals living in constant darkness would display high mela-tonin levels. This does seem to be the case, yet the role ofmelatonin in regulating activity rhythms in subterranean an-imals remains obscure.

Permanent darkness in subterranean burrows makes sightand eyes rather useless and, apart from the fact that it pre-cludes visual orientation in space, it also makes orientationin time problematic. Virtually all surface-dwelling mammalsexhibit more or less pronounced circadian cycles of activityand diverse functions. These cycles are maintained by an en-dogenous pacemaker synchronized (entrained) by the so-called zeitgeber (time-giver). The most universal zeitgeber isthe light-dark cycle perceived by photosensors. Consideringthe stability of the environment, constant availability of plantfood, darkness underground, and poor sight or even blind-ness, one might expect that herbivorous subterranean rodentswould not exhibit distinct diurnal activity/sleeping patterns.Field and laboratory studies on American pocket gophers(Geomys bursarius and Thomomys bottae) and African mole-rats(Heliophobius argenteocinereus and Cryptomys hottentotus) haverevealed dispersed activity occurring throughout the 24hours, for instance, arhythmicity and lack of distinct sleep-wake cycles. Interestingly, there are some other species ofsubterranean rodents that exhibit endogenous circadian ac-tivity rhythms that are free running in constant darkness andsynchronized by light-dark cycles. These animals have beenfound to be either mostly diurnal such as the east Mediter-ranean blind mole-rat (Spalax ehrenbergi species complex), theEast African mole rat (Tachyoryctes splendens), and the Kala-hari mole-rat (Cryptomys damarensis); or predominantly noc-turnal such as the African mole-rats (Georychus capensis andHeterocephalus glaber) and the Chilean coruro (Spalacopuscyanus).

There is no apparent correlation between the circadianactivity pattern, on the one hand, and the degree of con-finement to subterranean ecotope, development of eyes, sea-sonality of breeding, or social and mating systems, on theother. It should be noted, however, that findings in the samespecies have frequently been inconsistent. Available data havebeen obtained by different examination methods and may notbe fully comparable. Moreover, there may be differences be-tween individuals, sexes, and populations, between seasons ofthe year and habitats, as well as between the laboratory andthe field. The methodological problem can be demonstratedin the example of the naked mole-rat, which had been con-sidered to be arrhythmic by previous authors, yet was shownto display clear circadian rhythms and ability to synchronizethem by the light-dark cycle if given an opportunity to workon a running wheel in the laboratory. There is a similar find-ing in Cryptomys anselli. Further studies of activity patternsin other species of mammals are clearly needed. A possiblezeitgeber determining digging activity can be also tempera-ture and humidity, which may fluctuate in shallow tunnels(although certainly not in deep nest chambers), as well asconsequent changes in activity of invertebrates, which mayaffect foraging activity of moles.

The blind mole-rat, which is visually blind and has de-generated eyes, still has a hypertrophied retina and a large



The lips of the valley pocket gopher (Thomomys bottae) close behindits teeth to keep dirt out. (Photo by Tom McHugh/Photo Researchers,Inc. Reproduced by permission.)

harderian gland in which the so-called circadian genes as wellas the recently discovered photopigment melanopsin are ex-pressed in high concentrations, and these apparently con-tribute to regulation of photoperiodicity. In other words, thedouble function of any vertebrate eye changed: instead of sightand circadian functions, only a circadian eye remains.

The ability to perceive and recognize the length of thephotoperiod is important for seasonal structuring of repro-ductive behavior. It has also been suggested that melatoninmay suppress production of gonadotrophins, hormoneswhich, in turn, control activity of gonads and, thus, the sex-ual behavior and reproductive biology. Nothing is knownabout this aspect in subterranean mammals. Also unclear ishow circannual (approximately one year) cycles are synchro-nized in subterranean mammals. These cycles are associatedparticularly with seasonal breeding in solitary territorial ani-mals. It is assumed that the length of the photoperiod mayplay a role in seasonal breeders from temperate zones. Nev-ertheless, factors triggering breeding in mammals with longgestation from the tropics (where there is minimal variabilityin the daylight throughout the year) remain unknown andenigmatic in many cases. This is also the case for the easternAfrican silvery mole-rat. Alternating rains and drought rep-resent the main periodic environmental factor. However, asshown recently, mating takes place at the end of the rainy andbeginning of the dry season so that there is a substantial lagbetween the onset of rains (and subsequent softening of thesoil and change of vegetation that could provide a triggeringsignal) and onset of breeding behavior.

How to find the waySubterranean mammals construct, occupy, and maintain

very long and extensive burrow systems. An average subter-ranean mammal (single, weighing 5.3 oz [150 g]) controlsabout 203 ft (62 m) of burrows. Of course, there are species-specific, habitat, and seasonal differences. This also impliesthat an average mole-rat living in a group consisting of 10family members has to be familiar with at least 2,034 ft (620m) of burrows. The longest burrow systems were found inCryptomys mole-rats and coruros. Yet, the burrow system is acomplicated, complex, three-dimensional network. Althoughthere is evidence that subterranean mammals have an extra-ordinary spatial memory based on well-developed kinestheticsense (controlled, in part, by sensitive vestibular organs), thisfact does not explain how subterranean mammals can steerthe course of their digging and what, in absence of visual land-marks, is the nature of external reference cues for the kines-thetic sense. In 1990, the first evidence that Zambianmole-rats (Cryptomys anselli) show directional orientationbased upon the magnetic compass sense was published. In alaboratory experiment, mole-rats collected nest materials andbuilt a nest in a circular arena. They showed a spontaneoustendency to position their nests consistently in the southeastsector of the arena. When magnetic north was shifted (bymeans of Helmholtz coils), the animals shifted the positionof the nest accordingly. This laboratory experiment on mole-rats has become the first unambiguous evidence for magneticcompass orientation in a mammal and a paradigm for furthertests of magnetic compass orientation in small mammals.

Convergent spontaneous directional magnetic-based prefer-ence for location of nests in the laboratory was demonstratedalso in taxonomically unrelated blind mole-rats from Israel.In 2001, Nemec and associates observed, for the first time ina mammal, structures in a brain (populations of neurons incolliculus superior), which are involved in magnetoreceptionin Cryptomys anselli.

The problem of orientation underground was addressed asrecently as 2003, when it was reported that blind mole-ratscould avoid obstacles by digging accurate and energy-con-serving bypass tunnels. Apparently, the animals must possessboth the means to evaluate the size of the obstacle as well asthe ability to perceive its exact position relative to the origi-nal tunnel that it will rejoin. At present, information aboutpotential sensory mechanisms can be only speculated.

How to find foodSubterranean mammals are animals that live and forage

underground. However, the underground ecotope is low inproductivity, burrowing is energetically demanding, and, inaddition to these costs, foraging seems to be inefficient. It iswidely assumed that subterranean rodents must forage blindlywithout using sensory cues available to and employed by sur-face dwellers. Indeed, vision is ineffective underground, thereare no air currents to transmit airborne odorants over longerdistances, high frequency sounds are damped by the soil, andlow frequencies cannot be localized easily; touch and taste areonly useful on contact. Carnivorous and/or insectivorous subterranean mammals such as moles can dig a stable forag-ing tunnel system into which prey may be trapped. Moles run-



The black-tailed prairie dog (Cynomys ludovicianus) is well known forits large burrows. (Photo by Tim Davis/Photo Researchers, Inc. Re-produced by permission.)

ning along existing burrows can locate prey by hearing theirmovement in the tunnel system. Prey animals may also leavescent trails that the insectivorous predator can follow. In mostcases, the food is detected at encounter or in the immediatevicinity through touch. The most spectacular example for thistype of foraging is the star-nosed mole (Condylura), with itsEimer-organ-invested rostral tentacles. Mason and Narinshave shown that the Namib golden mole may use low-fre-quency vibrations produced by isolated hummocks of dunegrass and orient its movement toward the hummocks and theinvertebrate prey occurring there. However, in contrast to theprey of moles, tubers, bulbs, and roots are stationary andsilent.

It has been demonstrated that subterranean rodents areable to dig in relatively straight lines until they encounter afood-rich area and then make branches to their tunnels toharvest as much as possible from this area. Tunneling in rel-atively straight burrows conserves energy because the animalsdo not search in the same area twice. Because geophytes aregenerally distributed in clumps and patches, extensive bur-rowing around one geophyte upon encountering it increasesthe chances of encountering another. Although this dual strat-egy has been described and its functional meaning recognizedin different species of subterranean rodents, sensory mecha-

nisms that may underlie the switch from linear to reticulatedigging have not been addressed until a recent study. It hasbeen shown that subterranean rodents can smell odorous sub-stances leaking from growing plants and diffusing around theplant through the soil. Thus, herbivorous mammals are ableto identify the presence of the plants and possibly even toidentify particular types of plants specifically. They may beable to orient their digging toward areas that are more likelyto provide food sources.

How to find a partnerIn order to reproduce, mammals have to find and recog-

nize an appropriate mate (belonging to the same species, op-posite sex, adult, in breeding mood, sexually appealing).Monogamous mammals undergo this search once in life; soli-tary mammals have to seek mates each year. Subterraneanmammals do not differ in this respect from their surface-dwelling counterparts. In 1987, two research teams reported,simultaneously and independently, the discovery of a new, pre-viously unconsidered, mode of communication in blind mole-rats: vibrational (seismic) signaling. The animals can putthemselves into efficient contact through vibrational signalsproduced by head drumming upon the ceiling of the tunnel.Communicative drumming by hind feet was reported for soli-tary African mole-rats (Georychus and Bathyergus). This be-havior, however, could not be found in another solitary Africanmole-rat, the silvery mole-rat (Heliophobius). It can be specu-lated that seismic signaling evolved in those solitary speciesthat disperse and look for potential mates underground. Sub-terranean mammals that usually occur at lower populationdensities and whose burrow systems are far apart from eachother have to cover larger distances (which would be impos-sible to do by digging) in order to find a partner. They dareto carry out their courting above ground. These mammals suchas the silvery mole-rat, the naked mole-rat, or the Europeanmole have not invented seismic communication. Moles wan-dering at the surface in hopes of finding a burrow of a femaleprobably are led by olfactory signals.

Seeing, or not seeingSensory perception plays a pivotal role not only in spatial

and temporal orientation, foraging, and recognition of food,but also in communication with conspecifics. Like their sur-face dwelling counterparts, subterranean animals also mustfind and recognize a mate, recognize kin or intruders, andbe warned of danger. This all is very difficult in a monoto-nous, dark world where transmission of most signals and cuesis very limited. Some senses such as sight are apparently use-less, whereas others have to compensate for their loss. Oneof the most prominent features of subterranean mammals is,no doubt, reduction of eyes and apparent blindness. Thequestion of whether and what subterranean mammals see hasbeen studied by Aristotle, Buffon, Geoffroy, Cuvier, and Dar-win, among others. Still, today, no general unambiguous re-ply can be given. Thus, for instance, in comparing two of themost specialized subterranean rodents, the east Mediter-ranean blind mole-rat (Spalax) and the African mole-rat(Cryptomys), both are strictly confined to the underground



The thumb of the alpine marmot (Marmota marmota) has a nail in-stead of a claw to aid in digging. (Photo by St. Meyers/Okapia/PhotoResearchers, Inc. Reproduced by permission.)

and are of similar appearance, externally. They both havevery small eyes and they both are behaviorally blind, yetwhereas the eyes of the blind mole-rat are structurally de-generated and lie under the skin, the eyes of the African mole-rat are prominent, only miniaturized but in no respectdegenerate; on the contrary, they are fully normally devel-oped. As has been shown by several research groups, theyalso use different kinds of cone-pigments. Whereas the de-generated subcutaneous eye of the blind mole-rat has appar-ently adapted to a function in circadian photoreception, thefunction of a normally developed eye of the African mole-rat remains enigmatic.

Interestingly, whereas spalacines and bathyergids in theOld World lost their sight and have become completely sub-terranean, their New World counterparts, geomyids andoctodontids, converged to similar habitats and habits retain-ing their eyes and sight. Unfortunately, the eyes and the sightof most subterranean mammals have not yet been studied.

As do blind people, blind subterranean mammals compen-sate for loss of sight by well-developed somatosensory percep-tion, which was shown in the blind mole-rat, in the star-nosedmole, and in the naked mole. This somatosensory perceptionis over-represented also in the brain cortex where it occupiesareas dominated in seeing mammals by visual projections.

How to hear undergroundFor communication and orientation in darkness, acoustic

signals seem to be predestined, as exemplified by bats and dol-phins. However, high sound frequencies (characterized byshort wavelength), which can be well localized by small mam-mals and which are employed in echolocation, are quicklydampened underground. Low frequency sound, on the otherhand, is characterized by long waves and cannot be localizedeasily. Indeed, it was demonstrated that, in a burrow of theblind mole-rat, sounds with a frequency of about 500 Hz weremore efficiently transmitted than sounds of low and higherfrequencies. Although nothing is known so far about the ef-fect of the tunnel diameter, soil characteristics, temperature,and humidity, it is assumed that acoustic features of all bur-rows are rather similar. Consistent with the results of thesemeasurements, the vocalization of all nine species (represent-ing six genera) of subterranean rodents studied so far was alsotuned to a lower frequency range. Corresponding withacoustics of the environment and with vocalization charac-teristics, the hearing of five species (of five genera) of sub-terranean mammals studied exhibited its highest sensitivity inthe lower frequency range (0.5–2 kHz). This is quite unusualamong small mammals, because hearing and vocalization inrelated surface dwellers of a comparable body size are usuallymuch higher: about 8–16 kHz, or higher. The hearing rangeof subterranean mammals is very narrow, and frequencies ofabout 16 kHz and higher cannot be perceived (similar to hu-mans). Frequency of 500 Hz is characterized by a wavelengthof 27 in (68.6 cm). To be able to localize this frequency (towhich hearing is tuned), an animal would need to have a headof a corresponding width; this is not possible. However, thetransmission of airborne sounds in a tunnel is unidirectional,anyway. Consequently, animals that are confined to their un-

derground burrows do not need auricles for directional hear-ing. Some scholars would tend to label this restricted hear-ing as degenerated. However, looking at the morphology ofthe middle and inner ear, many progressive structural spe-cializations enabling tuning of hearing to the given lower fre-quency range are observed. Indeed, several papers havedescribed diverse morphological features of the middle andinner ear, as well as the expansion of auditory brain centers,which can be found consistently in non-related species of un-derground mammals and provide an example of convergentevolution. However, while the ear is clearly a low-frequency-tuned receiver, apparently the evolution has not fully utilizedall the possibilities, as demonstrated in ears of desert animals,to enhance the sensitivity. On the contrary, some features ofthe external ear canal, eardrum, and middle ear ossicular chainindicate that sensitivity has been secondarily and actively re-duced. Too little is known about the acoustics of burrows,and also the suggestion of Quilliam, 40 years ago, that soundin burrows can be amplified as in an ear-trumpet, has not yetbeen tested. Should there really be such a stethoscope effect,reduction of sensitivity (in order to avoid deafening) wouldhave to be considered an adaptation in the same way as its in-crease is in other species.

How to avoid tetanusHumid, thermally stable soil swarms with many microor-

ganisms (bacteria, fungi, protozoans), eggs, and larval stagesof diverse helminths and arthropods, many of which arepathogens. A renowned representative is Clostridium tetani, a



The European badger (Meles meles) builds onto underground tunnels,or setts, inherited from previous generations which results in settsthat can be centuries old. (Photo by Roger Wilmshurst/Photo Re-searchers, Inc. Reproduced by permission.)

bacterium that is particularly prevalent in soil contaminatedwith animal droppings and that, after entering wounds, causesa serious disease, tetanus. Subterranean mammals are para-sitologically understudied, and the results are inconsistent anddo not allow any generalization. Many more factors probablyinfluence whether an animal will be infected or infested byparasites. Higher lung infection by adiaspores of Emmonsiaparva was reported in burrowing voles, as compared to moresurface-dwelling mice. Yet, the preliminary examination ofSpalax and Cryptomys provided variable, inconsistent results.The ectoparasites in African mole-rats are, however, very rare,and infestation with endoparasitic helminths is unusual.Surely, the examination of the immune system of subter-ranean mammals may be of great interest and importance forhuman medicine. At least, the few existing studies of Spalaxdo suggest the opening of new research horizons.

Living in a safe, predictable worldThe underground ecotope is not only challenging, it is also

quite safe from predators. Certainly, naked mole-rats wouldnot be able to survive in any other ecotope than in the safe,humid, and ultraviolet-light-protected underground burrows.No wonder that convergent patterns can be seen also in lifehistories of subterranean mammals. They all show tendenciesto K-strategy, breed rather slowly, have slow and long pre-natal and postnatal development, slow rates of growth, and

unusually long lifespans (an age of over 25 years has beenrecorded in the naked mole-rat in captivity, and there is anAfrican mole-rat, Cryptomys anselli, that is at least 22 years oldand is still breeding). On the proximate level, slow growth issurely correlated with low metabolic rates. However, the ef-fect of phylogeny is very strong and phylogenetic relation-ships can best explain the length of pregnancy and many otherparameters of life histories, such as mating behavior and mat-ing system, as well as social systems.

In spite of all the similarities of the subterranean ecotope,there are differences in many of its biotic and abiotic para-meters in different geographic regions and different habitats,which in turn also influence underground dwellers. Thus, sub-terranean mammals may serve not only as an example for con-vergent evolution but they provide cases to study adaptivedivergence as well.

Last, but not leastLast, but not least, it should be mentioned that 40 million

years of evolution underground, including hypoxia tolerance,light absence, etc., may prove important to biomedical re-search and human gene therapy. Subterranean mammals maybecome unique laboratory and model animals of the next gen-eration.



ResourcesBooksBennett, Nigel C., and Chris G. Faulkes. African Mole-rats.

Ecology and Eusociality. Cambridge, UK: CambridgeUniversity Press, 2000.

Lacey, Eileen A., James L. Patton, and Guy N. Cameron, eds.Life Underground. The Biology of Subterranean Rodents.Chicago: University of Chicago Press, 2000.

Nevo, Eviatar. Mosaic Evolution of Subterranean Mammals:Regression, Progression and Global Convergence. Oxford:Oxford University Press, 1999.

Nevo, Eviatar, and Osvaldo A. Reig, eds. Evolution ofSubterranean Mammals at the Organismal and MolecularLevels. New York: Wiley-Liss, 1990.

Nevo, Eviatar, Elena Ivanitskaya, and Avigdor Beiles. AdaptiveRadiation of Blind Subterranean Mole Rats. Leiden: BackhuysPublishers, 2001.

Sherman, Paul W., Jennifer U. M. Jarvis, and Richard D.Alexander. The Biology of the Naked Mole-rat. Princeton,New Jersey: Princeton University Press, 1991.

Hynek Burda, PhD

IntroductionMammals, like other animals, can be expected to use what-

ever information is available to them when making decisionsabout activities such as foraging, mating, navigating, select-ing shelter, or locating habitats. The range of information ac-tually used by any one species can be predicted from itssensory apparatus—the stimuli they can perceive. Lifestyleplays an important role here, so that moles and other fosso-rial (also known as subterranean) mammals, including goldenmoles, some rodents, and at least one species of marsupial,can be expected to use vision less than species that are activeaboveground, including the lion (Panthera leo), vervet mon-key (Cercopithecus aethiops), or moose (Alces alces). Everyonewho has walked a dog (Canis familiaris) or experienced thespraying of a male housecat (Felis cattus) knows the impor-tance of odor in the lives of these mammals. The importantrole that sound plays in the lives of mammals becomes obvi-ous when listening to the echolocation calls of a bat attack-ing an insect or to the bugling of a male elk (Cervus elaphus)during the rut.

The media

Vision

Most of the 5,000 or so living species of mammals have eyesand, in many, the keenness of their vision (visual acuity) is atleast equivalent to that of humans. A few mammals have verylimited vision, such as river dolphins (Platanistidae, Lipotidae,Pontoporiidae, and Iniidae) that live in extremely murky wateror moles (Talpidae) that live in total darkness; indeed, in somemoles, the optic nerve has actually degenerated. In mammals’eyes, a lens focuses light on the retina, a layer of light-sensi-tive cells in the back of the eye. Different chemicals (pho-topigments) in the cells of the retina convert opticalinformation to electrical signals that are transmitted via the op-tic nerve to the brain. The retina has two main types of pho-tosensitive cells: rods (that respond to black and white) andcones (that respond to color, which are different wavelengthsof light). Color vision in mammals is uncommon, being pre-sent mainly in primates, some rodents, and some carnivores. Innocturnal mammals such as any microchiropteran bats, rodents(Muridae), and shrews (Soricidae), rods are often prevalent,

while cones may be absent. To these mammals, the world isblack, white, or shades of gray. The eyes of some diurnal mam-mals (for example, primates in the families Lorisidae and Leu-muridae, or rodents in the Sciuridae) have both rods and cones,and these mammals can see color. Other mammals such as somecats (Felidae) have color vision, but only perceive a few colors.

Mammals show a range of overlap between the field ofview of left and right eyes—this is the degree of binocularity.The position of eyes in the face and the size and shape of themuzzle influence the degree of binocularity. Humans, witheyes side-by-side and no muzzle to speak of, have a high de-gree of binocular overlap, which means they have stereoscopicvision. Stereoscopic vision allows mammals (and other ani-mals) to locate objects in space with accuracy. This is the abil-ity to perceive depth, which plays an important role inhand-eye coordination. The distance between the eyes alsoaffects binocularity. For example, African elephants (Loxodontaafricana) or blue whales (Balaenoptera musculus), with eyes sit-uated on the sides of huge faces, have almost no binocularoverlap. In animals such as California leaf-nosed bats (Macro-tus californicus), the degree of binocularity depends upon thedirection in which the bat is looking. There is minimal binoc-ular overlap when the bat looks down its muzzle, and a highdegree of overlap when it looks across the top of its muzzle.

Arboreal animals such as many species of primates(lemurs, galagos, and lorises) tend to have higher degrees ofbinocularity than more terrestrial species (horses, cows, andpigs, in the orders Perrisodactyla and Artiodactyla, respec-tively). Finally, in some cases, the significance of binocular-ity in the animal’s life is not known (for example, in the caseof the wrinkle-faced bat, Centurio senex, of South and Cen-tral America).

It is common for nocturnal mammals to have a tapetumlucidum behind the retina. The tapetum lucidum is a layer ofcells on the back of the eye that reflects light back throughthe retina, amplifying the stimulation of retinal cells by en-suring one round of stimulation as the light goes through, andanother as it is reflected back. Tapeta lucida account for the“eyeshine” when catching a house cat or raccoon (Procyon lo-tor) in a car’s headlights or in the beam of a flashlight. Pin-nipeds (Phocidae, Otariidae, and Odobenidae) and odontocetes(toothed whales and dolphins) also have tapeta lucida for


• • • • •

Sensory systems

helping gather available light at dark ocean depths, resultingin keen underwater vision. Visual displays from the tapetumlucidum are also common to the communication of diurnalmammals, but require that the individuals be close in prox-imity to each other.

Olfaction

Terrestrial mammals often have distinctive scents. In somesocieties, humans go to great lengths (and expense) to maskor alter olfactory information, as is reflected in the sales ofdeodorants and perfumes, respectively. Zookeepers recognizethe importance of smell in mammals because, immediately af-ter they have cleaned a cage, the animal often defecates, uri-nates, or otherwise marks its area again. Individual olfactorysignatures may be less likely in mammals that spend most oftheir lives in water, which would at the least dilute, if not washaway body odors. Water does not allow permanent scent-marking locations, whereas land provides many places to po-sition a long-term scent mark. In fact, whales and dolphinshave completely lost the olfactory-sensing portions of theirbrains.

Mammals use their noses to collect information aboutodors. Specifically, olfactory epithelium (sensors on the mu-cosal surfaces of mesethmoid bones nose) in the nostrils con-

vert chemical signals to electrical ones that are conveyed tothe brain via the olfactory nerves. Many species of mammalsalso use Jacobson’s organs (structures in the roof of themouth) to obtain additional olfactory data through the“Flehman” response (the curling of its upper lip as a malehorse [Equus caballus] or an impala [Aepyceros melampus] smellsthe urine of a female). One advantage of olfaction is that someodors are persistent and may continue to produce signals forlong periods of time, unlike visual displays, which are imme-diate. Distinctive aromas signal the locations of the perma-nent dens of river otters (Lontra canadensis or Lutra lutra) orthe burrows of shrews (Soricidae). Other olfactory materialssuch as mating pheromones in rodents are volatile and per-sist for only a short period of time. Pheromones can be quitepotent, causing the “strange male (or “Bruce”) effect” in somerodents (e.g., house mice, Mus musculus). With this effect, themere presence of another male’s urine can cause a female tomiscarry a litter.

An individual’s olfactory signature is often the product ofthe interaction of odors from different sources. Familiar ex-amples include the aromas of sweat and breath and, in somesituations, body products such as urine, feces, or oil fromglands. An animal’s scent can reveal a great deal about its con-dition and status, while yet more detailed information can beobtained from the aromas of its urine and/or feces. Bull elkduring the rut rub urine on their chests, providing a con-spicuous signal to females and other males of their condition.Male white-tailed deer (Odocoileus virginianus) leave urine andfeces in specific locations in the woods to announce their pres-ence to other deer. Male pronghorn antelopes (Antilocapraamericana) mark the boundaries of territories with piles of fe-ces, as do male white rhinos (Ceratotherium simum), which


Vol. 12: Mammals ISensory systems

Cross Section of Eye

Cellular Organization of Eye

Rod

Cone

Receptor Cells

Optic Nerve

Lens

Light SensitiveRetina

Choroid Membrane

Pigmented Epithelium

Mammalian Vision

The mammalian eye. (Illustration by Michelle Meneghini)

Tongue

Papillae

TasteReceptors

Mammalian Taste receptors

Mammals’ taste receptors, the taste buds, are concentrated on thesurface of the tongue. (Illustration by Michelle Meneghini)

both spray urine and kick feces at specific locations (middens)in their territories.

Many species of mammals also have glandular organs thatcontribute to their olfactory signatures. These organs typi-cally include sebaceous and/or sudoriferous glands that syn-thesize odoriferous molecules. Behavior that transfers theglandular product(s) to other surfaces, sometimes to other an-imals, is called “scent marking.” An example is the chinningbehavior of male rabbits, which serves to place the productsof exocrine glands located on the chin on the surfaces beingmarked. Scent glandular organs often are visually conspicu-ous, enhancing their role in advertisement. The behavior ofmammals rubbing scent glands on surfaces makes the glandseven more conspicuous, as in male white-tailed deer markingtwigs with scent from their tear ducts during rut. In somemammals, scent glandular organs are associated with special-ized hairs called osmotrechia, which are typically quite dif-ferent from body hairs, being larger in diameter, sometimeslonger, and often with a different scale structure; osmetrichiahold and transfer odoriferous molecules.

Although the wing sacs of some sheath-tailed bats (familyEmballonuridae) have been referred to as glands, closer ex-

amination reveals that they lack glandular tissue. Rather, thewing sacs are fermentation chambers to which the bats (adultmales) add various ingredients to enhance their personalscent. Greater sac-winged bats (Saccopteryx bilineata) put saliva,urine, and products of glands located near the anus into themix in the sac, where fermentation produces the distinctiveodors. Using their wing sacs, males can mark objects rangingfrom females in their group to their roosting sites.

AcousticsThe importance of sounds (acoustics) to mammals should

be obvious. As in vision, binaural cues are timing differencesbetween the arrival of sounds at one ear before the other, andthey assist in the localization of sources of sounds. Humansuse acoustical information to recognize the voices of familyand friends or to locate an accident from the wail of an emer-gency vehicle’s siren. In odontocetes, the ability to use bin-aural hearing is improved by an evolutionary shifting of thebones of the skull so that the hearing anatomy of the skull isasymmetrical. This makes odontocetes particularly sensitiveto the direction of an incoming sound.


Sensory systemsVol. 12: Mammals I

Receptor

Dendrite

Nerve Axon

Mammalian Sense of Smell

The sense of smell displayed by many mammals owes much to the in-ternal structure of the nasal passages. These are most highly devel-oped in predators such as dogs. (Illustration by Michelle Meneghini)

The western tarsier (Tarsius bancanus) has a heightened sense ofhearing to help it avoid danger and capture prey. (Photo by Fletcher &Baylis/Photo Researchers, Inc. Reproduced by permission.)

The auditory system of most mammals consists of the fol-lowing five main components:

• the pinnae, an external structure that acts as a soundcollector

• the ear drum, or tympanum, that converts vibrationsin air (sounds) to mechanical vibrations

• an amplifying system, the auditory ossicles (malleus,incus, and stapes) or bones of the middle ear

• a transducer (the oval window), where mechanicalvibrations are converted to vibrations in fluid in theinner ear

• sites for converting vibrations in fluid to electricalstimuli (hair cells attached to the basilar membranein the cochlea)

Through these components, electronic representations ofthe sounds are generated and transmitted to the brain via theauditory nerve.

Fossorial mammals, those that live most of their lives un-derground, may lack pinnae (which would only collect dirt).Many, but not all, aquatic mammals also lack pinnae (whichwould collect water). In fact, as a mammal progresses from am-phibious (otters, seals, walrus, and sea lions) to totally aquatic(whales and dolphins), the pinnae go from small and valvularto absent. In fossorial mammals, considerable fusion of the au-ditory ossciles has reduced sensitivity to high-frequency soundsand emphasized the importance of low-frequency ones. Inodontocetes, the lower jaw probably serves to conduct soundsto the middle ear and into the rest of the auditory system. Be-cause water is a denser medium than air, it transmits soundmore effectively (sound velocity in water is 4.5 times faster thanin air), meaning that the auditory systems of odontocetes, even

without pinnae, are no less sensitive than those of humans. Infact, the effective communication distance for all marine mam-mals is much greater than for any terrestrial animal because ofthe density of water. In contrast, the effective communicationdistance for fossorial mammals would be very small, being lim-ited by the reflective tunnel/burrow environment.

Sounds used by mammals can be of very different pitch orfrequency, depending upon the species and situation. Africanelephants are sensitive to sounds at frequencies below 40 Hz;blue whales produce sounds as low as 20 Hz. These are re-ferred to as “infrasounds,” because they are below the rangeof human hearing (arbitrarily, 40 Hz). Other mammals, no-tably many bats, most carnivores (Felidae, Canidae, Mustel-idae, Viverridae), and dolphins (Delphinidae), use sounds thatare well above the range of human hearing (these are ultra-sounds, theoretically >20,000 Hz). Humans hear best at fre-quencies from about 100–5,000 Hz, while some bats anddolphins hear very well at more than 200,000 Hz. In general,low-frequency sounds carry much farther (propogate) thanhigh-frequency ones, and sounds greater than 20,000 Hz arerapidly eroded by the atmosphere (attenuated).

Touch

Mammals use their sense of touch in different ways. Tac-tile interactions are important for intraspecific communica-tion, well known to a human who has benefited from thecomfort of a hug. Often, touch plays an important role in fe-male mammals recognizing their infants. Seal pups often re-unite with their mothers by exchanges of vocalizations that



The American bison (Bison bison) uses its vomero-nasal gland locatedon the anterior palate in the roof of its mouth to sense females in es-trus. (Photo by © Layne Kennedy/Corbis. Reproduced by permission.)

The giraffes’ 18-foot (5.5-meter) height and excellent vision make iteasy for them to spot predators from a distance. (Photo by David M.Maylen, III. Reproduced by permission.)

terminate in nuzzling. Grooming often involves touching,such as in two chimpanzees (Pan troglodytes) carefully strokingand picking at each other’s fur. Primates have an especiallywell-developed sense of touch, having friction ridges (fingerprints) on the tips of their digits used for careful investiga-tion of objects. Although dolphins do not have limbs forgrasping, their sleek, hairless skin is especially sensitive totouch at various locations on the body, specifically, the gapeof the mouth, the gum, and tongue, and the insertion pointof the flipper. Dolphins commonly swim close to each other,touching and rubbing their bodies together. The spectacu-lar nasal appendages of the star-nosed mole (Talpidae) areextremely sensitive to touch and are used to locate and iden-tify prey.

Vibration

Aye-ayes (Daubentonia madagascarensis) are among themammals most obviously specialized to use vibrations. TheseMadagascar natives have long, slender third fingers. A forag-ing aye-aye taps branches with its elongated fingers and lis-tens for reverberations that it uses to find hollows. Thevibrations, combined with the noises made by insects movingthrough tunnels in wood or chewing to excavate tunnels, helpaye-ayes find their prey.

Vibrations can also serve in communication. Vibrationstend to be low frequency, readily sensed by specialized hairs(whiskers) or other body parts. Nearly furless naked mole-rats(Heterocephalus glaber) live in a burrow system and announcetheir presence to nearby conspecifics in other burrows by tap-ping their heads against the roofs of tunnels. Elephants arethought to use vibrations to sense danger or intruders overlong distances. Recent studies of captive elephants showedthat male elephants in mating condition (musth) moved theirforeheads in and out, movements coinciding with the pro-duction of low-frequency sounds. Although African elephantscan detect acoustic signals of about 115 Hz at distances of 1.5mi (2.5 km), they need to be closer (0.6–0.9 mi [1–1.5 km])to extract individual-specific information about the sig-naler(s). Researchers also believe that elephants sense very-low-frequency vibrations with their large, flat feet, enablingthem to detect the movements and signals of other elephantsfrom great distances. Foot drumming is a common way togenerate vibrations that are used in communication by mam-mals such as lagomorphs (rabbits and hares) as well as kan-garoo rats and subterranean mammals.

Infrared

Around their nose leaves, vampire bats (Desmodus rotundus)have sensors sensitive to infrared energy. The bat’s sensors



The timber wolf (Canis lupus) uses its keen sense of smell to track its prey. (Photo by Wolfgang Baye. Bruce Coleman, Inc. Reproduced by per-mission.)

lack a lens, so they provide poor spatial resolution of infraredsources. Vampire bats probably use infrared cues to locateplaces on a mammal or bird’s body where blood flows closeto the skin, ideal places to bite and obtain a blood meal.Among mammals, some felids have vision that extends intothe infrared spectrum. Elsewhere among vertebrates, some pitvipers (rattlesnakes) use infrared sensors on the roofs of theirmouths to locate and track warm-blooded prey in cool desertnights.

Chemoreception (taste)

Mammals detect a wide range of flavors as odors and tastes.Bottlenosed dolphins (Tursiops truncatus) readily detected dif-ferent concentrations of bitter, sweet, and sour liquids pre-sented to them. Unlike some terrestrial mammals, bottlenoseddolphins are not sensitive to subtle changes in salinity, sug-gesting that an animal living in salt water would not be averseto the taste of salt in its mouth.

Geomagnetic

The ability to orient to geomagnetic fields has beendemonstrated in several species of migrating birds and in somerodents. In mammals, the geomagnetic sensing ability is cor-related with the presence of magnetite in the brain. Someclassic studies on trained rodents showed that the animals,when spun around 360°, could choose a particular orienta-

tion. Since the time of Aristotle, people have recognized thatsome odontocetes (toothed whales and dolphins) strand orbeach themselves, often in large groups. Stranded animalsmay be completely out of the water and face certain death.Some locations where cetaceans often strand themselves arein areas with abnormal or unpredictable geomagnetic fields.

Role of sensory dataMammals sense or gather information about their envi-

ronment and use it to make decisions that affect their survivaland reproduction. Sometimes, species initially respond to onetype of cue. For example, female hammer-headed bats (Hypsig-nathus monstrosus) in Africa locate groups of males by listeningto their distinctive calls. Picking a male to mate with, how-ever, is a decision females appear to make only after visitingseveral in the line of displaying suitors. A female’s actual choicemay involve more than just her response to the males’ calls.

Mammals typically use clues collected from several modal-ities. For example, vervet monkeys must cope with differentpredators. Social animals, vervets have keen vision and ex-tensive vocal repertoires that include several types of warn-ing calls, which indicate the presence of a predator. Usingdifferent warning calls, vervets can alert group members tospecific threats. One alarm call is given in response to snakes,another to mammals such as leopards (Panthera pardus), andyet another to raptors such as eagles. These predators posedifferent kinds of threats. Vervets typically see the predators,but use sound to alert their group mates to the danger. Be-cause each type of predator requires different defensive be-havior, the vervets have specific acoustic signals to increasethe precision of their communication.

The ability of recognizing other individuals in mammalsbegins at birth. Female mammals are expert at recognizing



Spectral bat (Vampyrum spectrum) locating prey. (Photo by AnimalsAnimals ©Stephen Dalton. Reproduced by permission.)

their own young. This is a valuable behavior because milk isexpensive to produce and vital to the survival of young. Thelevel of challenge to the mother varies with different mam-mals. Ewes recognize their lambs by smell, and she usuallyfinds her own lamb quite easily. The lamb imprints on itsmother within in a few days of birth. A female Brazilian free-tailed bat (Tadarida brasiliensis) faces a more difficult chal-lenge. She typically leaves her single young in a creche withhundreds or thousands of others. When she returns from for-aging and looks for her young, she initially relies on spatialmemory to locate the general area where her young mightbe, then she uses the calls of her young to pinpoint their lo-cation, and finally ensures that she is feeding the right youngby smelling its scent. When females depend upon odor to rec-ognize their offspring, the distinctive smell could be some-thing produced by the young, something in the milk she hasfed it, or her own distinctive aroma.

In mammals, distinctive odors do more than mediate inter-actions between mothers and young. Young piglets (Sus scrofa)can recognize other piglets by the odor of their urine, whichallows them to distinguish between familiar and strange indi-viduals. In summer, Bechstein’s bats (Myotis bechsteinii) live to-gether in small groups (colonies). Individuals have specific odorsignatures produced by a gland located between their ears. Inother bats, such as big browns (Eptesicus fuscus), lesser-crestedmastiff bats (Chaerephon pumila), or pipistrelles (Pipistrellus pip-istrellus), odors allow bats to identify their home groups orroosts. It is typical for individual aromas to reflect a combina-tion of odor sources, not just the products of a single gland.

Groups of mammals can also have distinctive vocalizations.Greater spear-nosed bats (Phyllostomus hastatus) use group-specific screech calls to locate other group members whenthey are feeding. In big brown bats and little brown bats (My-otis lucifugus), echolocation calls provide cues to group mem-bership. Humpback whales (Megaptera novaeangliae) havedistinctive songs that consist of phrases and arrangement ofphrases in a music-like organization. Songs within a podslowly change, so that last year’s song is slightly different thanthe current year’s song. Furthermore, phrases come and goin the overall repertoire. Songs also play a role in maintain-ing group cohesion. Male humpbacks sing from an invertedposition and project their sounds over large ocean expanses.In the Antarctic, Weddell seals (Leptonychotes weddellii) have alarge vocal repertoire of 34 underwater vocalizations, 10 ofwhich are used only by males.

EcholocationAnimals, including some mammals and birds, use echoes

of sounds they produce to locate objects in their surround-ings. This is echolocation behavior. Microchiropteran batsproduce echolocation signals by vibrating their vocal cords—exactly the same operation humans use in speaking. Echolo-cating mammals hear echoes through their auditory systems,just as humans hear sounds. While echolocating bats collectechoes of their own sounds by their pinnae (external ears),odontocetes appear to collect sounds via their lower jaws.

An echolocating animal uses the differences between thesound it produces and the reflected echoes to collect informa-tion about its surroundings. Echoes arrive sometime after theproduction of the outgoing signal, providing time cues to theecholocator. Echoes can differ in frequency composition fromthe outgoing signal, encoding information about the target’ssurface. Echolocating mammals, including some toothed whalesand many bats, use echolocation to detect targets (food items)in their path, whether fish or insects, as well as objects such astrees or seamounts. They use echolocation to determine threefactors about detected targets: identity; distance; and move-ment, whether toward or away from the echolocator. Some ofthis information is obtained by comparing information from



Spectral bat (Vampyrum spectrum) with a mouse caught at night us-ing echolocation. (Photo by Animals Animals ©Stephen Dalton. Re-produced by permission.)

Beluga whales (Delphinapterus leucas) use echolocation to navigate,locate holes in the ice, and to find their deep dwelling prey. (Photo byEd Degginger. Bruce Coleman, Inc. Reproduced by permission.)

sequences of calls and their echoes. Some microchiropteran batsand toothed whales also use echolocation to obtain fine detailsabout objects. Echolocating dolphins can distinguish betweenechoes from same-sized spheres of aluminum and glass (downto accuracy of 0.001 in [0.0025 cm]), while some echolocatingbats detect insects smaller than midges and can distinguish fly-ing moths from flying beetles.

It is not obvious that other echolocating mammals (somespecies of shrews and tenrecs) collect and use such detailedinformation. Shrews and tenrecs appear to use echolocationwhile exploring, providing another medium for collectinggeneral information about their surroundings rather thanabout specific targets. Most species of pteropodids, plant-vis-iting flying foxes of the Old World, do not echolocate. Fur-thermore, not all bats echolocate. Or, while Egyptian fruitbats (Rousettus aegyptiacus) and perhaps some other species inthis genus (Rousettus) echolocate, they produce echolocationsounds by clicking their tongues. A further complication isthat the role echolocation plays in the lives of some other batsis not known. Then, some phyllostomid, nectar-feeding bats,visit flowers that are specialized to deliver strong echoes ofultrasonic (echolocation) calls and thus guide the bats to thenectar they seek.

While toothed whales living in turbid waters may useecholocation to find prey, it is not clear how often these an-imals use echolocation to find food in clear waters. It is notknown if any of the mysticete (baleen) whales use echoloca-tion because none has been held in captivity to conduct thenecessary perceptual studies.

The echolocation signals of toothed whales, shrews, andtenrecs are short, click-like sounds composed of a range of

frequencies (broadband). The echolocation signals of mi-crochiropteran bats are tonal, because they show structuredchanges in frequency over time. The echolocation signals oftoothed whales and some microchiropteran bats are very in-tense, measured at over 110 decibels; in the toothed whales,it is measured at over 200 decibels. Other microchiropteranbats and shrews and tenrecs produce signals of low-intensity(<60 decibels). Many species of echolocating bats that huntflying insects and other species that take prey from the sur-face of water change the details of their calls according to thesituation. Longer calls, often consisting of a narrow range offrequencies (narrowband) and dominated by lower frequencysounds, are produced when the bats are searching for prey.Once prey has been detected, the bats often produce shorter,broadband signals. Over an attack sequence, the calls get pro-gressively shorter as does the time between them. The endsequence (or terminal feeding buzz) has closely spaced signalsfor precisely timed capture of the prey. Odontocetes can ad-just the frequency and amplitude of their echolocation sig-nals, depending on the amount of environmental noise. Inareas of noise from snapping shrimp, dolphins produce louderand higher frequency signals to avoid the masking sounds ofthe shrimps’ snaps.

To ensure that they can hear faint returning echoes,echolocating mammals typically separate pulse and echo intime. In other words, most echolocating mammals cannottransmit signals and receive echoes at the same time becausestrong outgoing pulses deafen the echolocator to faint re-turning echoes, which means that collecting informationabout close objects requires signals that are short enough tobe over before the echoes return. Differences in the densityof water and air indicate that sound travels much faster in wa-ter, and cetacean echolocation signals are much shorter thanthose commonly used by bats.

Some microchiropteran bats, including species of horse-shoe bats (Rhinolophidae), Old World leaf-nosed bats (Hip-posideridae), and Parnell’s moustached bat (Pteronotusparnellii; Mormoopidae), take a different approach to echolo-cation. They separate pulse and echo in frequency, meaningthat they can transmit signals and receive echoes at the sametime. These bats depend upon Doppler shifts in the frequen-cies of their echolocation sounds to collect information abouttheir surroundings and targets.

Microchiropteran bats that separate pulses and echo intime produce short echolocation calls separated by long pe-riods of silence. Separating pulse and echo in frequency pro-duces much longer signals that are separated by shorterperiods of silence. Some bats produce short signals that arecalled low-duty cycle, while others produce longer signals thatare called high-duty cycle, reflecting the percentage of timethat the signal is on (10% versus >50%, respectively). Anatom-ical evidence from Eocene fossil bats indicates that both high-duty cycle and low-duty cycle approaches to echolocation hadevolved over 50 million years ago.

The distance over which an animal can use echolocationto collect information will depend upon the strength of theoriginal signal and the sensitivity of the echolocator’s audi-tory system. As a signal moves away from the source (an



The naked-mole rat (Heterocephalus glaber) has sensory whiskers onits face and tail. (Photo by Neil Bromhall/Naturepl.com. Reproducedby permission.)

echolocator’s mouth), it loses energy through spreading lossand, for higher frequency signals in air, by attenuation. Thesame rules apply to the echo returning from the target. Fora big brown bat, this means that the effective range for de-tecting a spherical target 0.7 in (19 mm) in diameter is 16.4ft (5 m). This assumes that the initial signal was 110 deci-bels and that the bat’s hearing threshold is 0 decibels. For0.7-in (19-mm) diameter spheres located 32.8 ft (10 m) infront of the bat, the original signal would reach the target,but the echo would not have sufficient energy to return tothe bat.

The same general situation applies to echolocating por-poises and dolphins, although the distances are greater be-cause of a combination of original signal strength and thesound-conducting properties of water. A false killer whale(Pseudorca crassidens), for example, can detect a 3-in (76-mm)diameter water-filled, aluminum sphere at 377 ft (115 m), arange that is far beyond visual detection. Similarly, an echolo-cating big brown bat would detect a 0.7-in (19-mm) long in-sect at 16.4 ft (5 m), but see it only at 3.2 ft (1 m). However,because of spreading loss and atmospheric attenuation overlonger distances, the same bat would detect a tree-sized ob-ject at 49.2 ft (15 m), but would have been able to see it atover 328 ft (100 m).

Echolocation is an orientation system that allows animalsto detect objects in front of them, and some species also useit to detect, track, and assess prey. The short operationalrange of echolocation in terrestrial mammals means that it isof much less value in navigation. But short operational rangeused in combination with local knowledge can be effective ina longer-range orientation. Greater spear-nosed bats de-prived of vision and taken 31 mi (50 km) from their homecaves could find their way back. Odontocetes use echoloca-tion for navigation in murky, deep, dark waters and a variedunderwater topography. Beluga whales (Delphinapterus leucas)use echolocation to survey the irregular undersurfaces of theirice-covered habitats.

Information leakage is an important disadvantage toecholocation. The signals one animal uses in echolocation areavailable to any other animals capable of hearing them. Manyspecies of insects (e.g., some moths, beetles, mantids, crick-ets, and lacewings) have ears that allow them to detect theecholocation calls of bats. Moths with bat-detecting ears evadecapture in 60% of attacks by echolocating bats, while deafmoths are most often caught. Some herring-like fish changetheir behavior when they hear the echolocation clicks of dol-phins. Weddell seals dramatically reduce their underwater vo-calization rate from 75 calls per minute to no calls when theyhear sounds from their predators, killer whales (Orcinus orca)and leopard seals (Hydrurga leptonyx).

The most obvious eavesdroppers on echolocation calls aremembers of the same species. Bats often use the echolocationcalls of other bats to detect patches of prey or vulnerable prey.Echolocation calls also can serve as communication signalspromoting cohesion in groups of flying bats.

Echolocating animals also have repertoires of social calls.While echolocation signals can serve a communication func-

tion, many social calls are too long to be useful in echoloca-tion. A long signal masks echoes that return as the call is be-ing produced.

NavigationSome species of mammals make long-distance migrations,

typically repeated annual movements between summer andwinter ranges. Gray whales (Eschrichtiidae), bowhead whales(Balaena mysticetus), right whales (Eubalaena species), andhumpback whales make predictable, long-range migrationsbetween summer feeding areas and winter breeding areas.Manatees (Trichechus manatus) make shorter seasonal migra-tions up and down the east coast of Florida. Other migratingmammals include some species of bats, caribou (Rangifertarandus), and antelopes that regularly move between summerand winter ranges.

The navigational cues used by migrating mammals appearto vary. Over shorter distances, perhaps first traveled withtheir mothers or group members, young may learn the land-marks that guide them from one place to another. This ap-pears to be true of manatees off the east coast of Florida. Overlonger distances, geomagnetic cues may be more important.However, compared to the situation in migrating birds, rela-tively little is known about the mechanisms of navigation inmammals.



Bottlenosed dolphins (Tursiops truncatus) use echolocation for hunt-ing and communication. (Photo by Jeff Rotman/Photo Researchers,Inc. Reproduced by permission.)



ResourcesBooksAttenborough, D. The Life of Mammals. London: BBC, 2002.

Au, W. W. L. The Sonar of Dolphins. New York: Springer-Verlag, 1993.

Fenton, M. B. Bats: Revised Edition. New York: Facts On FileInc., 2001.

Fay, R. R., and A. N. Popper (editors). Comparative Hearing:Mammals. New York: Springer-Verlag, 1994.

Griffin, D. R. Listening in the Dark. The Acoustic Orientation ofBats and Men. Ithaca, NY: Cornell University Press, 1986.

Nowak, R. M. Walker’s Mammals of the World, Volume 1.Baltimore: Johns Hopkins University Press, 1999.

Popper, A. N., and R. R. Fay (editors). Hearing by Bats. NewYork: Springer-Verlag, 1995.

Sebeok, T. A. How Animals Communicate. Bloomington, IN:Indiana University Press, 1977.

Smith, W. J. The Behavior of Communicating. Cambridge, MA:Harvard University Press, 1977.

Thomas, J. A., and R. A. Kastelein. Sensory Abilities of Cetaceans:Laboratory and Field Evidence. New York: Plenum Press,1990.

Thomas, J. A., C. A. Moss, and M. A. Vater (editors).Echolocation in Bats and Dolphins. Chicago: University ofChicago Press, 2003.

Vaughan, T. A., J. M. Ryan, and N. J. Czaplewski.Mammalogy, Fourth Edition. Forth Worth, TX: SaundersCollege Publishing, 2000.

Walther, F. R. Communication and Expression in HoofedMammals. Bloomington, IN: Indiana University Press, 1984.

PeriodicalsDeutsch, C. J., J. P. Reid, R. K. Bonde, D. E. Easton, H. I.

Kochman, and T. J. O’Shea. “Seasonal Movements,Migratory Behavior, and Site Fidelity of West IndianManatees along the Atlantic Coast of the United States.”Wildlife Monographs, 151 (2003): 1–77.

Erickson, C. J. “Percussive Foraging in the Aye-aye,Daubentonia madagascariensis.” Animal Behaviour, 41 (1991):793–801.

Scully, W. M. R., M. B. Fenton, and A. S. M. Saleuddin. “AHistological Examination of Holding Sacs and ScentGlandular Organs of Some Bats (Emballonuridae,Hipposideridae, Phyllostomidae, Vespertilionidae andMolossidae).” Canadian Journal of Zoology, 78 (2000):613–623.

Voight, C. C. “Individual Variation in Perfume Blending inMale Greater Sac-winged Bats.” Animal Behaviour, 63(2002): 907–913.

Jeanette Thomas, PhDM. B. Fenton, PhD

Suckling as a defining featurePatterns of reproduction are truly fundamental to mam-

mal biology. This is at once apparent from the word mam-mal itself. In all species of the class Mammalia (monotremes,marsupials, and placentals), females suckle their offspring, andalmost all of them have teats (mammae) to deliver the prod-ucts gathered from the milk-generating glands. As definingfeatures of the class Mammalia, mammary glands and milkproduction (lactation) are clearly central to mammalian evo-lution. Indeed, these features undoubtedly appeared at an ear-lier stage than the birth of live offspring (vivipary). Whereasmarsupials and placentals give birth to live offspring after aperiod of development within the mother’s body, monotremes(platypuses and echidnas) still lay large, yolk-rich eggs. Al-though the milk-generating glands of monotremes releasetheir products through milk patches in the pouch rather thanthrough a small number of teats, suckling of the offspring isclearly evident. Hence, suckling occurs in all extant mammals,and most species show a characteristic duration of this be-havior (lactation period) as one of their reproductive hall-marks. Unfortunately for biologists concerned with thereconstruction of mammalian evolution, reproductive featuresare very rarely preserved in fossils. For this reason, the ori-gin of mammals is defined for practical purposes by the emer-gence of a new jaw hinge between the dentary and thesquamosal, replacing the original reptilian jaw hinge betweenthe articular and the quadrate. Even in the dentition, how-ever, there are features that reflect the mammalian pattern ofreproduction. One defining dental feature of mammals is thepresence of only two sets of teeth throughout life (diphyo-donty), contrasting with the typical reptilian pattern of con-tinuous, wave-like replacement of teeth (polyphyodonty).Young mammals usually have an initial set of deciduous teethcontaining only incisors, canines, and premolars, which is re-placed by a permanent set of teeth in which molars are alsoadded. It is in itself revealing that the deciduous teeth of youngmammals are referred to as “milk teeth”, although the re-placement of teeth may continue well after the end of the lac-tation period.

An intriguing question that arises is why lactation and suck-ling of offspring are consistently limited to female mammals.In principle, it should be possible for male mammals to pro-duce milk as well and thus contribute directly to the survival

of their offspring. This question is all the more appropriatebecause most male mammals (including the human male) haveteats that serve no apparent function. As a rule, anatomicalstructures that have no function tend to disappear in thecourse of evolution, one striking example being the reductionand eventual loss of eyes in cave-living animals that live in thedark. Yet teats are so widespread among male mammals thatit seems quite likely that male teats were present in the com-mon ancestor of the marsupials and placentals. So why arethey still present in most male mammals today, after some150 million years of evolution? We are still awaiting a satis-factory answer to this enigma. All that can be said is that theinitial structure that eventually gives rise to teats and (in fe-males) to functional mammary glands appears very early infetal development in both sexes, in the form of so-called milklines, one on each side of the ventral surface of the body. Suchearly appearance in development is, in fact, a further indica-tion of the basic importance of lactation and suckling in theevolution of mammals. But we still have no explanation forthe fact that milk lines develop not only in the female fetusbut also in the male.

The development of mammary glands is linked to anotheruniversal feature of mammals, namely the possession of hairand associated sweat glands, both developed in connectionwith the evolution of a relatively constant body temperature(homeothermy). It seems highly likely that mammary glandswere derived from sweat glands through a secondary conver-sion that enabled them to produce a nutrient fluid instead ofsweat.

Reproductive tractTwo key features in the initial development of the mam-

malian reproductive tract are crucial for understanding itsevolution in both males and females. First, the system beginsdevelopment as essentially separate left and right halves thatare virtually mirror images of one another (bilateral symme-try). Second, there is a very close connection between the de-velopment of the reproductive tract and that of the kidneysand allied structures (renal system). According to species,these initial conditions are progressively reduced to varyingextents in the course of development, but they provide im-


• • • • •

Life history and reproduction

portant clues for distinguishing between primitive and ad-vanced features.

The basic features of the female reproductive tract arecommon to all mammals. On each side of the body, there isan ovary that discharges the egg(s) into an oviduct, which leadsto a uterus that is in turn connected with the vagina. Likeother land-living vertebrates, all mammals have internal fer-tilization, which requires insertion of the male’s erectile pe-nis through the external opening (vulva) into the vagina. Onevariable feature of the vaginal region of the female repro-ductive tract in mammals concerns the relationship with theoutlet of the urinary system (urethra) on either side of thebody. In most mammals, the ureter enters the female tract atsome distance from the vulva and there is a combined urinaryand reproductive passage (urogenital sinus). This is the casefor most small mammals, such as numerous marsupials, manyinsectivores, tree shrews, many rodents and carnivores. Per-haps the most spectacular case is the female elephant, whichhas a urogenital sinus that is close to 2 ft (61 cm) in length.In contrast, there is no urogenital sinus and the ureter has aseparate opening adjacent to the vulval orifice in primates (in-cluding humans) and certain other mammals. Because a closeconnection between the urinary and reproductive systems isknown to be primitive, the loss of the urogenital sinus is un-doubtedly a secondary development. It should be noted, in-

cidentally, that in many mammals (e.g. monotremes, marsu-pials, and some placentals) the reproductive, urinary, and di-gestive tracts all open into a common structure known as thecloaca. Indeed, the word monotreme means “one-holed”, re-ferring to the fact that there is a single cloacal opening. Inseveral groups of placental mammals, such as hoofed mam-mals and primates, the cloaca has been completely lost andthere is a wide separation between the anus and the repro-ductive/urinary outlets.

The form of the uterus also shows substantial variationamong mammals. In the widespread primitive condition,there are two separate uterine chambers (bicornuate uterus),reflecting the initial development of two completely separatereproductive tracts in the female. A bicornuate uterus is foundin marsupials and most placentals, although there is variationin the degree of separation between the two uterine cham-bers. In contrast, some placental mammals have the two orig-inal uterine chambers completely fused to form a singlemidline structure (simplex uterus). This relatively unusualcondition is found in simian primates (monkeys, apes, and hu-mans), but not in prosimian primates (lemurs, lorises, and tar-siers), which have retained the primitive bicornuate condition.A single-chambered, simplex uterus is also found in someedentates (armadillos and sloths) and in a few bat species. In-terestingly, several bats show conditions intermediate be-


Vol. 12: Mammals ILife history and reproduction

A sheep (Ovis aries) giving birth. (Photo by Animals Animals ©G. I. Bernard, OSF. Reproduced by permission.)

tween the typical bicornuate uterus and the advanced, single-chambered form, thus providing clues to the evolution of thesimplex uterus. All placental mammals show some degree ofmidline fusion of the right and left female reproductive tractsin that there is a single vaginal passage (with or without a uro-genital sinus). In marsupials, there are separate left and rightvaginal passages and the penis is correspondingly bifid inmales. This difference between marsupials and placentalmammals may have arisen through a chance difference in de-velopment. In marsupials, the ureters pass between the pairedvaginal tracts, thus preventing full midline fusion, whereas inplacentals, the ureters are located lateral to the vagina and donot stand in the way of midline fusion.

In the male reproductive system, sperm are produced inthe testis, stored in the epididymis and transported into thepenis by the vas deferens. As a further consequence of theearly close connection between the urinary and reproductivesystems, the bladder and the vas deferens from each testisopen into a common channel in the penis, which conveys bothurine and seminal fluid to the outside world. An unusual phe-nomenon found in most marsupials and placental mammals(but not in monotremes) is descent of the testes into specialscrotal sacs outside of the main abdominal cavity. Once againreflecting the close developmental connection between theurinary and reproductive systems, the testes initially developclose to the kidneys. In most mammals, they subsequently mi-grate into external scrotal sacs. In addition to monotremes,mammals that show no descent of the testes, or only partialmigration within the abdominal cavity, notably include bur-rowing marsupials, insectivores and rodents, various aquaticmammals (certain marsupials, insectivores, and rodents, along

with seals, sea-cows, hippopotamus, whales, and dolphins) andheavily built pachyderms (elephant and rhinoceros). It haslong been suspected that descent of the testes is in some wayconnected with avoidance of the relatively constant, elevatedcore body temperature that characterizes mammals. However,recent evidence suggests that it is not the actual productionof sperm (spermatogenesis) that requires a lower temperaturebut rather sperm storage. For instance, in some mammalspecies that lack descent of the testis as such, the tail of theepididymis migrates to a position close to the ventral ab-dominal wall. This adaptation, which ensures a lower tem-perature for sperm storage but not for sperm production, isfound, for example, in hyraxes and elephant shrews.

A further special feature of both male and female repro-ductive organs in many mammals is the presence of a bacu-lum. This is commonly present both in the penis of the male(os penis) and in the clitoris of the female (os clitoridis), al-though the baculum is typically significantly larger in themale. Various mammals have secondarily lost the baculum.This is, for example, true of certain higher primates, includ-ing humans. The function of the baculum is still unclear, al-though there is some evidence that the os penis may play arole in stimulating the female during copulation. However,rather like teats in males, no function has been proposed forthe os clitoridis in females.

Reproductive processesThe primary reproductive process in female mammals is

the production of eggs (ova) from follicles in the ovary. In anon-pregnant female mammal, production of eggs is typicallya cyclical process, although there are varying degrees of sea-sonal restriction such that some female mammals do not showrepeated cycles. Seasonality of reproduction in mammals ismainly governed by annual variation in rainfall and vegeta-tion, and hence becomes increasingly common at high lati-tudes. In many mammals, seasonality of reproduction isindirectly triggered by annual variation in day length, but insome mammals, it is a direct response to rainfall or food avail-


Life history and reproductionVol. 12: Mammals I

A deer mouse (Peromyscus maniculatus) nursing its two-day-old young.(Photo by Joe & Carol McDonald. Bruce Coleman, Inc. Reproduced bypermission.)

The African lion (Panthera leo) courtship ritual includes hitting, spit-ting, and roaring. (Photo by Jack Couffer. Bruce Coleman, Inc. Repro-duced by permission.)

ability. The typical ovarian cycle of mammals begins whenone or more follicles ripen to the point where the egg can bereleased (ovulation). Following ovulation, the residue of thefollicle is converted into a corpus luteum (yellow body), whichproduces progesterone that maintains at least the early partof pregnancy. The basic stages of the ovarian cycle are com-mon to all mammals, with a follicular phase preceding ovu-lation and a luteal phase afterwards. However, there is afundamental difference between different mammal groupswith respect to the occurrence of ovulation and changes inthe ovary. In many mammals, ovulation occurs only if mat-ing takes place (induced ovulation), and therefore formationof a corpus luteum also requires mating. Some species showa slightly different condition in which ovulation takes placewithout mating, but mating is necessary for formation of acorpus luteum (induced luteinization). In both cases, matingis required for a corpus luteum to form, such that withoutmating ovarian cycles are confined to follicular phases and arecorrespondingly short. By contrast, in other mammals bothovulation and formation of a corpus luteum occur regardlessof whether mating takes place (spontaneous ovulation). Inthese species, cycles always include combined follicular andluteal phases and are correspondingly long. Induced ovula-tion and induced luteinization are found in mammals thatbreed relatively rapidly, as is the case with most insectivores,tree shrews, many rodents, and numerous carnivores. On the

other hand, spontaneous ovulation is typical of mammalscharacterized by slow breeding, such as hoofed mammals,cetaceans (whales and dolphins), hystricomorph rodents, andprimates.

Following ovulation in marsupials and placentals, the eggtravels down the oviduct, where fertilization will take place ifthe female has been inseminated. The fertilized egg (zygote)begins to divide as it completes its journey down the oviduct.By the time the zygote reaches the uterus, it has transformedinto a hollow ball of cells (blastocyst). In placentals, the blas-tocyst is ready to implant in the wall of the uterus as the firststage in the development of placentation that will nourish thedeveloping embryo/fetus. (By definition, a developing embryobecomes a fetus when recognizable organs are formed.) Inboth marsupials and placentals, development of the em-bryo/fetus within the uterus involves four embryonic mem-branes that play different roles. The chorion is the outermostmembrane and remains intact throughout development rightup to birth. Hence, any nutrients supplied by the mother tothe developing offspring must first of all pass through thechorion. In all placental mammals, the chorion is in intimatecontact with the wall of the uterus in the placenta. A secondembryonic membrane, the amnion, surrounds the developingembryo/fetus throughout pregnancy and its fluid content (am-niotic fluid) provides a protective hydrostatic cushion. The



Galápagos fur seals (Arctocephalus galapagoensis) in their breeding territory in Ecuador. (Photo by Harald Schütz. Reproduced by permission.)

remaining two embryonic membranes, the yolk sac (vitellinesac) and the allantois, play a crucial role in transfer of nutri-ents from the mother and in transfer of waste products in theopposite direction across the placenta, to be disposed of bythe mother. In the enclosed egg of reptiles, which has beenretained by monotremes, the vitelline sac contains a nutrient-rich yolk that is absorbed by blood vessels running over thesurface of the sac, while the allantois stores waste productsdeposited by similar superficial waste products. When a rep-tile or montreme emerges from the egg, the waste-filled al-lantois is shed. In the development of the embryo and fetusfrom the yolk-poor egg in marsupials and placentals, nutri-ents must be provided directly by the mother and waste prod-ucts must be removed in some way. In a fascinating reversalof function, the superficial blood vessels of the yolk sac inmarsupials and placentals absorb maternal nutrients arrivingfrom outside rather than absorbing yolk from inside. In manycases, the superficial blood vessels of the allantois also absorbnutrients coming from the mother as a substitute for the orig-inal function of depositing waste products inside the sac. Inaccordance with the original functional adaptations, in mar-supials and placentals the blood vessels of the yolk sac typi-cally develop their exchange role first (chorio-vitellineplacenta), while blood vessels of the allantois do so secon-darily (chorio-allantoic placenta).

Because monotremes still lay eggs, they are commonly la-beled Prototheria to distinguish them from the Theria (mar-supials and placentals), which all have live births. Althoughthe fertilized egg is retained within the mother’s body for theinitial phase of development in marsupials, the impression isoften given that there is no placentation in marsupials. It is,indeed, true that in all marsupials a shell membrane is pre-sent over the chorion at least for the major part of pregnancy.Widespread use of the name “placental mammal” has unfor-tunately tended to reinforce the false impression that placen-tation is lacking in all marsupials. In fact, some form ofplacentation is developed in certain marsupials and a few ofthem, such as the bandicoot (Perameles), even develop a rela-tively advanced chorio-allantoic form of placentation. For thisreason, many mammalogists prefer the terms metatherian formarsupials and eutherian for placentals, derived from the for-mal names Metatheria and Eutheria. The fact remains, how-

ever, that proper formation of a placenta is characteristic ofall eutherians, whereas it has secondarily been developed onlyin some marsupials, so continued use of the easily under-standable term “placental mammal” is surely acceptable.

In placental mammals, there is considerable variation in theform of the definitive chorio-allantoic placenta, although as ageneral rule each order, or at least suborder, of mammals tendsto have a particular kind of placentation. Following Grosser(1909), a basic classification of types of placentation into threemajor categories, reflecting different degrees of invasiveness,can be made with respect to the relationship between thechorion and the inner wall of the uterus. In the least invasivetype of placentation, the placenta is diffuse and the chorion issimply apposed to the inner epithelial lining of the uterus. Itis labeled epitheliochorial placentation. In the other two kindsof placentation, invasion of the uterine wall occurs to somedegree and the placenta is accordingly relatively localized (dis-coid). When moderate invasion occurs, the uterine wall is bro-ken down in the region of the placenta and the chorion comesinto contact with the walls of maternal blood vessels (en-dothelium). This type of placentation is called endothelio-chorial. In the most invasive form of placentation, the walls of



A mother cheetah (Acinonyx jubatus) play fighting with cubs, inKenya. (Photo by Joe McDonald. Bruce Coleman, Inc. Reproducedby permission.)

Gray squirrel (Sciurus carolinensis) babies in their tree nest. (Photo byE. R. Degginger. Bruce Coleman, Inc. Reproduced by permission.)

the maternal blood vessels are themselves broken down in theregion of the placenta, such that the chorion is directly bathedby maternal blood (haemochorial placentation). Epitheliocho-rial placentation is found in a few insectivores and it is uni-formly characteristic of hoofed mammals, whales and dolphins,hyraxes, and strepsirrhine primates (lemurs and lorises). En-dotheliochorial placentation is found in some insectivores, treeshrews, carnivores, sloths, anteaters, armadillos, elephants, andsea cows. Haemochorial placentation is found in many insec-tivores, rodents, bats, and haplorhine primates (tarsiers, mon-keys, apes, and humans).

The evolutionary history of the three basic types of pla-centation is still subject to debate. It is often stated that theleast invasive, epitheliochorial kind of placentation is the mostprimitive. This seems to be only logical, as the initial devel-opment of placentation must surely involve simple superficialcontact between the chorion and the inner lining of the uterus.Because it is regarded as primitive, the epitheliochorial pla-centa is also often believed to be inefficient, notably with re-spect to development of the brain. By contrast, the highlyinvasive, haemochorial type of placentation is commonlythought to be very advanced and efficient. Human beings havethe largest brain size (relative to body size) found amongmammals and they also have highly invasive haemochorialplacentation, so this is often seen as proof of the advanced na-ture of that very invasive type of placentation. However, manymammals with endotheliochorial or haemochorial placenta-tion have relatively small brains, while dolphins, which havenoninvasive epitheliochorial placentation, come a close sec-ond to humans with respect to relative brain size. In fact, thereis much to be said for the alternative interpretation that an-cestral placental mammals already had a moderately invasivetype of placenta, following a long previous history of devel-opment. According to this view, noninvasive epitheliochorialand highly invasive haemochorial types of placentation rep-

resent divergent specializations away from a moderately in-vasive ancestral condition. It is noteworthy that during preg-nancy, mammals with epitheliochorial placentation show greatproliferation of uterine glands in the wall of the uterus. Theseuterine glands produce a nutrient secretion (so-called uterinemilk) that is absorbed by special structures (chrionic vesicles)on the surface of the chorion. The selective advantages of thedifferent basic types of placentation have yet to be identified.However, it is clear that the degree of invasiveness of the pla-centation has little to do with development of large-bodiedoffspring or of offspring with relatively large brains. Instead,it seems likely that the degree of invasiveness of the placentareflects a trade-off between the advantages of an intimate pla-cental connection between the mother and her developingoffspring and the disadvantages of potential immunologicalconflict between the mother and her embryo/fetus.

The process of spermatogenesis typically takes placethroughout the life span of male mammals, although it maybe subject to periodic interruption in those species with a sea-sonal pattern of breeding. Spermatogenesis occurs as a wave-like process along the seminiferous tubules and completion of



Burchell’s zebras (Equus burchellii) with their albino offspring. (Photoby Fritz Polking. Bruce Coleman, Inc. Reproduced by permission.)

A rat embryo at 17.5 days. (Photo © Science Pictures Limited/Corbis. Reproduced by permission.)

sperm development in any one region takes between severaldays and a number of weeks. After transfer to the epididymis,the sperm are then stored until ejaculation takes place.

Gestation and neonate typeWith only a few exceptions, each mammal species has a

characteristic gestation period that shows remarkably littlevariation. In comparisons between species, gestation periodstend to increase as body size increases. However, effectivecomparisons of gestation periods among mammals must takeinto account a fundamental distinction in the state of theneonate at birth. As a general rule, it is possible to distinguishfairly clearly between mammals that give birth to severalpoorly developed (altricial) offspring and those that give birthto a few (usually just one) well-developed (precocial) off-spring. Altricial offspring are largely hairless at birth and theireyes and ears are sealed with membranes. They are relativelyhelpless at birth and are typically deposited in a nest. By con-trast, precocial offspring, which are usually born with a well-developed coat of hair and with their eyes and ears open, aretypically able to move around quite actively at birth and arerarely kept in a nest. Other things being equal, it is obviousthat the gestation period should be relatively longer for pre-

cocial offspring than for altricial offspring. In principle, itmight be expected there would be a smooth continuum be-tween altricial and precocial offspring. In practice, however,there is a fairly sharp division between them. When the re-lationship between gestation period and body size is exam-ined for altricial and precocial mammals separately, it is foundthat there is a wide gap between them. At any given mater-nal body size, the gestation period for precocial offspring isabout three times as long as that for altricial offspring. Fur-thermore, each main mammal group (order or suborder) isdistinguished by the typical condition of the neonate and therelative length of the gestation period. Most insectivores, treeshrews, carnivores, and many rodents (myomorphs and sci-uromorphs) give birth to altricial offspring after a relativelyshort gestation period, whereas hoofed mammals, hyraxes,elephants, cetaceans, pinnipeds, primates, and hystricomorphrodents give birth to precocial offspring after a relatively longgestation period. This is one of the few reproductive charac-ters for which there is supporting evidence. Pregnant fossilhorses from the Eocene and Miocene have consistently beenfound to have only one fetus, while an Eocene fossil bat hasbeen found with twin fetuses. This shows that the small lit-ter size of horses and bats, at least, have characterized thosegroups for at least 45 million years.



A gemsbok (Oryx gazella) with its nursing calf in Etosha National Park, Namibia. (Photo by Animals Animals ©Ana Laura Gonzalez. Reproducedby permission.)

An inverse relationship between the average number of off-spring produced at birth (litter size) and the gestation periodis only to be expected. For a given uterus volume, there isclearly a trade-off between the number of developing off-spring and the extent to which they can develop prior to birth.One corollary of this is that, for any given adult body size, al-tricial offspring must grow more after birth than precocialoffspring.

Postnatal developmentAcross mammal species generally, there is a fairly consis-

tent relationship between the average litter size and the typ-ical number of teats possessed by the mother. As a rule, it canbe said that there is one pair of teats for each offspring in thetypical litter. However, suckling of the offspring is just oneaspect of parental care in mammals. Maternal care, which caninclude nest building, grooming of the offspring, and infantcarriage, is found in all mammals. Paternal care is relativelyrare and is usually restricted to grooming and/or carriage.Predictably, paternal care in mammals is usually restricted tomonogamous species in which there is a relatively high levelof certainty of paternity.

Once the effects of body size have been taken into account,it emerges that the pattern of maternal care for any mammal

species is quite closely reflected in milk composition. Threeprincipal components of mammalian milk are carbohydrates,fats, and proteins. As a crude approximation, it can be saidthat the carbohydrate content of milk reflects immediate en-ergy needs of the offspring, while the fat content indicates en-ergy needs over a longer term. The protein content of milkprovides a fairly good indication of requirements for growth.Milk composition also provides an indication of maternal be-havior. Here, a major distinction can be drawn between moth-ers that feed on schedule and those that feed on demand. Foroffspring that are fed on schedule, it is the mother that de-termines the suckling frequency. Commonly, this applies tooffspring that are left in a nest. These tend to be fast grow-ing but relatively inactive altricial offspring that must main-tain their body temperature unaided in the absence of themother. As a result, the milk of such species tends to be highin protein and fat but relatively low in sugar. The most ex-treme example of suckling on schedule known for mammalsis found in certain tree shrews species that keep their offspringin a separate nest and suckle them only once every 48 hours.The milk of these tree shrews is extremely concentrated, con-taining more than 20% fat and 10% protein. By contrast, inmammals that feed on demand, it is the offspring (usually asingleton) that determines suckling frequency. Usually, thisrequires close proximity between the offspring and its mother,so that it can signal its intention to suckle. Suckling on de-



Opossum babies in their mother’s pouch. (Photo by © Mary Ann McDonald/Corbis. Reproduced by permission.)

mand is, for example, generally typical of primates, most ofwhich show parental carriage of the infant. Because infantsthat suckle on demand are usually slow growing but quite ac-tive precocial singeletons, the milk tends to be low in proteinand fat but relatively high in sugar. This is the case with hu-man milk, which is evidently naturally adapted for sucklingon demand.

Eventually, provision of milk by the mother comes to anend and the offspring are weaned. In altricial mammal species,there is usually a fairly constant lactation period, and wean-ing tends to occur within a few weeks after birth. In preco-cial mammals, the lactation period can be quite variable andit may last months or even years. In fact, there is some indi-cation that for certain hoofed mammals and primates there isa feedback relationship between the frequency of suckling andthe mother’s resumption of fertility, driven by the level of ma-ternal nutrition. If food availability is low, the mother pro-duces more dilute milk, which results in an increased sucklingfrequency. A higher frequency of suckling can suppress ma-ternal fertility and also lead to an extension of the lactationperiod.

After weaning, the developing offspring must forage forfood independently in order to meet its nutrient requirementsfor growth and maintenance. Eventually, it will attain sexualmaturity and enter the breeding population. Here, too, altri-cial mammal species tend to have fairly standard ages for theattainment of sexual maturity, whereas precocial mammals canshow more flexibility, according to prevailing environmentalconditions. Despite such variability, the age of sexual matu-rity is an important milestone for comparisons among mam-mal species. It should be noted, incidentally, that sexualmaturity may or may not coincide with the attainment of theadult condition in other respects, for example in body sizeand/or skeletal and dental maturity. In some cases, individu-als may continue to grow for some time after achieving sex-ual maturity. It is noteworthy, however, that mammals (likebirds) differ from reptiles, amphibians, and fish in showing atarget body size. In each species, individuals tend to ceasegrowing at a fairly standard size.

Life historiesAll of the basic parameters that can be identified in the life

cycle of any given mammal species, such as gestation period,litter size, lactation period, time taken to reach sexual matu-rity, and life span (longevity), contribute to its overall life his-tory. Numerous lines of evidence suggest that these individualcomponents of the life history of a species together consti-tute an adaptive complex that has been shaped by natural se-lection. For instance, one fundamental finding is that speciesthat are subject to relatively heavy mortality under naturalconditions tend to breed earlier. Because early breeding typ-ically translates into a higher reproductive turnover, it can beconcluded that heavy mortality promotes rapid breeding. Insuch comparisons between species, it has become common-place to refer to “reproductive strategies.” However, this isan anthropomorphic term and it is perhaps better to use amore neutral term like “life-history pattern.”

In examining life-history patterns across species, it is es-sential to take account of the scaling influence of body size.It is only to be expected that large-bodied species will breedmore slowly than small-bodied species, as it is generally likelythat the time taken to grow to maturity will increase with in-creasing body size. However, it is also possible for mammalsto show divergent life-history patterns even when body sizeis the same. David Western has aptly referred to these twokinds of difference as “first-order strategies” and “second-or-der strategies.” For any given animal population, increase inpopulation size is typically geometric until the populationreaches a particular level (carrying capacity) determined bylimiting factors (e.g. food supply, predation) in its environ-ment. During the geometric phase of population growth, pop-ulation increase depends on the intrinsic rate of increase (r)that is permitted by the reproductive parameters of thespecies. Because it is very difficult and time-consuming to ob-tain field data on the intrinsic rate of increase for natural pop-ulations, especially for large-bodied species, comparisons areoften based on the maximum possible intrinsic rate of increase(rmax) that is permitted by standard reproductive values. Anumber of basic parameters such as age at sexual maturity,gestation period, litter size, interbirth interval, and longevityare used to calculate the rmax value for each species. As ex-pected, for mammals rmax generally declines with increasingbody size. In addition, there are distinctions between groupsin the value found at any given body size. Primates, for ex-ample, generally have markedly lower values of rmax than othermammals. The two parameters that have the greatest influ-ence in the calculation of rmax values are litter size and age atsexual maturity. Hence, the distinction between altricial andprecocial mammals, in which litter size is a crucial feature, isclearly connected to a divergence in life-history patterns.

Various attempts have been made to develop general the-ories to explain the evolution of life-history patterns in mam-mals and other organisms. One basic problem that isencountered is that differences found between species do notfit well with the patterns that are observed within species, Forinstance, within a mammal species a particularly long gesta-tion period is typically associated with a decrease in the du-ration of postnatal growth. In comparisons between species,however, it is found that species with long gestation periodstend to have extended periods of postnatal growth as well. Itis therefore unclear how natural selection can shape life-his-tory patterns. One model that has been suggested is “r- andK-selection.” In this, it is proposed that species living in un-predictable environments with occasional catastrophic mor-tality will be subject to selection to increase rmax (r-selection).By contrast, species that live in predictable environments withmoderate mortality will be subject to selection to increasecompetitiveness at carrying capacity (K-selection). An alter-native model is that of “bet-hedging,” in which it is suggestedthat high mortality among juveniles will favor slow breedingwhereas high mortality among adults will favor rapid breed-ing. In fact, neither of these models fits all of the facts, so aconvincing overall model remains elusive.

One point that deserves special mention is a potential linkbetween life span (longevity) and relative brain size. Variousauthors have reported that mammals with relatively large



brains tend to have particularly long life spans. Although thisproposed link is controversial, especially because of claimsthat it may be based on a secondary correlation, there is cer-tainly enough evidence to indicate that some kind of con-nection exists. Hence, slow-breeding, long-lived mammalsmay also have relatively large brains as part of their overalllife-history patterns.

Mating systemsMammals exhibit a wide variety of mating systems, which

can be basically divided into promiscuous, monogamous,polygynous, and multi-male. In mammals that live in gregar-ious social groups, the mating system is commonly (but notalways) reflected by the composition of those groups, whereasin dispersed mammals patterns of mating must be determinedfrom observations of interactions between separately ranging,“solitary” individuals. In all cases, however, it must be re-membered that social systems and mating systems do not nec-essarily coincide. Even with mammals that are seeminglymonogamous, genetic tests of paternity are quite likely to pro-duce surprises just as they have already done for several birdspecies.

Monogamy, which is the predominant pattern of social or-ganization and widely assumed to be the dominant mating

system among birds, is relatively rare among mammals. It issomewhat more common in carnivores and primates than inother mammals, but even in those groups it is found in onlya minority of species. It seems likely that promiscuous mat-ing was present in ancestral mammals in association with theirlikely nocturnal, dispersed habits, as it is in various relativelyprimitive nocturnal mammals today that lack any obvious so-cial networks (e.g. many marsupials, insectivores, carnivores,and rodents). Another common mating pattern among mam-mals is polygyny, in which a single male has exclusive or al-most exclusive mating access to a number of females.Polygyny is commonly found, for example, in hoofed mam-mals, pinnipeds, and elephants. By contrast, it is relatively rareto find multi-male systems in which several adult males arepresent in a social network or group competing for matingaccess to females, although it is widespread among higher pri-mates. A key issue here is the potential occurrence of com-petition between sperm from different males. In matingsystems in which a single male has clear priority of access toone or more females (monogamous and polygynous systems),the probability of sperm competition is presumably low,whereas in promiscuous and multi-male systems there is likelyto be a high incidence of sperm competition. This expecta-tion has been confirmed by studies of the relative size of thetestes in mammals. Species with promiscuous or multi-malemating systems generally have significantly larger testes, rel-



Fossa (Cryptoprocta ferox) breeding in the canopy at dawn in Madagascar. (Photo by Harald Schütz. Reproduced by permission.)

ative to body size, than species with monogamous or polyg-ynous systems. This indicates that males show increased lev-els of sperm production in cases where sperm competition isrelatively intense.

Sexual dimorphismMale and female mammals obviously differ in various fea-

tures that are directly linked to reproduction, as is the casewith the sex organs of both sexes and the mammary glands offemales (primary sexual characteristics). However, males andfemales can also differ in a variety of features that are not di-rectly associated with reproduction (secondary sexual charac-teristics). Such secondary differences between males andfemales, like the human facial beard, are collectively labeledsexual dimorphism. The simplest form of sexual dimorphismdistinguishing male and female mammals involves overalladult body size. As a general rule in mammals, males tend tobe bigger than females, but there are some cases in which fe-males are bigger than males (reverse sexual dimorphism). Dif-ferences in body size between the sexes are often relativelymild, as is the case in humans, where adult males are about20% heavier than females; but there are also some strikingcontrasts. In the most extreme case of dimorphism in bodysize found among mammals, namely in the elephant seal(Mirounga), adult males are about four times heavier than fe-males (8,000 lb [3,629 kg] compared to 2,000 lb [907 kg]).Sexual dimorphism in mammals can also affect other features,notably involving differences in external appearance (e.g. coatcoloration), the size of the canine teeth and special appendagessuch as the antlers of deer (Cervidae). Overall, there seems tobe a general tendency for the degree of sexual dimorphism insize of the body or its appendages to increase with increasingbody size (Rensch’s Rule), although the validity of this gen-eralization has been questioned. An additional generalizationthat can be made is that sexual dimorphism in body size, ca-nine size, and the size of such appendages as horns is gener-ally lacking from species with a monogamous pattern of socialorganization. However, this does not apply to sexual dimor-phism in coat coloration, as is shown by striking differencesin external appearance between males and females in certainspecies of monogamous gibbons and lemurs.

The baseline expectation for mammals is that males andfemales will be similar in size and other features unless somespecial selective factor intervenes. However, there is no realreason why males and females should be similar in the size ofthe body and its external appearance or appendages. Giventhe major inequality in contribution to reproduction thatcharacterizes all mammals, because gestation and lactation areexclusive to females, the baseline expectation should surely be

that male and female strategies are quite likely to diverge. Weshould be more surprised by the numerous cases in whichmales and females are very similar in size and appearance thanwe are by sexual dimorphism. The standard explanation forsexual dimorphism in mammals is that selection acts on themale to increase the size of the body or its appendages be-cause of competition for mating access to females (sexual se-lection). In elephant seals, for example, the big bull males fightone another to establish mating territories and maintainharems that may contain three dozen females. The large bodysize of males and their large canine teeth are therefore rea-sonably interpreted as features that increase male success incompetition for females. A similar explanation is provided forthe development of large antlers in male deer. Among pri-mates, this interpretation is also applied to various species thatshow conspicuous sexual dimorphism. A prime example is themandrill (Mandrillus sphinx), in which males are more thantwice as heavy as females, vividly colored and equipped withvery prominent canine teeth.

There has been a general tendency to overlook the po-tential part played by selection on females in the evolution ofsexual dimorphism in mammals. In the first place, it is obvi-ous that a single unitary explanation for sexual dimorphism,such as improved competitive ability of males, is inadequatebecause the different kinds of sexual dimorphism (e.g. bodysize, canine size, and coloration) can vary independently to alarge degree. In primates, for example, it is possible to findmarked dimorphism in coat coloration and mild variation incanine size without any matching difference in body size. Fur-thermore, most lemur species lack any kind of sexual dimor-phism despite sometimes fierce competition among males formating access to females. When males and females of a speciesdiffer in body size, it is commonly assumed that selection hasoperated to increase male body size, but it should be re-membered that selection might also act to reduce (or increase)female body size. Because many reproductive features arescaled to body size (e.g. neonate size and age at sexual re-production), one effect of reduction of female body size willbe to decrease nutritional requirements for reproduction andincrease the rate of reproductive turnover. In principle, sex-ual dimorphism between males and females in adult body sizecould be achieved by an increased rate of growth in males, byan extension of the growth period in males, or by some com-bination of these two possibilities. In practice, sexual dimor-phism in mammalian body size is always associated with atleast some delay in the attainment of sexual maturity in malesrelative to females, so there are consequences for reproduc-tive dynamics in every case. Hence, it seems likely that sex-ual dimorphism reflects the effects of diverging selectionpressures operating on both sexes.



ResourcesBooksAustin, Colin R., and Roger V. Short. Reproduction in

Mammals. Book VI: The Evolution of Reproduction. Cambridge:Cambridge University Press, 1976.

Austin, Colin R., and Roger V. Short. Reproduction inMammals. Book I: Germ Cells and Fertilization. Cambridge:Cambridge University Press, 1982.

Bronson, Frank H. Mammalian Reproductive Biology. Chicago:University of Chicago Press, 1989.



ResourcesHayssen, V., and A. Van Tienhoven. Asdell’s Patterns of

Mammalian Reproduction: A Compendium of Species-SpecificData. Ithaca, New York: Comstock Publishing Associates,Cornell University Press, 1993.

Johnson, Martin H., and Barry J. Everitt. Essential Reproduction.Oxford: Blackwell Scientific Publications, 1980.

Martin, Robert D., Lesley A. Willner, and Andrea Dettling.“The evolution of sexual size dimorphism in primates.” InThe Differences between the Sexes, edited by Roger V. Shortand Evan Balaban. Cambridge: Cambridge University Press,1994, pp. 159–200.

Mossman, Harland W. Vertebrate Fetal Membranes. NewBrunswick, New Jersey: Macmillan/Rutgers UniversityPress, 1987.

Perry, John S. The Ovarian Cycle of Mammals. Edinburgh:Oliver & Boyd, 1971.

Stearns, Steven C. The Evolution of Life Histories. Oxford:Oxford University Press, 1992.

Steven, D. H. Comparative Placentation: Essays in Structure andFunction. London: Academic Press, 1975.

PeriodicalsBen Shaul, D. M. “The composition of the milk of wild

animals.” International Zoology Yearbook 4 (1962): 333–342.

Charnov, E. L. “Evolution of life history variation amongfemale mammals.” Proceedings of the National Academy ofSciences of the United States of America–Biological Sciences 88(1991): 1134–1137.

Cowles, R. B. “The evolutionary significance of the scrotum.”Evolution 12 (1958): 417–418.

Daly, M. “Why don’t male mammals lactate?” Journal ofTheoretical Biology 78 (1979): 325–345.

Derrickson, E. M. “Comparative reproductive strategies ofaltricial and precocial eutherian mammals.” FunctionalEcology 6 (1992): 57–65.

Fenchel, T. “Intrinsic rate of natural increase: The relationshipwith body size.” Oecologia 14 (1974): 317–326.

Harvey, Paul H., and Zammuto, R. M. “Patterns of mortalityand age at first reproduction in natural populations ofmammals.” Nature (London) 315 (1985): 319–320.

Kenagy, G. J., and S. C. Trombulak. “Size and function ofmammalian testes in relation to body size.” Journal ofMammalogy 67 (1986): 1–22.

Kleiman, Devra G. “Monogamy in mammals.” QuarterlyReview of Biology 52 (1977): 39–69.

Long, C. A. “Two hypotheses on the origin of lactation.”American Naturalist 106 (1972): 141–144.

Martin, Robert D. “Scaling effects and adaptive strategies inmammalian lactation.” Symposium of of the Zoological Societyof London 51 (1984): 87–117.

Martin, Robert D., and Ann M. MacLarnon. “Gestationperiod, neonatal size and maternal investment in placentalmammals.” Nature (London) 313 (1985): 220–223.

Møller, Anders P. “Ejaculate quality, testes size and spermproduction in mammals.” Functional Ecology 3 (1989): 91–96.

Oftedal, O. T. “Milk composition, milk yield, and energyoutput at peak lactation: a comparative review.” Symposiumof the Zoological Society of London 51 (1989): 33–85.

Pianka, E. R. “On r- and K-selection.” American Naturalist 104(1970): 592–597.

Pond, Caroline M. “The signficance of lactation in theevolution of mammals.” Evolution 31 (1977): 177–199.

Ralls, K. “Mammals in which females are larger than males.”Quarterly Review of Biology 51 (1976): 245–276.

Read, A. F., and Paul H. Harvey. “Life history differencesamong the eutherian radiations.” Journal of Zoology, London219 (1989): 329–353.

Rose, R. W., Claire M. Nevison, and Alan F. Dixson. “Testesweight, body weight and mating systems in marsupials andmonotremes.” Journal of Zoology, London 243 (1997):523–531.

Sacher, George A., and E. Staffeldt. “Relation of gestationtime to brain weight for placental mammals.” AmericanNaturalist 108 (1974): 593–615.

Schaffer, William M. “Optimal reproductive effort influctuating environments.” American Naturalist 108 (1974):783–798.

Western, David. “Size, life history and ecology in mammals.”African Journal of Ecology 17 (1979): 185–204.

Robert D. Martin, PhD

Mammalian reproductionReproduction is pivotal to the continuation of life. From

an evolutionary standpoint, there is no single factor that hasmore impact on the development of species. The impetus toreproduce shapes morphology, physiology, life history, and be-havior of all animals, mammals included. From the egg-layingplatypus (Ornithorhynchus anatinus) to the wildebeests (genusConnochaetes) that have neonates that can run mere seconds af-ter birth, a wide variety of strategies have evolved to success-fully bear offspring in a multitude of environments.

Fundamentals of mammalian reproductionMammals reproduce sexually, and both sexes must unite to

conceive offspring. The physical contact of both sexes does notconstitute reproduction, but instead, it is the union of the sex-ual cells or gametes produced by each sex that constitutes thefirst step to reproduction. In females, the gamete is the egg orovum. In males, the gamete is sperm. Each gamete containsone copy of each of the parental chromosomes, and thus, whenthe gametes unite, they form a zygote, the first complete cellof a new animal. Division of this first cell will result in the de-velopment of a full-grown animal. But before the two gametescan be united, several events must occur, all contributing to thephenomenon of mammalian reproduction. First, animals mustfind and choose mates. This very basic step will allow for a va-riety of adaptations to conquer, convince, attract, or seducemates of the other sex. Second, mammals must get their ga-metes together, and this will be discussed under copulation andfertilization. Third, offspring growth and development toadulthood will be discussed under ontogeny and development.Because several aspects of development will be affected by therole of the two sexes, the importance and implications of mat-ing systems will be discussed as well as strategies of reproduc-tion and associated life history. Finally, some of the peculiarreproductive strategies present in mammals, and their role inthe evolution and development of mammalian reproductiveprocesses will be explored.

Mate choiceFor a mammal to reproduce it must unite its gametes with

the gametes of a member of the other sex. Because each ga-

mete provides half of the genetic material of the offspring,the choice of mate has direct implications on the resultinggenotype (genetic makeup) of the offspring. For this reason,animals do not mate randomly and instead choose mates.Mate choice is among the most important pressures affectingthe evolution of species because failure to be able to select a“good” mate results in poor offspring quality (offspring thatmay be less adept to survive or reproduce), or worse yet, nooffspring. Animals that fail to reproduce disappear from thegene pool, so mate choice is a critical factor.

In mammals, both sexes produce gametes of different size.Females produce relatively large eggs, and, typically, in lim-ited number. In contrast, males produce tiny, cheap (from anenergy standpoint), and extremely abundant sperm. Thus,from the outset, females adopt a “quality” strategy whereasmales adopt a “quantity” strategy. This very basic differencein the size of gametes and parental investment in gamete pro-duction will trickle down and affect almost all subsequent re-productive processes. The larger initial investment of femaleswill also result in females taking care of growing embryo(s).Production of offspring in mammals involves placental growth(monotremes and marsupials are exceptions—see below), andthis is performed by females. Once born, young are nursedwith milk, also produced by the mother. So although the ge-netic contribution of each sex in the offspring is equal, theinvestment of females in offspring is greater. Thus, femaleshave more to lose from bad mating decisions. This asymme-try in investment between sexes will be reflected throughoutmost sexual adaptations, and will lead to females being almostinvariably the most selective in mate choice.

Sexual selection and the evolution of speciesand their attributes

The pressures caused by females choosing males will leadto two types of evolutionary selection: inter-sexual selection(adaptations to win members of the other sex), and intra-sexual selection (adaptations to win access to mates over mem-bers of the same sex). Both vary in importance according tospecies and environments.

Inter-sexual selection leads to the development of adapta-tions, morphological, physiological, or behavioral, to seduce


• • • • •

Reproductive processes

mates. Typically, females are choosers, so most of the inter-sexual selection targets males. Adaptations resulting from in-ter-sexual selection are meant to reveal genetic quality, somales will harbor features, or perform behaviors that indicatequality. Examples of inter-sexual selection are numerous inmammals, and the best known morphological examples areprobably the growth of horns in ungulates such as giraffe (Gi-raffa camelopardalis), or bighorn sheep (Ovis canadensis).

In contrast to inter-sexual selection, which arises frompressures imposed by the other sex, intra-sexual selectionleads to adaptations as a result of pressures imposed by thesame sex. Displays of strength or resources may serve to in-dicate dominance and establish hierarchy among males, al-lowing better individuals to access more mates. Best examplesin the mammals are the sparring competitions of ungulatessuch as deer (genus Odocoileus), or the banging of heads inmusk oxen (Ovibos moschatus). In these examples, some of themorphological attributes such as large antlers may be used forboth inter-sexual selection (seduction of mates), intra-sexualselection (indication of dominance), and even individual se-lection (defense against predators). But multiple functions do

not lessen their attractiveness as large antlers indicate that themales that harbor them are able to find resources to grow andcarry heavy antlers, and thus indicate that they are in goodhealth and have good genes. The extinct Irish elk possessedthe largest antlers ever. They were up to 6 ft (1.8 m) in length.However, the purpose of these was not to fight. It is unlikelythey could be used for this purpose as they were too big. Thesemassive antlers seem to have evolved because of runaway sex-ual selection. Females prefered males with larger and largerantlers, so the antlers got bigger and bigger.

Sperm and egg formationSperm cells are made in the testes of males. Through a

process of cellular division called meiosis, sperm-producingcells with regular genetic material (diploid cells, meaning theyposses two copies of each chromosome) undergo division withthe end product being two cells each with only one copy ofeach chromosome (haploid, half of the parent cell). Becausesperm production is optimal at temperatures slightly colderthan average body temperature, testes are housed in a pouch


Vol. 12: Mammals IReproductive processes

Top: Placental mammal development. Middle row: Marsupial mammal development. Types of uterus: A. Simplex; B. Bipartite; C. Bicornuate; D.Duplex; E. Marsupial. (Illustration by Patricia Ferrer)

A B C D E

2 months 4 months 8 months 11 months

21 days 26 days 4 weeks after birth 12 weeks after birth

vagina

uterus

fallopian tube

cervix

ovary uterinehorn

lateralvagina

birthcanal

uterus

allantoiccavity

amnioticcavity

placenta

amnioticcavity

allantois yolk sac

chorion

of skin just outside the body, the scrotum. But not all specieshave scrotal testes year-round, and some species such as batshave testes that are kept internal for most of the year and be-come external prior to breeding. Other species such as aquaticcetaceans (whales and dolphins) or sirenians (dugong andmanatees), as well as terrestrial armadillos, elephants, andsloths retain internal testes even during reproductive season;interestingly, sperm production readily occurs at normal bodytemperatures in these species.

Once formed, the sperm cells are stored in the epididymiswhere they remain until sperm is ejaculated. Not surprisingly,the mating system of species is often correlated with the sizeof testes, and many species with promiscuous mating systemswill have larger testes simply because copulations are morefrequent and males require more sperm, for example lions.Sperm production in humans is constant throughout repro-ductive life, but in seasonally breeding animals it only occursimmediately prior to the reproduction period as sperm madetoo far in advance degrades with age. Because millions ofsperm are released with each ejaculate, the number of spermproduced by a male during a lifetime is astronomically high.

In females, the process is much different. At birth, femalesalready possess in their ovaries all the eggs they will ever pro-duce. Eggs are stored as follicles, and they will start develop-

ing into fully functional eggs once sexual maturity is reached.As follicles mature, they expand in size on the surface of theovary until ovulation is triggered by release of luteinizing hor-mone. Peaks of this hormone occur either as part of the es-trous cycle or are triggered by physical stimuli in inducedovulators such as cats (Felidae) and rabbits (lagomorphs).

Copulation and fertilizationOnce eggs are released from the female ovaries, they mi-

grate down into the uterus. Eggs are not self-propelled, andmigration occurs passively by gliding over cells that have mi-nuscule sweepers (cilia). In contrast, sperm cells each have along flagellum that provides mobility. But for sperm to reachthe egg or eggs, copulation must first occur.

Copulation in most terrestrial species occurs as the malestraddles the female from behind. Typical examples of thistype of copulation occur in deer, elephants, mice, and cats.Most animals remain in this position, but some, especiallydogs (Canidae), may then turn 180 degrees and continue aprolonged copulation in a copulatory lock, where the penispoints 180 degrees away from the head, and both animalsface in the opposite direction. Another situation occurs inCetaceans (whales and dolphins) where copulation occurs as


Reproductive processesVol. 12: Mammals I

These giraffes illustrate flehmen behavior through which the male assesses the sexual receptivity of the female by sniffing her urine and allow-ing it to run over the Jacobson’s organ in the roof of the mouth. (Photo by Rudi van Aarde. Reproduced by permission.)

both animals lay or swim belly to belly. In primates, includ-ing humans, copulation positions are more flexible but mostoften consist of the ventral-dorsal mount or the ventral-ventral position.

The position assumed during copulation helps transfer thegametes from the male to the female tract, and physical con-straints of size and position necessitate the use of a gamete-transfer organ, the penis. Depending on challenges faced byeach species, characteristics of the penis such as size, length,or structure will vary. But all penes have the same function:to facilitate the transfer of the sperm cells from the male bodyto the female reproductive tract. Unlike fishes, which can re-lease their sperm in water, mammalian sperm loses its mo-bility when exposed to air and internal copulation andfertilization maximizes the chances of successful transfer ofviable sperm.

Both sexes have evolved adaptations to facilitate every stepof reproduction, and copulation is no different. For exam-ple, females that come into heat will often produce thickvaginal secretions that not only attract males, but that alsoserve to lubricate the reproductive tract in preparation forcopulation. Males also produce a lubricant via their bulbo-urethral glands to help facilitate copulation. In some species,including humans, the vaginal tract is highly acidic to serve

as a barrier against diseases or microbial infections that mayoccur in or on the reproductive organs of males. To neu-tralize the acidity of the female tract that could damage oraffect the motility of sperm cells, males have a prostate glandthat secretes an alkali buffer to bring the pH of the femaletract closer to neutral (pH = 7) so that sperm mobility andsurvival is optimized.

Once sperm cells reach the egg, a single sperm cell fuseswith the egg cell. An enzyme then allows penetration of thegenetic material of the sperm into the egg cell. Once thisis done, the membrane of the egg becomes sperm proof toprevent inclusion of additional genetic material that wouldunbalance the process and possibly render the zygote non-viable.

Although this process seems simple, males release millionsof sperm in each ejaculation so obviously not all sperm reacheggs. Sperm mobility may be affected by external conditions(such as acidity in the female tract), but also by their age, andolder sperm become less mobile as they age. Strength andmobility of sperm cells is crucial, especially if females copu-late with numerous males, and in these cases, sperm of mul-tiple males may be present at the same time, forcing males tocompete again for the available eggs, this time via sperm warswithin the female’s reproductive tract.



Two bison (Bison bison) bulls sparring, a common play-fight among young bulls in which there are neither winners nor losers. (Photo by © WallyEberhart/Visuals Unlimited, Inc. Reproduced by permission.)

Sperm competitionGametes evolved to different sizes. Females by definition

are the sex that produces larger gametes. Once they’ve de-posited their smaller gametes, males are in the advantageousposition to limit energetic input (e.g., leave). The females arethen left with the decision to raise offspring or not, and thisdecision has important energetic implications. But males alsohave one evolutionary uncertainty to overcome: the certaintyof paternity. If males release millions of sperm and can fathermultiple litters within a single reproductive season (by breed-ing with several females), the certainty of paternity is seldomassured, and the uncertainty of paternity may well be thegreatest challenge that mammalian males face when it comesto reproduction. Not surprisingly, a myriad of adaptations hasevolved to overcome this uncertainty—from mate guardingand mate defense to strategies inside the reproductive tractsuch as sperm competition. Also, if there are fights to preventother males from mating, these males will fight to overcomebarriers put in place by previous males. One could argue thatwhen males fight, females ultimately win because whichevermale succeeds probably has better genes or the kind of genes

that will enable her male progeny (i.e., son) to produce morechildren (i.e., increased fitness).

Mate guarding and defense following mating is a simpleway for a male to reduce the odds of another male copulat-ing with a female. However, the trade-off is obvious: stayingwith one mate precludes males from courting others, andstrategies that allow males to protect their paternity withoutbeing present would yield great advantages. Sperm competi-tion is one such process that can be simply summarized as anyevent that leads to sperm of two or more males being presentat once inside the reproductive tract of a female. Males thatrelease seminal fluids with greatest number of sperm, andsperm with the greatest mobility are thus more likely to fer-tilize female eggs.

Other strategies also exist for males to ensure paternity. Insome species of primates such as the Senegal bush baby (Galagosenegalensis) or ring-tailed lemur (Lemur catta), males have apenis that is highly spinuous, and the function of these spinesis to alter the reproductive tract of the mated female so thatshe become less receptive to subsequent mating from othermales. In carnivores such as wolverines (Gulo gulo) or Ameri-can mink (Mustela vison), the penis bone may also play a rolein causing enough stimulation for females to abort the first setof fertilized eggs, thus allowing males with larger penis bonesto father more offspring. This also would allow females tocompare male quality via the size of males’ penis bones insidethe reproductive tract instead of by classic displays.

In many species of rodents such as brown rats (Rattusnorvegicus), primates, or bats, some of the seminal fluids willform a copulatory plug. This plug is formed soon after cop-ulation and it appears that its main function is to prevent leak-age of sperm from the female reproductive tract following



After the koala (Phascolarctos cinereus) leaves its mother’s pouch atseven months, it stays on her back for another four months. (Photoby Tom McHugh/Photo Researchers, Inc. Reproduced by permission.)

A Dall’s sheep ram (Ovis dalli) in the November rut season in a urine-testing pose, testing the female’s urine for signs of estrus. (Photo by© Hugh Rose/Visuals Unlimited, Inc. Reproduced by permission.)

copulation. The longer the sperm stays inside the female, thebetter the odds of fertilization by maximizing the amount ofsperm and hence number of sperm cells active in the femaletract. Interestingly, the tip of the penis (the glans) is used bymales to remove sperm plugs deposited by other males.

Ontogeny and developmentMammalian ontogeny and development can, from a phys-

iological standpoint, be separated into three general strate-gies. First, the monotremes such as platypus and echidnas areoviparous, meaning that they conceive young via copulation,but give birth to young inside an eggshell. After a short pe-riod of development in the egg, young hatch and then sucklethe mother’s milk as it leaks into the fur and not through anipple as monotremes do not have nipples.

In contrast, marsupials and placental mammals are vivip-arous, meaning they give birth to live young. But their re-spective strategies differ, especially with regards to level ofdevelopment of the young at birth. Marsupials give birth tolive young, but they have a short gestation and produce youngthat are extremely altricial, i.e., very early in their develop-ment stage. Marsupial offspring are born blind and naked,and with underdeveloped organs except for a pair of ex-tremely well-developed and strong front limbs. The youngare also minuscule in size compared to adults. They spendmost of their growth phase outside of the female reproduc-tive tract but securely attached to the maternal nipple fornourishment, often, but not always, in a pouch. Kangaroosfor example give birth to tiny young which then crawl to thepouch (with the strong front limbs) and find a nipple. At-tachment to the nipple ensures that the blind and naked

young does not fall off the mother and always remains closeto its source of nourishment.

Placental mammals constitute the largest group of mam-mals. In these species, which includes, cats, dogs, horses, bats,rats and humans, fertilized ova migrate to the uterus wherethey implant and fuse with the lining of the uterus called en-dometrium, which then leads to the creation of a placenta, ahighly vascular membrane that acts as the exchange barrierbetween embryo(s) and mother. Young develop inside the fe-male tract to varying degrees, but even the most altricial ofplacental mammals (polar bears Ursus maritimus, for exam-ple) still are more developed at birth than marsupials. Inter-nal development can be extremely advanced and lead to birthof young that are able to stand and run almost immediatelyafter birth. Wildebeests, elephants and guinea pigs all haveprecocial young (offspring born fully developed) in this cat-egory.

Milk and lactationAt birth, the young no longer can rely on the direct ex-

change of nutrients through the placenta (or in monotremes,through nutrient stored in the egg). Thus, nutrition of youngrequires an additional process, and milk is the nutrient thatserves that purpose. Milk is unique to mammals, and allspecies of mammals are capable of producing milk. Milk pro-duction occurs in the mammary glands, which resemble sweatglands in form but become mature only following parturitionor birth of young. The milk is delivered through nipples orteats (except in monotremes), and typically the number ofteats is roughly twice the average litter size. Although maleshave fewer and smaller teats that are vestigial, only femalesproduce milk and consequently they have larger teats. All ruleshave their exception and in mammals, there is one species inwhich males can also produce milk and nurse young, the Dyakfruit bat (Dyacopterus spadiceus).



Florida manatee mother nursing her calf in Crystal River, Florida, USA.Photo by Animals Animals ©Franklin J. Viola. Reproduced by per-mission.)

A female cape fur seal (Arctocephalus pusillus pusillus) reacting to a male. (Photo by David Dennis/Nature Portfolio. Reproduced by permission.)

Sexual maturitySexual maturity in many species occurs when body size

reaches adult size. However, there are some notable excep-tions: male least weasels (Mustela nivalis) often seek maternitydens of females and will copulate the newly born females, assoon as 4 hours after birth. At that time, neonates still havetheir eyes and ears closed, are pink and hairless. This strat-egy enables females to have a first litter within weeks of birth(least weasels do not exhibit delayed implantation), and thenagain before the end of their first year. Another example ofearly sexual maturity is in musk shrews (Suncus murinus) inwhich mating and repeated ejaculations from males inducepuberty and ovulation in virgin females.

Mating systemsDepending on the environment, mammals will adopt var-

ious mating strategies. In some species such as beaver (genusCastor), the maintenance of a pond, lodge, and dam to main-tain water level and insure security of the offspring requiresthe efforts of both parents, and thus both sexes must combineefforts to raise young to adulthood successfully. In suchspecies, the sexes not only combine gametes, but also effortsand they remain together throughout the mating season, orfor life. The term monogamy describes such systems, whereanimals remain with one mate either annually or permanently.Only 3% of mammals are monogamous but monogamy isfound within nearly all mammalian orders and predominatesin some families, for example in foxes, wild dogs and gibbons.Some examples of seasonal monogamy would be in red foxes

(Vulpes vulpes), in which males provide parental care, butwhere couples break-up after rearing of young. Permanentmonogamy would be best exemplified in North Americanbeavers that mate for life (Castor canadensis). Generally speak-ing, monogamy occurs in species where the support from themales is instrumental to the rearing of young, and males gainmore from limiting the number of offspring (by staying withone female) and investing instead in the growth of their off-spring. However, many so-called monogamous males will op-portunistically attempt breeding with other females, paired ornot, to increase their genetic fitness, and true monogamy oc-curs rarely when lack of potential mates occurs, or under pres-sures from the environment.

Polygynous mating systems occur when males do not pro-vide paternal care, and hence pursue matings with numerousfemales. Such are probably best exemplified in ungulates andpinnipeds, where males maintain access to several females si-multaneously. In these harems, males try to control femalebreeding by asserting their dominance over other males, andif successful, winning males sire offspring from several fe-males, whereas females only breed with a single male.

Not all females accept a single male, and in some species,both males and females will mate with numerous individuals.Promiscuity describes such a system, and is probably best ex-emplified in wide-ranging carnivores such as mink or wolver-ines. In these species, females cannot compare mates becausethey are spatially widely scattered, so females may mate withnumerous individuals, and rely on other mechanisms tochoose mates such as sperm competition. Promiscuous fe-males also occur in certain social structures where uncertaintyof paternity in males prevents them from killing the offspringof the female (infanticide). Such a social structure occurs inprides of lions (Panthera leo).

Finally, a mating system exists where male alliances mayform to care for the offspring and allow females to spend mostof their energy producing, and not caring for, offspring. Thissystem, called polyandry, may occur in mammals under ex-tremely biased sex-ratio in adulthood where males are ex-tremely abundant, and females extremely rare, as for examplewith the African wild dog or the naked mole rat, with one“queen” and all else workers. This scenario is much less com-mon but occurs in some human cultures.

Life history strategiesJust like gamete production, offspring production can fol-

low the same two strategies: quantity or quality. The qualitystrategy is best exemplified in African elephants (Loxodontaafricana), the largest living land animal. African elephants pro-duce one young, rarely two, after a gestation of 22 months.Young are born precocial, and can stand up and follow themother within 15–30 minutes. They are nursed for 2–3 years(sometimes up to 9 years), and reach sexual maturity at 8–13years of age. In their lifetime of 55–60 years, female elephantsaverage four calves, with a range of one to nine.

In contrast to the “quality” strategy of elephants, numer-ous rodents and lagomorphs have multiple litters each year,each with numerous young, and spend little time investing in



A short-beaked echidna (Tachyglossus aculeatus) hatching in the pouchof the mother. (Photo by McKelvey/Rismiller. Reproduced by permission.)

offspring growth (quantity strategy). Obviously, a continuumexists between the two extremes and typically these life his-tory strategies are influenced by the size and life span of theanimal and the environment. For example, small rodents growfaster, and live shorter lives, and thus invest in “faster” re-production such as earlier age at maturity, and smaller butmore numerous neonates. In contrast, larger mammals suchas ungulates, elephants, and whales have relatively larger butfewer neonates, and attain sexual maturity much later. Thelatter species are typically longer-lived, and thus spread theirreproductive efforts over a longer time span than smallermammals.

Reproduction in monotremesThree species of mammals differ completely from the more

common placental animals: the short-beaked echidna (Tachy-glossus aculeatus), the long-beaked echidna (Zaglossus bruijni),and the duck-billed platypus (Ornithorhynchus anatinus).Monotremes differ from placental mammals mostly becausedevelopment of the offspring occurs outside of the female re-

productive tract. Monotreme females conceive young via cop-ulation, but fertilized ova then move to a cloaca (a commonopening of urinary and reproductive tract) where they arecoated with albumen and a shell, and eggs are laid after 12–20days. Female echidnas carry the egg into a pouch whereasplatypus lay the eggs into a nest of grass. At hatching, youngechidnas remain in the pouch and subsist on the milk thatdrips from the fur (monotremes lack nipples). Once largeenough, young are deposited in a nest where they are nurseduntil weaning. In contrast, female platypus lay their eggs in agrass nest inside a burrow, incubate them until hatching 10days later, and then nurse the young in the den. Young emergefrom the burrow when fully furred and approximately 12 in(30 cm) in length.

Reproduction in marsupialsIn marsupials, ova are shed by both ovaries into a double-

horned or bicornate uterus. The developing embryos remainin the uterus for 12–28 days, and most of the nourishmentcomes from an energy sac attached to the egg (yolk sac). Thereis no placenta (except for one groups of marsupials, the bandi-coots, that have an interchange surface that resembles a trueplacenta). Gestation is thus short (less than one month), andmuch of the development of the young will occur outside ofthe female reproductive tract.

At birth, the offspring are extremely altricial (poorly de-veloped). In many marsupials such as kangaroos, offspring willmigrate to the nipples where they attach. This will ensure thatthey remain in contact with their nourishment sources, andalso probably serve to secure the young and prevent them fromfalling off the mother at an age when they do not have thestrength to hold on by themselves. In red kangaroo (Macropusrufus), the largest of all marsupials, young climb unaided tothe pouch within a few minutes of birth, remain on the nip-ple for 70 days, protrude from the pouch at 150 days, emergeon occasion at 190 days, and permanently leave the pouch at235 days, but is fully weaned only after a year.

Marsupials have the tiniest young in relation to adult size.In the eastern gray kangaroo (Macropus giganteus), young atbirth weigh less than 0.0001% of the female mass. Put intocontext, this would be similar to a 150 lb (68 kg) human fe-male giving birth to individual babies that would each weigh0.0048 lbs (22 g), or 0.08 oz. But extreme altriciality is not adisadvantage in evolutionary terms. In fact, many scientistsbelieve that this is instead a great advantage as the small in-vestment in each neonate allows females to minimize invest-ment in young and be more flexible and responsive toenvironmental conditions. Mechanistically, if environmentalconditions become too tough to raise young successfully, star-vation would terminate the production of milk and lead torapid death of young, thereby saving energy lost (versus pla-cental mammals that have a greater energy investment). Thiswould give marsupial females a competitive advantage overanimals with internal pregnancy (placental mammals) in un-predictable environments.

Some marsupials such as the eastern gray kangaroo alsodisplay other reproductive oddities. Pregnancy following cop-



An African elephant (Loxodonta africana) bull in “musth,” a state ofsexual excitement characterized by aggressive posturing, continuousdribbling of urine, and secretions running from the temporal glands.(Photo by Rudi van Aarde. Reproduced by permission.)

ulation does not affect the cycle and the female can becomepregnant again as her first young (litter size usually is one)move to the pouch. The second fertilized egg undergoes di-apause (halt in development) until the first young eitherreaches adulthood or dies. In this case, the diapause is facul-tative or changes length depending on circumstances such asfood availability or season. Then, the second egg immediatelyresumes development so that birth occurs as soon as themother’s pouch is available. So at any one time, the femalecan have three young: one in the placenta, one in the pouch,and one joey out of the pouch and still suckling.

Placental mammalsPlacental mammals constitute the largest group of mam-

mals. In placental mammals, fertilized eggs migrate to theuterus or to the uterine horns where they implant and beginto develop. In the process, a placenta is grown to act as theinterface between mother and offspring. The highly vascularplacenta then connects to growing embryos via the umbilicalcord, and exchanges of nutrients and waste between motherand fetus occur in the placenta as fluids are not shared be-tween mother and fetus in the womb.

Not all placental mammals have the same reproductionscheme. Most females have estrous cycles with well-defined“heat” periods and will only accept mates and breed duringthis period. The estrous period often is fairly conspicuous andrecognized by mates through hormonal, pheromonal, or be-havioral cues. Most mammals fit in this category, and bestknown examples may include deer, dogs, and otters.

Primates are recognized by many as the most advancedmammals, possibly because of advanced cognitive skills and alarger brain relative to body size. Many primates including hu-mans do not have an estrous cycle, but instead a menstrual cy-cle. The menstrual cycle typically leads to more frequentovulation (every 28 days on average in humans) and consider-able bleeding associated with breakdown of the endometriallining in the uterus (menstruations). Moreover, females of ad-vanced primate species including humans do not show clearsign of ovulation and in many females, ovulation fits into aprocess called the menstrual cycle. In this cycle, the uterus isprepared prior to ovulation, the egg or eggs are released sev-eral days later, and if fertilization does not occur, the lining ofthe uterus degenerates and is shed during a period called themenstruations. The combination of regular but hidden ovula-tion in females probably allow primates to evolve promiscuousmating systems because males cannot assess when ovulationoccurs, and thus mate guarding either occurs throughout theyear (monogamy in many human societies), or uncertainty ofpaternity leads to child care in large promiscuous groups(chimpanzees) and lessens the risk of infanticide.

Peculiar mechanisms: Induced ovulationInduced ovulation occurs when release of eggs in females

is triggered by a stimulus, most often physical such as copu-lation, but also behavioral or pheromonal such as the vicin-ity of males. In contrast to spontaneous ovulators, or specieswhere the release of eggs depends on the seasonal photope-

riod signal, species with induced ovulation develop ova thatare ready for release but require a stimulus for release.

Induced ovulation occurs in many species, but is best un-derstood in mammalian carnivores. Examples of species withinduced ovulation include cats (Felidae), bears (Ursidae), andnumerous Mustelidae such as wolverine (Gulo gulo), stripedskunk (Mephitis mephitis), and North American river otter(Lontra canadensis). For species with induced ovulation, it ap-pears that a certain level of stimulation is required for eggsto be released, and thus it has been hypothesized that femalesmay use the ability of a male to induce her ovulation as anindicator of male vigor, hence male quality. In these species,females may not be able to compare males simultaneously andbecause of the severity of the environment, may not be sureof her ability to find mates. In this case, the best strategy forthe females would be to mate with all males encountered, andbear offspring from the male that induces the greatest stim-ulus. Evidence in black bears (Ursus americanus) of multiplepaternity within single litters suggests that induced ovulationmay be used by females as a mate choice strategy within thereproductive tract. For males, inducing ovulation may be amethod of ascertaining paternity when pair bonds must beshort to allow for encounters with other females. It is alsopossible that induced ovulation evolved as a strategy againstsexual coercion in carnivores. In this case, females forced intocopulation by males of lesser quality could abort eggs if theysubsequently bred with a better quality male that provided agreater stimulus. Although the complexity of induced ovula-tion is still being investigated, it appears that benefits may ex-ist for both males and females of species living in highlyseasonal environments.

Peculiar processes: Delayed fertilization anddelayed implantation

The opportunity to find a suitable mate is essential for re-production, but because gestation is fixed in duration, timingof mating has direct implications on the timing of parturition.However, mammals have evolved two strategies to separate



African lioness (Panthera leo) with her cubs. (Photo by Joe McDonald.Bruce Coleman, Inc. Reproduced by permission.)

in time mating and parturition: delayed fertilization and de-layed implantation.

Delayed fertilizationSperm storage occurs in bats inhabiting northern temper-

ate regions such as the little brown bat (Myotis lucifugus), andalso in many bats such as noctule (Nyctalus noctula). In the lit-tle brown bat, the testes become scrotal in the spring, andmost sperm production is completed by September. Thesperm are then stored until copulation commences monthslater. Females are inseminated in the fall and winter, whilethey are in hibernation. Sperm are then stored again, this timein the female reproductive tract, the uterus, where they re-main motile for almost 200 days in the noctule. Females ovu-late much later, and active development of the embryos startsin the spring. For bats, delayed fertilization allows males tocopulate when they are in best condition in the fall, and par-turition to occur just prior to emergence of insects. Becauseof the energy required for copulation, mating in the springwould be at the time of worst male condition. Delayed fer-tilization also allows females to give birth immediately afterspring arrives, thus allowing more time for offspring growthbefore the next hibernation period. Thus, delayed fertiliza-tion is especially advantageous for species with long periodsof dormancy, and allows females to compare breeding malesvia sperm competition.

Delayed implantationDelayed implantation is a peculiar reproductive process in

which fertilized eggs come to a halt in their development, usu-ally at the blastocyst stage. After a period of time that variesamong species and that is somewhat flexible, the blastocystsimplant on the uterine wall and start developing for a dura-tion called “true gestation.” Delayed implantation occurs in

marsupials, rodents, roe deer, and bats, but probably is bestknown in carnivores. In the Carnivora, not all species exhibitdelayed implantation, but the best examples probably are inthe Mustelidae, Ursidae, and pinnipeds (Odobenidae, Phoci-dae, Otariidae). Examples of species that have delayed im-plantation include American marten (Martes americana),wolverine (Gulo gulo), black bear (Ursus americanus), giantpanda (Ailuropoda melanoleuca), and northern fur seal (Cal-lorhinus ursinus). In bears, mating occurs after den emergencein the spring, but birth of offspring does not occur until latewinter of next year, a full 9-10 months later. Delayed im-plantation likely evolved to uncouple the tight relationshipbetween mating and birth, and because it is most prevalent innorthern species, would provide an advantage to allow par-turition at the time of greatest food availability and possiblymating to occur at the time of greatest mate availability. Pos-sibly, mating systems may influence delayed implantation andat least two species in North America show variable delay, theAmerican mink (Mustela vison) and the striped skunk (Mephi-tis mephitis), where the delay varies from 0–14 days. In thepinnipeds, delayed implantation would allow females to matewhen conditions are favorable to maximize male competitionand availability, thus allowing females to breed at a time whenseals are aggregated, thus facilitating mate choice.

Peculiar mechanisms: Inbreeding avoidanceInbreeding is a word that describes breeding of one indi-

vidual to another that is related, and in most animals, mam-mals included, is relatively rare. This is likely so becausebreeding with relatives has deleterious effects on the survivalof the offspring, and often leads to reduced fertility. In evo-lution, inbreeding is rapidly selected against. Not surprisinglythen, animals go to great lengths to avoid breeding with an-imals to whom they are related. To accomplish this, animalsmust be able to either recognize relatives (kin recognition) or,as an alternate strategy, recognize situations that could leadto breeding with relatives.

Kin recognition has been demonstrated in numerous mam-mals, and is probably most developed in humans. The alter-nate scenario of recognizing situations that lead to breedingwith relatives is thought to explain sex differences in disper-sal. In mammals, dispersal from natal areas is most commonin males whereas females tend to stay closer to the home rangeor territory of their mother. Although several explanations fordispersal have been proposed, at the top of the list is that dis-persal may reduce possibility of inbreeding. This would bemost common in polygamous species where males copulatewith numerous females. In this scenario, many of the residentfemales present during the next breeding season would be re-lated to the males, and hence, males often disperse after a suc-cessful breeding season.

Peculiar mechanism: Reproduction inarmadillos

Armadillos are placental mammals (Order Xenarthra) thatoccupy the southern United States, Central America, and thenortheastern half of South America. They differ from otherplacental mammals in numerous ways. The uterus is simplex,



A western barred bandicoot (Perameles bougainville) joey suckling inmother’s pouch. (Photo by © Jiri Lochman/Lochman Transparencies.Reproduced by permission.)

just like that of humans, but there is no vagina and instead, aurogenital sinus serves as vagina and urethra. Males have in-ternal testes and no scrotum, and have among the longer penesof mammals, reaching one third the length of the body in nine-banded armadillos (Dasypus novemcinctus). The oddities are notlimited to morphology, but include the physiology as well.

Nine-banded armadillos have unusual delayed implanta-tion. Armadillos breed in June, July or August, and the onlyfertilized egg becomes a blastocyst after 5-7 days at which pointit enters the uterus. Development then ceases and the blasto-cyst remains free-floating in the uterus until November or De-cember when it implants, and then the zygote divides twice toform four identical embryos. After 5 months of gestation, fouridentical quadruplets are born usually in May. Although iden-tical twins are known to occur in humans, nine-banded ar-madillos regularly have identical offspring, most often four ofthem. But the mystery does not end there: a captive femaleheld in solitary confinement gave birth to a litter of four fe-males 24 months after her capture, or 32 months after shecould have mated in the wild! Although the mechanism is notclearly understood, either her implantation delay lasted 23-24months, or this particular female had produced two eggs, oneof which would have remained dormant for at least 15 months.

Peculiar morphology: The mammalian penis bone

A peculiar bony structure exists in the penis of manymammalian species, and this bone, often referred to as bac-

ulum or os penis, is probably one of the most puzzling andleast understood bones of the mammalian skeleton. Presentin a variety of orders including Insectivora, Chiroptera, Pri-mates, Rodentia, and Carnivora, this bone does not occur inall Orders in the Mammalia, but also does not occur in allspecies within each Order. Within a species the bone alsovaries in size, with older individuals typically possessinglonger penis bones. In the mammals, the largest penis bonein absolute and relative size occurs in the walrus (Odobenusrosmarus), where the baculum may reach up to 22 in (54 cm)in length. In contrast, the bone is mostly vestigial in rodentssuch as North American beavers (Castor canadensis), and verysmall in all felids (cats), which have spines on the penis.

There are obvious costs to possessing a penis bone as ev-idenced from accounts of penis bone fractures. Historical hy-potheses suggested that the bone may provide additionalsupport to the penis for copulation, may protect the urethrafrom collapsing and blocking sperm passage in species thatcopulate for long periods, or else may help stimulate femalesinto ovulation. However, all hypotheses have weaknesses andthe most current hypothesis explaining the evolution of themammalian penis bone in carnivores suggest that the largestpenis bone evolved in species with promiscuous mating sys-tems as a way for females to assess male quality during cop-ulation. However, explanations may not be exclusive andpossibly other functions may exist in other taxa. Undoubt-edly, the full significance of this bone into the evolution ofmammals has not yet been fully understood and remains anenigmatic puzzle to solve for mammalian scientists.



ResourcesBooks

Adams, C. E., ed. Mammalian Egg Transfer. Boca Raton: CRCPress, 1982.

Asdell, S. A. Patterns of Mammalian Reproduction. 2nd ed.Ithaca, NY: Cornell University Press, 1964.

Eberhard, W. G. Sexual Selection and Animal Genitalia.Cambridge, MA: Harvard University Press, 1985.

Kosco, M. Mammalian Reproduction. Eglin, PA: AlleghenyPress, 2000.

Tomasi, T. E. Mammalian Energetics: Interdisciplinary Views ofMetabolism and Reproduction. Ithaca, NY: ComstockPublishing Association, 1996.

Zaneveld, L. J. D., and R. T. Chatterton. Biochemistry ofMammalian Reproduction. New York: John Wiley & Sons,1982.

Periodicals

Ferguson, S. H., J. A. Virgl, and S. Lariviére. “Evolution ofdelayed implantation and associated grade shifts in lifehistory traits of North American carnivores.” Écoscience 3(1996): 7–17.

Jaffe, K. “The dynamics of the evolution of sex: Why the sexesare, in fact, always two?” Intersciencia 21 (1996): 259–267.

Jia, Z., E. Duan, Z. Jiang, and Z. Wang. “Copulatory plugs inmasked palm civets: Prevention of semen leakage, spermstorage, or chastity enhancement?” Journal of Mammalogy 83(2002): 1035–1038.

Kenagy, G. J., and S. C. Trombulak. “Size and function ofmammalian testes in relation to body size.” Journal ofMammalogy 67 (1986): 1–22.

Larivière, S., and S. H. Ferguson. “On the evolution of themammalian baculum: Vaginal friction, prolongedintromission or induced ovulation?” Mammal Review 32(2002): 283–294.

Larivière, S., and S. H. Ferguson. “The evolution of inducedovulation in North American carnivores.” Journal ofMammalogy 84 (2003): in press.

Laursen, L., and M. Bekoff. “Loxodonta africana.” MammalianSpecies 92 (1978): 1–8.

McBee, K., and R. J. Baker. “Dasypus novemcinctus.” MammalianSpecies 162 (1982): 1–9.

Miller, E. H., and L. E. Burton. “It’s all relative: Allometryand variation in the baculum (os penis) of the harp seal,Pagophilus groenlandicus (Carnivora: Phocidae).” BiologicalJournal of the Linnean Society 72 (2001): 345–355.

Miller, E. H., A. Ponce de León, and R. L. DeLong. “Violentinterspecific sexual behavior by male sea lions (Otariidae):



ResourcesEvolutionary and phylogenetic implications.” MarineMammal Science 12 (1996): 468–476.

Moller, A. P. “Ejaculate quality, testes size and spermproduction in mammals.” Functional Ecology 3 (1989): 91–96.

Pasitschniak-Arts, M., and L. Marinelli. “Ornithorhynchusanatinus.” Mammalian Species 585 (1998): 1–9.

Patterson, B. D., and C. S. Thaeler Jr. “The mammalianbaculum: Hypotheses on the nature of bacular variability.”Journal of Mammalogy 63 (1982): 1–15.

Poole, W. E. “Macropus giganteus.” Mammalian Species 187(1982): 1–8.

Rissman, E. F. “Mating induces puberty in the female muskshrew.” Biology of Reproduction 47 (1992): 473–477.

Sharman, G. B. “Reproductive physiology of marsupials.”Science 167 (1970): 1221–1228.

Sharman, G. B., and P. E. Pilton. “The life history andreproduction of the red kangaroo (Megaleia rufa).”Proceedings of the Zoological Society of London 142 (1964):29–48.

Stockley, P. “Sperm competition risk and male genitalanatomy: Comparative evidence for reduced duration offemale sexual receptivity in primates with penile spines.”Evolutionary Ecology 16 (2002): 123–137.

Storrs, E. E., H. P. Burchfield, and R. J. W. Rees.“Superdelayed parturition in armadillos: A new mammaliansurvival strategy.” Leprosy Review 59 (1988): 11–15.

Serge Larivière, PhD

Ecology, the study of an organism’s relationship to its sur-roundings, consists of several distinct areas, all of which havetheir own specific approaches and methods. Ecophysiologydeals with physiological mechanisms, evolutionary ecology isconcerned with life history-related, fitness-relevant, and pop-ulation-genetic aspects, behavioral ecology looks at how theanimal deals with its surroundings, and community ecologyasks how groups of species can live together. This text willapproach how mammals are able to adapt to extreme condi-tions and will also consider spatial and temporal distribution,predator-prey relationships, and relationships between speciesforming similar niches.

Mammals are endotherms. This means that they have toput a great deal of energy into regulating their body temper-atures. In a cold environment, there are several strategies todeal with those challenges: mammals, contrary to reptiles, areoften capable of developing a rather thick isolatory tissue (sub-cutaneous fat) plus thick fur. This option is not open to rep-tiles due to the fact that they need to retain the high thermalconductancy of their integument in order to heat themselvesby exposure to sun rays. Small mammals, however, have thiscapability in a lesser extent than larger ones. An additionaloption for larger species is migration.

Another mammalian adaptation is known as non-shiveringthermogenesis (NST), the burning of so-called brown fat, aspecial tissue rich in mitochondria and often deposited aroundthe neck or between the shoulder blades. The most effectiveway of dealing with the challenge of a cold environment istorpor, the reduction of one’s body temperature and basalmetabolic rate, in some species to around or even slightly be-low 32°F (0°C). For example, the Arctic ground squirrel (Sper-mophilus parryii) goes down to a startling body temperatureof 28°F (-2°C). Daily torpor, or larger periods of hibernation,can be found in members of at least five placental and twomarsupial orders. The largest species found with “real tor-por,” lowering their body temperatures by at least 50°F(10°C), are badgers (both the American and the Eurasianspecies—in the latter case it was found in an individual of 27lb [13 kg] body weight). Bears also become dormant in win-ter, but their body temperature is lowered only by about 41°F(5°C), and their physiological mechanisms are different fromthose of the smaller species.

How do mammals deal with desert conditions? Deserts arenot only characterized by extreme temperatures (hot and cold,many small species thus also exhibit daily torpor), but also byarid conditions and a low biodiversity. One strategy for smallermammals to deal with this low productivity again is het-erothermy, to reduce basal metabolism and thus economize onone’s energy demand. Large mammals such as camels can alsostore heat quite effectively in their large bodies; camels can in-crease their body temperatures under heat-stress up to 106°F(41°C) during the day, and lower it to around 93°F (34°C) atnight. This can save about 12,000 kJ and 1.3 gal (5 l) of sweat.Water balance in many species of desert-dwelling mammals isimproved by a counter-current system in their nasal conchae,and by recycling water in the kidneys. Kangaroo rats(Dipodomys) are among those species that regularly live withoutthe need to drink open water; they are able to survive on thewater content of their food (seeds), and from oxidation. Graz-ing mammals can improve their water balance by feeding atnight, because grass species are rather rich in tissue fluid at thattime. Carnivores extract water from vertebrate prey—even fen-necs can keep their water balance simply by feeding on mice.The effectiveness of desert mammals is increased by behavioraladaptations, such as regularly retreating into burrows or shadyareas where it’s not only cooler but also more humid.

An even more challenging habitat for mammals is extremehigh altitude. While desert means cold plus dry plus foodscarcity, high altitude means desert plus low oxygen. Thus,physiological adaptations found in mammals at high altitudesinclude all those just discussed, plus specific ones to improvegas exchange (lung tissue and blood capillaries becoming moreintricate), better oxygen transport in the blood, and betteroxygen-dissociative capabilities from hemoglobin to body tis-sues. Also, smaller mammals in arid or mountainous habitatsoften retreat into underground burrows.

Living underground continually, or at least for a largepart of the animal’s daily activities, is as challenging an en-vironment as the one they might escape from. Members ofat least 11 families (marsupials, insectivores, and rodents)have adopted a subterranean lifestyle with two differentmethods of digging: hand digging, as performed by molesand the marsupial mole, mostly in loose soils, or tooth dig-ging, performed by rodents in hard substrates. The envi-ronment in an underground tunnel has several specific


• • • • •

Ecology

characteristics. It is often hot, rather humid, and carriesmore carbon dioxide and less oxygen than fresh air does.Most subterranean species thus are rather small (the largestreaching a few kilograms only), sparsely furred, have a lowresting metabolic rate, and have a more effective cardiac andrespiratory system (for example, myoglobin density and cap-illarization in muscle tissue is higher, hemoglobin has ahigher oxygen affinity, hearts are bigger and more effective,and the animals are more tolerant of hypoxia than related,non-burrowing species). Another way of dealing with highcarbon dioxide concentrations seems to be excreting bicar-bonates via urine, which is achieved by a high concentrationof calcium-ion (Ca2+) and magnesium-ion (Mg2+) in theurine. Subterranean mammals also encounter a unique sen-sory environment. Their preferred mode of communication,even in small species, is low-frequency acoustics, as they arerather insensitive to high frequencies and vibratory com-munication. Some mole rats (Cryptomys hottentotus, Spalaxehrenbergi) are also capable of magnetic field orientation.

There are, especially for smaller mammals, other ecolog-ical factors at least as important (if not even more so) that alsodetermine which activity patterns (being diurnal, nocturnal orcrepuscular, being active in short or long bouts, etc.) are mostadaptive under given situations. One of these factors is pre-dation. Even larger species, such as kangaroos, tend be active

at times when their predators are less likely to attack. In smallmammals, predator-prey relationships are perhaps even moredecisive. This holds true not only for prey species but also forthe predators. Small mammalian predators such as weasels,mongooses, or small dasyurids are potential prey to other rap-tors and larger mammals themselves. On the other hand, be-ing of small body size means that the energy demands andconstraints are particularly severe. Thus, they have to termtheir activity patterns much more carefully than larger species.Being potential prey puts a heavy ecological load on all smallermammals. Being active at times of low predator activity (duskand dawn, when most diurnal raptors are no longer active andmany owls and mammals not yet active) is one possibility ofescape. Being active in a synchronized way provides safety innumbers (the dilution effect), and predation stress can explainecologically the often dramatic suddenness in the onset of ac-tivity. It is also interesting to note that the onset of activity,in most species, is more fixed by internal factors—termina-tion, however, is more variable.

Besides predation, inter- and possibly intra-specific com-petition also must be considered as influencing activity. Be-ing active at different times of day or using different parts ofa habitat at different times can raise the possibility of nicheseparation, as has been shown in communities of Gerbillus aswell as heteromyid species. The behaviorally or ecologically


Vol. 12: Mammals IEcology

Migrating herds of blue wildebeest (Connochaetes taurinus), Paradise Plains, Masai Mara. (Photo by Animals Animals ©Rick Edwards. Reproducedby permission.)

dominant species in these communities regularly excludes theothers from the “best” temporal niche. Similarly, intra-spe-cific competition often drives subordinate individuals intoother temporal niches and is often the first step in excludingan individual from a group or litter, long before agonistic ex-pulsion is to be seen.

In general, there is a clear relationship between body sizeand activity patterns of mammals: the smaller the species, themore likely it is to be nocturnal. This is confirmed for bothherbivores and carnivores. Being nocturnal offers better pro-tection from being detected by predators as well as competi-tors (which is a more important factor when belonging to asmall species). In small carnivores, additionally, the effect offinding more prey during the night further enhances this pref-erence. There are, however, exceptions to this rule. Micro-tine rodents are characterized by very short, ultradian activitypatterns, which are very adaptive to the present ecologicalconditions. Insectivorous and gregarious small mongooses arediurnal, and tree squirrels are all diurnal.

Predators and prey—are they influencing each other’s pop-ulation biology? The answer to this question is as variable as

the species and ecosystems studied to answer it: populationcycles of voles, lemmings, and snowshoe hares, mostly in a3–5 year period, have long been suggested to be driven byspecialist predators. However, controlled removal of weasels(Mustela nivalis) in one study did not prevent populationcrashes of field voles, nor did it influence population dynam-ics at any other stage of the cycle. Also, for several popula-tions of snowshoe hares, both cyclic and non-cyclic ones,predators (weasels, mink, bobcats, lynx, coyotes, and severalbirds of prey) were the most frequent cause of death for ra-dio-collared hares, and hare population cycles did heavily in-fluence the reproduction, mortality, and movement of thepredators. Nevertheless, at or near peak densities, predatoractivity appeared to have almost no influence on hare den-sity. At lowest density, no influence was evident either, pro-vided that enough cover was available for the hares to retreatinto. Survival of hares was directly related to good cover andgood feeding conditions. Juvenile and malnourished individ-uals were more at risk not only due to predators but also dueto hard winters.


EcologyVol. 12: Mammals I

The black-footed ferret (Mustela nigripes) takes over abandoned prairiedog (Cynomys sp.) burrows. (Photo by © D. Robert & Lorri Franz/Cor-bis. Reproduced by permission.)

Caribou (Rangifer tarandus) eat a wide variety of vegetation, which en-ables them to survive through harsh winters. Much of their native landhas been taken over for human use, but large areas have been pro-tected by the government to preserve their habitiat. (Photo by © An-nie Griffiths Belt/Corbis. Reproduced by permission.)

In a large, comparative, long-term study of many speciesof predators and prey (wolf and lynx, weasels and stoats, andraptors and owls, and prey from European bison and moosedown to amphibians and shrews), it was found that the largestspecies were barely influenced by predators at all, that am-phibians were mostly influenced in their population densitiesby weather, and that predators in general could neither influ-ence prey densities nor fluctuations. There were, however, afew exceptions: lynx were able to limit roe deer densities be-low carrying capacity, and both wolves and lynx were obvi-ously able to influence population densities of roe and red deer.The reason might be that, contrary to most other predator-prey systems, both predators are smaller and have a higher re-productive rate than their prey. In those cases, predators mightbe able to react (numerically, by means of litter size and sur-vival) more rapidly to changing conditions than their preydoes. In many ecosystems, both temperate and tropical, largespecies of prey migrate and thus leave the areas with highestpredator activity. Both migrating gnu and caribou, for exam-ple, have been shown to lower predation risk by this strategy.Comparison of migrating and nonmigrating ungulates in theSerengeti, following a severe decline of buffalo (the largestnonmigrating herbivore there) and large predators to poach-ing, led to astonishing results: topi (Damaliscus lunatus), impala(Aepyceros melampus), Thomson’s gazelle (Gazella thomsonii),and warthog (Phacochoerus aethiopicus) seem to be predator-controlled. The red hartebeest (Alcelaphus buselaphus), a closerelative of topi (but one with a different feeding style) seem tobe regulated by intra-specific competition, and giraffe (Giraffacamelopardalis) and waterbuck (Kobus ellipsiprymnus) declined

due to poaching. At least in Thomson’s gazelle, but probablyalso others, the reason for the influence of predators on pop-ulation performance seem to be more complex than simplemortality. Vigilance and flight increase, whenever predatorpressure increases, and this of course affects all individuals, notonly the unlucky ones being killed. These costs of anti-preda-tor behavior (avoiding potentially dangerous feeding habitats,spending time alert or on the move, etc.) have to be carriedby all members of the population, and they do not bring anybenefit to the predators (contrary to the “direct costs” of killedanimals). This example demonstrates again the complexity ofthe whole issue.

How can communities, groups of several or even manyspecies, live together? The ecological term “guild” defines agroup of species that use the same resources in a comparableway. Thus we would expect them to compete for these re-sources, and either ecological displacement or niche separa-tion, at least along one or a few niche axes, should occur. Inmany guilds of species, a recurring phenomenon known ascharacter displacement exists. This means that in areas wheretwo or more competing species occur (sympatric occurrence),at least one trait should differ more pronouncedly than be-tween populations of the same species in non-overlapping (al-lopatric) habitats. One example: the ermine, a small weasel,is smaller in Ireland than in Great Britain, where an evensmaller species, the least weasel (M. nivalis) occurs sympatri-cally. Guilds of carnivores have been studied in many coun-tries, and in many cases character displacement is evident. Inareas of sympatry between two small cat species of SouthAmerica, the margay (Leopardus wiedii) and the jaguarundi(Herpailurus yaguarondi), the margay is more aboreal. Degreeof arboreality is also a frequent pattern in separate primatespecies, both in guilds of guenons and between sympatriclorisids such as the angwantibo (Arctocebus) and the potto (Per-odicticus) in tropical Africa. In the case of the lorisids, one isa smaller, more slender-built species using thinner branchesand the upper canopy, while the other is larger and morestoutly built, using the lower, thicker branches.



An adult hippopotamus (Hippopotamus amphibius) feeds on grass onthe banks of the Chobe River in Botswana. Hippopotamuses usuallyfeed at night, but on relatively cool mornings they may wander out ofthe water to feed on nearby grass. (Photo by Rudi van Aarde. Repro-duced by permission.)

Female African lions (Panthera leo) are predators in their ecosystem.(Photo by David M. Maylen III. Reproduced by permission.)

Carnivore communities are special in that direct, aggressivecompetition can be observed. Nevertheless, there are many axesalong which species can separate. One is body size, which di-rectly relates to prey size. In African savannas, lions, leopards,hyenas, hunting dogs, cheetahs, and jackals all coexist, and di-rect competition for similar-sized prey is almost fully restrictedto cheetahs versus hunting dogs. This relatively peaceful coex-istence is due to many factors: social hunting allows somespecies to take prey of much larger size than their own; theleopard is more arboreal than the other predators; and somepredator species migrate to follow their prey while others don’t.In sympatric carnivore species of similar body size, gape size(the ability to open one’s mouth more or less widely) often actsas a separating axis (as in the guild of cats in South America,mentioned above). Comparative studies of carnivore guilds inIsrael (13 species, 4 families), the British Isles (5 species ofmustelids), and East Africa (3 species of jackals) found that thereis regular separation, apart from body size, in terms of degreeof cursorial locomotion, in diameter or shape of canine teeth,and in skull length. Direct overlap of all these niche parame-ters mostly occurred when a newly introduced species such as

American mink (Mustela vison) or a recently immigrated one,such as the striped jackal (Canis adustus) in East Africa, was pre-sent. In those cases, character divergence and niche shifts orniche compression did become evident, and mostly led to dis-placement in one species (European mink [Mustela lutreola], sil-verback jackal [Canis mesomelas]).

A guild of granivorous (seed-eating) rodents was studiedin the Sonora Desert of Arizona. One cricetid and four het-eromyid species of different sizes did occur in this commu-nity, and all appeared to eat seeds of the same plant species(except for one large species eating a somewhat larger num-ber of insects and one small species eating more seeds of oneparticular bush). A remarkable difference, however, was foundin the spatial arrangement of their feeding places. The largespecies, a kangaroo rat, mostly exploited patches rich in seeds,such as near rocks or in depressions in the soil. The smallspecies, a pocket mouse, also collected seeds from patches butonly in about 6.6% of observed feeding bouts. For the rest,seeds were collected in a more systematic way, while search-ing in a “sauntering” manner. Both species used olfactory cuesto search for food. However, as the kangaroo rats movebipedally in a rapid hop, and thus can easily move from onepatch to the other, the smaller species walk quadrupedally.These differences in locomotion not only carry different en-ergetic costs but also allow the animals to make use of olfac-tory gradients (gradual increases/decreases of concentration)differently: the faster an animal moves, the easier it can de-tect an olfactory gradient when a larger patch of seeds exudessome stronger smell. The slow-moving pocket mouse, on theother hand, can sniff out individual grains.



New species of animals are still being discovered. Shown here is therecently described species of mouse lemur (Microcebus griseorufus).(Photo by Harald Schütz. Reproduced by permission.)

A four-striped grass mouse (Rhabdomys pumilio) sheltering in its bur-row from the heat of the day. When temperatures above ground reachto 108°F (42°C), temperature inside the burrows will remain below77°F (25°C). Such sheltering enables a variety of mammals to survivein desert and semi-arid regions throughout the African continent. (Photoby Rudi van Aarde. Reproduced by permission.)

The most obvious and oft-cited guilds of larger mammalscertainly are ungulate communities. Many studies have beenmade on groups of herbivore species both in temperate andtropical areas. Despite the fact that up to at least six speciesof native ungulates can coexist in temperate climes and morethan 20 in some African savannas, it is surprising that moststudies do not find obvious competition effects. Contrary tocarnivores, where inter-species killing and direct competitionover food are regular features, there is practically no evidenceof direct aggressive competition. Even indirect, long-term ef-fects on population density caused by the changing numberof another species is mostly absent. Things only change assoon as newly introduced species come into the community.Thus it was found that feral muntjacs (Muntiacus) in GreatBritain severely competed with roe deer (Capreolus). Whencattle were introduced into an area where black-tailed deer(Odocoileus) were numerous, the deer retreated into otherhabitats, which cattle avoided. Competition between speciesof deer was documented in communities of deer in NewZealand, where all three species (red [cervus elaphus], fallow[Dama dama], and white-tailed deer [Odocoileus virginianus])had been introduced. Thus it seems that guilds of ungulateshaving a long (co-) evolutionary history together can coexist,probably because there are enough dimensions along whichto separate. The most famous example is the grazer-browser

division or, more accurately, the division into concentrate se-lectors, bulk-feeders, and intermediate feeders. Apart from se-lecting leaves, grass, or something in between, there aresubdivisions in each set of species. Height preference is alsoa separating criterion for grazers: some species, such as zebra,feed on high and dry or lignified grass, while others feed onlyon lower, mostly fresh plants. Another separating axis is bitesize, which is determined by jaw/snout size and tooth rows.Animals with a broader mouth are less selective in feeding.Body and gut size are also important criteria in deciding whatto forage and how to digest. The smaller species have a higherenergy demand and specialize on high quality leaves; largerspecies feed on lower quality grass such as stems or leafsheaths, or older plants. The reason for this is that largerspecies, with larger fermentation chambers in their guts, candigest cell walls more effectively and need less energy per unitof body mass. Equids are better able to extract energy fromlarge amounts of fiber-rich food, and ruminants do better withrestricted food mass. Equids have a lower reproductive ratethan ruminants but are better able to defend themselvesagainst predators due to their sociality. Often in savannasthere is a succession of different ungulate species foraging onthe same spot, one after the other: zebras (Equus) start by eat-



A black rhinoceros (Diceros bicornis) browses on low-growing shrubs.(Photo by Rudi van Aarde. Reproduced by permission.)

The bamboo that the panda (Ailuropoda melanoleuca) eats provides itwith very little nutrition, but it is available year round. (Photo by ©Keren Su/Corbis. Reproduced by permission.)

ing the high, old, dry grass; wildebeest (Connochaetes) followand eat the lower grass plants, but still select on the level ofwhole plants; Thomson’s gazelle, with their narrow snouts,select only the freshest parts in the middle of grass plants; andkongoni feed on the long, lignified stalks that remain. Mi-grating versus non-migrating is another axis of niche separa-tion. This is the famous Bell-Jarman principle first describedfor the Serengeti and other East African ecosystems, whichallows up to eight species of grazers and about 20 species ofruminants in total to coexist.



The capped langur (Trachypithecus pileatus) is one of the rarest pri-mates and lives in the trees of Bhutan. (Photo by Harald Schütz. Re-produced by permission.)

Humans have an effect on other mammals’ ecology. Here an Antarcticfur seal (Arctocephalus gazella) has plastic packaging around its neck.(Photo by Paul Martin/Nature Portfolio. Reproduced by permission.)

ResourcesBooksDayan, T., and D. Simborloff. “Patterns of Size Separation in

Carnivore Communities.” In: Carnivore Behavior, Ecology andEvolution, vol. 2, edited by J. C. Gittleman, 243–266.Chicago: University of Chicago Press, 1996.

Halle, S., and N. C. Stenseth, eds. Activity Patterns in SmallMammals. Berlin: Springer, 2000.

Jedrzejewska, B., and W. Jedrzejewski. Predation in VertebrateCommunities. The Bialowieza Primeval Forest as a Case Study.Berlin: Springer, 1998.

Keith, L. B. “Dynamics of Snowshoe Hare Population.” InCurrent Mammalogy, vol. 2, edited by H. H. Genoways,119–196. New York/London: Plenuum, 1990.

Nevo, E. Mosaic Evolution of Subterraneous Mammals. Oxford:Oxford University Press, 1999.

Putman, R. J. Competition and Resource Partitioning in TemperateUngulate Assemblies. London: Chapman & Hall, 1996.

Reichman, O. J. “Factors Influencing Foraging in DesertRodents.” In Foraging Behavior, edited by A. C. Kamil andT. D. Sargent, 195–214. New York: Garland, 1981.

Sinclair, A. R. E., and P. Arcese, eds. Serengeti II. Chicago:University of Chicago Press, 1995.

PeriodicalsDuncan, P. “Competition and Coexistence Between Species in

Ungulate Communities of African Savanna Ecosystems.”Advances in Ethology 35 (2000): 3–6.

Oli, M. K. “Population Cycles of Small Rodents Are Causedby Specialist Predators: Or Are They? TREE 18 (2003):105–107.

Udo Gansloßer, PhD

The dietary needs of mammalsLike the rest of the animal kingdom, mammals need food

for energy and the maintenance of bodily processes such asgrowth and reproduction. The chemical compounds used tosupply the energy and building materials are obtained by eat-ing plants or organic material. Both plant- and animal-basedsources of food are made up of highly complex compoundsthat need to be digested and broken down into simpler forms.

Four of the most common naturally occurring elements—oxygen, carbon, hydrogen, and nitrogen—make up 96% ofthe total body weight of an animal. The remaining 4% is madeup of the seven next most abundant elements—calcium, phos-phorus, potassium, sulfur, sodium, chlorine, and magnesium,in that order. Necessary for many physiological processes, anychange in their concentrations may be deleterious or fatal.

An animal’s major dietary components are fat, water, pro-tein, and minerals. The main digestion products of these com-pounds are amino acids (from proteins), various simple sugarsthat are present in the food or derived from starch digestion,short-chain fatty acids (from cellulose fermentation), andlong-chain fatty acids (from fat digestion). The oxidation ofthese digestion products yields virtually all the chemical en-ergy needed by animal organisms.

Despite carbohydrates’ essential role in animal metabo-lism, their total concentration is always less than 1%. The twomajor animal carbohydrates are glucose and glycogen.

Body lipids act as energy reserves, as structural elementsin cell and organelle membranes, and as sterol hormones. Be-cause lipids can be stored as relatively non-hydrated adiposetissue containing 2–15% free water, eight times more calo-ries per unit of weight can be stored as fat than as hydratedcarbohydrates. This is the reason fat storage is essential foractive animals, while carbohydrates are a major energy reservefor plants. Hibernating mammals deposit fat and may doubletheir body weight at the end of the summer prior to hiber-nation; the white adipose tissue reserves allow them to sur-vive the winter.

In addition, there are 15 elements making up less than0.01% of the body of a mammal. These elements occur insuch small amounts that they became known as trace ele-ments. Still, they have vital physiological and biochemical

roles. Iron, for instance, is a key constituent of hemoglobinin blood and several intercellular enzyme systems. While theamount of iron found in an adult human is only 0.14 oz (4 g)—70% in hemoglobin, 3.2% in myoglobin, 0.1% in cy-tochromes, 0.1% in catalase, and the remainder in storagecompounds in the liver—growing animals need more iron,and adult females need to replace that which is lost in repro-ductive processes such as the growth of the fetus and men-struation. The dietary requirement for adult mammals is verysmall since iron (from the breakdown of hemoglobin) is storedin the liver and used again for hemoglobin synthesis. Othertrace elements include copper, zinc, vanadium, chromium,manganese, molybdenum, silicon, tin, arsenic, selenium, flu-orine, and iodine.

Animals can differ markedly in their vitamin requirements.Ascorbic acid (vitamin C), for example, can be synthesized bymost mammals, but humans and a few other mammals suchas non-human primates, bats, and guinea pigs, need to haveit supplied in their diet.

Ruminants do not appear to need several vitamins in theB group since the microbial synthesis of vitamins in the ru-minant stomach frees these animals from having to seek outadditional dietary sources.

Adaptations in the digestive systemAll carnivores, when fed a whole prey-based diet, consume

proteins and fats from the muscle, vitamins from organs andgut contents, minerals from bones, and roughage from thehide, feathers, hooves, teeth, and gut contents. Felids are setapart from other, more omnivorous meat eaters because oftheir inability to effectively utilize carbohydrates as an energysource. They therefore depend on a higher concentration offats and protein in their diet, as well as dietary sources of pre-formed vitamin A and D, arachadonic acid (an essential fattyacid), and taurine.

Herbivores, on the other hand, have adapted numerousmethods of utilizing roughage-based diets. Plankton feed-ers such as the baleen whales have a filtering apparatus thatconsists of a series of horny plates attached to the upper jawand then left hanging from both sides. As the whale makesits course through the ocean, water flows over and between


• • • • •

Nutritional adaptations

the plates, and plankton is caught in the plates’ hair-likeedges.

Ruminants and some non-ruminant herbivores (e.g.,sloths, hippos, colobines, large marsupials) utilize pre-gastricmicrobial fermentation to break down cell wall constituents,while the odd-toed hoofed animals, or perissodactyls, rely pri-marily on post-gastric fermentation.

Some small herbivores, like rodents and rabbits, have rel-atively higher nutrient requirements compared with largerherbivores. In order to meet these requirements, they mustroutinely practice coprophagy to obtain the protein, water,enzymes, vitamins, and minerals provided by the microbes.Coprophagy, which comes from the Greek copros, meaning“excrement,” and phagein, meaning “to eat,” is of great nu-tritional importance. If coprophagy is prevented in rabbits,their ability to digest food decreases, as does their ability toutilize protein and retain nitrogen. This process is reversible,however. When coprophagy is allowed again, the rabbits’ abil-ity to digest cellulose is restored.

The soft feces that a rabbit re-ingests originate in the ce-cum, or “blind gut,” a large blind pouch forming the begin-ning of the large intestine. Upon ingestion, these feces arenot masticated and mixed with other food in the stomach. In-

stead, they tend to lodge separately in the base of the stom-ach. A membrane coats the soft feces, and they continue toferment in the stomach for many hours. One of the fermen-tation products is lactic acid.

For most herbivores, the gastrointestinal microbial popu-lation is an integral component of the feeding strategies, es-pecially since most of them live on food that make cellulosedigestion essential. Some of the most important domesticmeat- and milk-producers (cattle, sheep, goats) have special-ized tracts that are highly adapted to symbiotic cellulose di-gestion; they are known as ruminants.

The stomach of a ruminant consists of several compart-ments, or in more precise terms, the true digestive stomach,the abomasum, is preceded by several large compartments. Theabomasum corresponds to the digestive stomach of othermammals. The first and largest compartment of this systemis the rumen, which serves as the main fermentation centerin which the food, after it has been mixed with saliva, under-goes heavy fermentation.

Both bacteria and protozoans reside in the rumen in largenumbers. These microorganisms work to break down cellu-lose and make it available for further digestion. The fermen-tation products (mostly acetic, propionic, and butyric acids)


Nutritional adaptationsVol. 12: Mammals I

A cougar (Puma concolor) will take down prey larger than itself, usually breaking the animal’s neck. (Photo by © Charles Krebs/Corbis. Repro-duced by permission.)

are absorbed and utilized, while gases (carbon dioxide andmethane) formed in the fermentation process are releasedthrough belching. A cow fed 11 lb (5 kg) of hay a day can giveoff 1 qt (191 l) of methane each day.

What is rumination?The act of rumination, or “chewing the cud,” is the re-

gurgitation and remastication of undigested fibrous materialbefore it is swallowed again. As the food reenters the rumen,it undergoes further fermentation. The products of fermen-tation—in the form of broken-down food particles—thenslowly pass to the other parts of the stomach, where the usualdigestive juices of the abomasum perform their work.

Ruminants secrete copious amounts of saliva that serve tobuffer fermentation products in the rumen. It also serves asa fermentation medium for the microorganisms. The total se-cretion of saliva per day has been estimated at 6–17 qt (6–16l) in sheep and goats, and 105–200 qt (100–190 l) in cattle.Since sheep and goats have an average weight of 88 lb (40 kg)and cattle, 1,100 lb (500 kg), the daily production of salivamay reach about one-third of the body weight.

The obligate anaerobic organisms residing in the rumeninclude ciliates that occur in numbers of several hundred

thousand per fluid ounce (milliliter) of rumen contents. Lab-oratory extracts from pure cultures of rumen organisms havedemonstrated cellulase activity, the enzyme that breaks downcellulose so that its byproducts become available to the hostmammal.

Rumen microorganisms can also synthesize protein frominorganic nitrogen compounds such as ammonium salts.Dairy farmers have been supplementing the feed of milk cowswith urea—normally, an excretory product eliminated in theurine—to increase protein synthesis, rather than through theuse of more expensive high-protein feed.

In the rumen, urea is hydrolyzed to carbon dioxide andammonia—the latter being used by the microorganisms forthe resynthesis of protein. Since a camel fed a nearly protein-free diet of inferior hay and dates excretes virtually no ureain the urine, it can recycle much of the small quantity of pro-tein nitrogen it has available this way. A similar reutilizationof urea nitrogen in animals fed low-protein diets has been ob-served in sheep and, under certain conditions, rabbits.

Rumen microorganisms can also contribute to the qualityof the protein that is synthesized. If inorganic sulfate is addedto the diet of the ruminant, the microbial synthesis of pro-


Vol. 12: Mammals INutritional adaptations

A camel’s (Camelus dromedarius) hump is primarily fat, which is metabolized when food is scarce. (Photo by © Dave G. Houser/Corbis. Repro-duced by permission.)

tein is improved and the sulfate is incorporated into the es-sential amino acids, cysteine and methionine.

Since the microbes in the ruminant stomach can synthe-size all the essential amino acids, ruminants are nutritionallyindependent of these, and therefore the quality of the proteinthey receive in their feed is not of vital importance.

Some important vitamins are also synthesized by rumenmicroorganisms, including several of the vitamin B groups.The natural supply of B12 for ruminants, for example, is ob-tained entirely from microorganisms.

Rumen fermentation takes place in the anterior portion ofthe gastrointestinal tract so that the products of fermentationcan pass through the long intestine for further digestion andabsorption. This way, the mechanical breakdown of the foodcan also be carried much further, and coarse and undigestedparticles can be regurgitated and masticated repeatedly.

If a comparison is made of the fecal material of cattle (ru-minants) and horses (non-ruminants), it will be found thathorse feces contain coarse fragments of still-intact food, while

cow feces are smooth and well-ground up with few large, vis-ible fragments.

Multi-compartment stomachs are not unique to the rumi-nants, or even the ungulates. Animals such as the sloth, thelangur monkey, and even certain marsupials have rumen-likestomachs. The diminutive quokka, for instance, has a largestomach harboring microorganisms that participate in cellu-lose digestion. For an animal weighing in at 4.4–11 lb (2–5kg), its stomach equals about 15% of its body weight, a num-ber similar to that found in most ruminants.

The kangaroo and wallaby are ruminant-like large marsu-pials that utilize the same mechanism of microbial fermenta-tion taking place anterior to the digestive stomach. At thebeginning of the dry season, when the nitrogen content in thevegetation starts to decline, wallabies begin to recycle ureaand continue to do so throughout the prolonged dry season.This way, they are relatively independent of the low qualityof the available feed.

There are other species-specific anatomical morphologiesthat adapt to the animal’s specific nutritional needs. The smallintestine, for instance, is the primary site of enzymatic diges-tion and absorption. The mammalian small intestine is mor-phologically divided into a proximal duodenum loopingaround the pancreas, intermediate jejunum, and distal ileum.The length of all intestinal segments in mammals relative tobody weight is longest in herbivores, intermediate in grain-and fruit-eaters, and shortest in carnivores and insectivores.Relative intestinal length, weight, and volume within eachspecies vary with sex, age, seasonal food habits, as well as withchanging nutritional requirements or food quality and thelevel of intake.



The North American porcupine (Erethizon dorsatum) derives all of itsnutrition from vegetation. (Photo by Corbis. Reproduced by permission.)

A jaguar’s (Panthera onca) diet varies with its location. It has beenknown to eat cattle and horses, deer, peccaries, larger rodents suchas capybara, paca, and agouti, and reptiles, monkeys, and fish. (Photoby Animals Animals ©Gerrard Lace. Reproduced by permission.)

The large intestine, to provide another example, varies inlength depending on the species and its dietary regimen. Itslength relative to the small intestine averages 6% in small car-nivorous mammals, 33% in omnivores, and 78% in herbi-vores as fiber digestion, bulk, and a reduced rate of passageincrease in importance.

The ceca and the large intestine work towards the fer-mentation of plant fiber and soluble plant matter, as well asthe absorption of water and small water-soluble nutrients suchas ammonia, amino acids, and volatile fatty acids. They alsofunction to synthesize bacterial vitamins.

Seasonal changes in nutritional requirementsChanges in diet often follow the changes in seasons. When

researchers at Sea World, Durban, traced the annual foodconsumption of their female dusky dolphin (Lagenorhynchusobscurus) over a 13-year period, they found that her annualfood intake jumped from 4,784 lb (2,170 kg) when she wasfive years old, to nearly 6,393 lb (2,900 kg) the year after. Thisincrease coincided with the installation of a cooling systemthat was used in the summer in the years thereafter, and af-ter her sixth year, her food consumption fluctuated between5,290 lb and 6,173 lb (2,400–2,800 kg) per year. In general,her food intake was above average during autumn and win-ter, and below average during spring and summer, and theaverage pool water temperature fluctuated seasonally.

A similar study of California sea lions (Zalophus californi-anus californianus) found that the voluntary decrease in foodintake during summer was associated with increased aggres-

sive behavior in males, while the seasonal fluctuation in non-reproductive females was negligible. Seasonal fluctuations inmale food intake was especially pronounced between the agesof four and eight, when sexual maturity was reached.

Territorial male California sea lions defended their terri-tories in the breeding season, during which they do not feed,and remain in their territory for an average of 27 days. In cap-tivity, they have been shown to lose as much as 198 lb (90 kg)during the breeding season—independent of food availabil-ity, suggesting the possibility of an endogenous rhythm. Thesimultaneous increase in aggression suggests testosterone in-volvement as well. The females, on the other hand, showedless profound fluctuations in monthly food intake than theirmale counterparts, possibly because females are non-territo-rial and do feed during the breeding season.

Seasonal variation in temperatures may also be importantas male sea lions in particular ate less when air and water tem-peratures were high and a thick fat layer was less importantfor maintenance of constant body temperature.

Sheep have also been observed to alter their diets accord-ing to the shifting seasons. They are known to consume amore fibrous type of forage such as tussock grass during thewinter season or seasons with a scarcity of resources. Two in-dependent studies, in the semiarid rangelands of Argentinaand Australia, respectively, reported that sheep preferred tus-socks only in winter, and avoided them during the growingseason. Although sheep behave generally as bulk grazers, theywill also consume, when offered, a considerable amount ofshrubs in the fall and winter seasons. This preference for ever-green shrubs corresponds with times of the year when grassesare less available or nutritious. Scottish sheep, in a compara-ble high-latitude oceanic climate, also displayed a similar feed-



The domestic cow’s (Bos taurus) stomach has evolved into four cham-bers that allow the animal to derive the most nutrients from its vege-tative diet. (Photo by © Richard T. Nowitz/Corbis. Reproduced bypermission.)

A brown bear (Ursus arctos) feeds on salmon in the summer months.(Photo by © John Conrad/Corbis. Reproduced by permission.)

ing pattern, i.e., they consumed a high proportion of shrubsonly in winter. Shrubs are also a type of forage that maintaina relatively high-protein content during the colder seasons.

Variation in the diet of a species over seasons may also bethe result of habitation in different landscapes of the same re-gion, thus linking prey use with availability. The swift fox(Vulpes velox), for example, occupies two distinct landscapesin western Kansas that are dominated by either cropland orrangeland. In spring and the fall, plants such as sunflowerseeds, and birds were consumed more frequently in croplandthan in rangeland. However, birds were more common in theswift fox diet in cropland during the fall.

Nutrition and the reproductive cycleEnergy requirements and food intake of pregnant females

are about 17–32% higher than non-reproducing females, andyet only 10–20% of this additional energy is retained as newtissue by the developing uterus. The rest of the energy is lostas heat, slowing down the growth rate and thus lengtheningthe gestation period. A slower fetal growth rate may be ad-vantageous in an environment with limited dietary protein orminerals, especially in the case of such animals as the fruit-eating or leaf-eating primate.

In females, the fetus represents 80% of the energy retainedby the uterus. Most of the increase in mass in the mother oc-curs after 50–60% of the gestation period has elapsed. Thewater content of the developing fetus also decreases while thefat, protein, and mineral content increase during gestation.The mammalian newborn, or neonate, averages 12.5 ± 2.3%protein and 2.7 ± 0.8% ash at birth. Neonatal fat, water, andenergy content vary between different species. For instance,neonatal seals, guinea pigs, and humans contain 4–8 timesmore fat than other mammals, whose content averages 2.1 ±1.0%. The fat reserves of the guinea pig are broken down justa few days after its birth, while those of the seal are retainedbecause of the cold environment and the short milk produc-tion period.

Because of the very low fat content of neonatal mammals,their high metabolism, and frequently, poor insulation, thechances of survival are only a few hours to days without carefrom the mother.

After giving birth, the production of milk by the mam-malian female bridges the dietary gap between the passive,completely dependent fetus to the weaned and more or lessnutritionally independent juvenile. Milk production, or lac-tation, enables the young mammal to continue its growth inan almost embryonic manner without having to remain



Barren-ground caribou (Rangifer tarandus) favor lichens, especially caribou moss, but they are not essential for survival. (Photo by Michael Gian-nechini/Photo Researchers, Inc. Reproduced by permission.)

anatomically attached to its mother. The female, in this way,is freed from the locomotory, nutritional, and anatomicalconstraints of carrying the fetus.

According to Lopez and Robinson in 1994, nutrient re-quirements for pregnancy are moderate in comparison withthe estimated nutrient requirements for maintenance. In thecase of captive Atlantic bottlenose dolphin, food consumptionin the females showed little increase during gestation, but was58–97% higher during lactation than during similar periodsin non-reproductive years.

For most mammals, milk production closely follows thenutrient requirements of the newborn animals. In the first fewdays, the requirements of the newborn may be substantiallylower than the mother’s potential to produce milk. As theneeds of the growing animal increase, so does its requirementsfor milk and milk production.

Lactation itself can put an enormous nutritional burden onthe female. In terms of energy expenditure, lactation is two tothree times more costly than gestation, and the female’s nutri-ent requirements may increase considerably. The total energyexpenditure, including milk produced, of the lactating femaleis about 215% higher than her non-lactating counterpart.

The production of milk generally rises during early lacta-tion and hits a maximal peak. This is the point where wean-ing takes place since the neonate has to increase its nutrientintake further by relying on nutritional sources other thanmilk.

The decline in milk production once the peak has beenreached can last for as little as five days in mice to manymonths in large ungulates. While it seems to make evolu-tionary sense for larger species to have longer lactation peri-ods, there are many exceptions to the evolutionary constraints.The hooded seal, for instance, has one of the shortest lacta-tion periods despite a maternal weight averaging 395 lb (179kg). The pup grows from 47.4 to 96.3 lb (21.5 to 43.7 kg),with 70% of the gain being fat, in just four days.

A basic rule of thumb, however, is that poorly nourishedfemales and those nursing larger litters often reduce milk pro-duction faster than do well-nourished females.

Milk compositionAccording to Elsie Widdowson in 1984, of the 4,300

species of mammals, only the milks of 176 have been analyzedfor protein, fat, and carbohydrate. Of these analyses, she said,only the figures for 48 of those species are considered to bereliable. The difficulty in the analyses lies with the fact thatmilk composition changes rather markedly during a lactationcycle.

The first milk, or “colostrum,” contains a high concentra-tion of maternal antibodies, or immunoglobins, active phago-cytic cells, and bacteriocidal enzymes. While neonatalprimates, guinea pigs, and rabbits acquire their circulatingmaternal immunoglobins in utero, other mammals such as un-gulates, marsupials, and mink depend on the colostrum astheir sole source of a passive immune system. Yet anothergroup, intermediate to these two, acquire maternal immuno-globins, both in utero and from colostrum. Among these an-imals are rats, cats, and dogs. The differences in in-uterotransfer of immunoglobins are determined by the number ofcellular layers in the placenta that separates fetal and mater-nal circulation.

In order for the secretion of colostral immunoglobins tobe effective, the neonatal gut needs to remain permeable totheir absorption and minimize any upper-tract digestion ofthese proteins. The time the mammalian intestine remainspermeable to the intact immunoglobins varies betweenspecies: 24–36 hours after birth in the case of ungulates; 16–20days in mice and rats; eight days in mink; and 100–200 daysin large marsupials. The marsupial’s prolonged absorption ca-pabilities relate to the time the young reside in the mother’spouch.

Other types of immunoglobins that occur in milk, after ab-sorption of the first wave of intact molecules has ceased, pro-tect the neonatal gut from infection.

The major constituents of milk are water, minerals, pro-teins (such as casein), fat, and carbohydrates. Protein con-centration ranges from under 3.5 oz/qt (10 g/l) in someprimates to more than 3.5 oz/qt (100 g/l) in hares, rabbits,and some carnivores. Fat concentrations vary from smallamounts in the milk of rhinoceroses and horses to more than17.6 oz/qt (500 g/l) in some seals and whales. The main car-bohydrate of placental mammal milk is the disaccharide lac-tose, a polymer of glucose and galactose. Lactose content alsoranges from trace amounts in the milk of some marine mam-



North American beavers (Castor canadensis) eat mostly cellulose, whichis broken down by microorganisms in their cecum. (Photo by © PhilSchermeister/Corbis. Reproduced by permission.)

mals and marsupials to more than 3.5 oz/qt (100 g/l) in someprimates. Marsupial milk, nevertheless, can be very high incarbohydrates, but the sugars are primarily oligo- and poly-saccharides-rich in galactose.

Compromises have to be made between the physiologicalconstraints to milk synthesis and selective pressures to maxi-mize offspring survival. The variation in milk composition be-tween species is one of them. Most aquatic mammals producehighly concentrated milks. The reduction in milk water con-tent in aquatic mammals provides a high-energy, low-bulkdiet that is useful in offsetting neonatal heat loss in cold en-vironments. It also conserves water in the mothers of species(such as the northern elephant seal) that abstain entirely fromeating or drinking during a relatively short, but intense, lac-tation. Similarly, seals that give birth on pack ice and have ashort lactation period (e.g., hooded seals—four-day lactation)or those that leave the neonate for feeding trips lasting sev-eral days produce more concentrated, higher fat milks thando other seals.

For terrestrial mammals, the largest changes in milk com-position over time occur in marsupials. Some marsupials canproduce several kinds of milk simultaneously since they mayhave young of different ages. For the embryonic marsupialconfined to the pouch, dilute, high-sugar milk provides nour-ishment similar to that occurring in the uterus of a placen-tal mammal during its longer gestation. Once the young leavethe pouch, the milk becomes more concentrated with morefat and protein and less sugar. Most terrestrial placentals pro-duce milks that are intermediate in concentration to the nu-trient-rich milk of aquatic mammals and the very dilute milksof primates and perissodactyls. The milks of domestic cattle,goats, and camels contain about one-half the protein and en-ergy per unit volume that occurs in the milks of wild even-toed hoofed mammals (also known as artiodactyls). Thedilute milks from domestic artiodactyls are more similar tothat produced by humans than they are to wild artiodactyls.Because sugars, particularly lactose, and some minerals suchas sodium and potassium are important regulators of the os-motic potential or water content of milk in the mammarygland, concentrated milks have either a low sugar (such asmarine mammals) or mineral content, while dilute milks havea higher sugar (such as primates and perissodactyls) or min-eral content.

The actual composition of the milk fat, protein, and sugaralso differs between animals. For example, the fatty acids ofmost milk are dominated by palmitic and oleic acids. How-ever, the main fatty acid of lagomorph and elephant milk iscapric acid, which is synthesized in the mammary gland. Sealmilk is composed of long-chain unsaturated fatty acids thatare probably derived directly from the diet.

In carnivores, the amino acid, taurine, appears to be es-sential for the diets of most of their neonates. The taurinecontent of colostrum is usually higher than in mature milk.However, carnivores have a much higher concentration oftaurine in the mature milk than do herbivores.



Koalas (Phascolarctos cinereus) have developed bacteria in their stom-achs to break down the toxins found in the eucalyptus leaves they eat.(Photo by © L. Clarke/Corbis. Reproduced by permission.)

ResourcesBooksRobbins, C. T. Wildlife Feeding and Nutrition, 2nd edition. San

Diego: Harcourt Brace Jovanovich, 1993.

Schmidt-Nielsen, K. Animal Physiology: Adaptation andEnvironment, 4th edition. Cambridge: Cambridge UniversityPress, 1990.

Vague, J. Obesities. London: John Libbey and Company, 1998.

PeriodicalsBarry, R. E., Jr. “Length and Absorptive Surface Area

Apportionment of Segments of the Hindgut for Eight

Species of Small Mammals.” Journal of Mammalogy, 58(1977): 1978–1984.

Bishop, J. P., J. A. Froseth, H. N. Verettoni, and C. H. Noller.“Diet and Performance of Sheep on Rangeland in SemiaridArgentina.” Journal of Range Management, 25 (1975): 52–55.

Blix, A. S., H. J. Grau, and J. Ronald. “Some Aspects ofTemperature Regulation in Newborn Harp Seal Pups.”American Journal of Physiology, 236 (1979): R188–R197.

Kastelein, R. A., N. Vaughan, S. Walton, and P. R.Wiepkema. “Food Intake and Body Measurements of theAtlantic Bottlenose Dolphins (Tursiops truncatus) in



ResourcesCaptivity.” Marine Environmental Research, 53 (2002):199–218.

Kastelein, R. A., C. A. van der Elst, H. K. Tennant, and P. R.Wiepkema. “Consumption and Growth of a Female DuskyDolphin (Lagenorhynchus obscurus).” Zoo Biology, 19 (2000):131–142.

Kastelein, R. A., N. M. Schooneman, N. Vaughan, and P. R.Wiepkema. “Food Consumption and Growth of CaliforniaSea Lions (Zalophus californianus californianus).” Zoo Biology,19 (2000): 143–159.

Kurta, A., G. P. Bell, K. A. Nagy, and T. H. Kunx.“Energetics of Pregnancy and Lactation in Free-rangingLittle Brown Bats (Myotis lucifugus).” Physiological Zoology, 62(1989): 804–818.

Lopez, S., and J. J. Robinson. “Nutrition and Pregnancy inSheep.” Investigacion Agraria Production y Sanidad Animales,9, no. 2 (1994): 189–219.

Mattingly, D. K., and P.A. McClure. “Nutrition andPregnancy in Sheep.” Ecology, 63 (1982): 183–195.

Posse, G., J. Anchorena, and M. B. Collantes. “Seasonal Dietsof Sheep in the Steppe Region of Tierra del Fuego,Argentina.” Journal of Range Management, 49 (1996): 24–30.

Robbins, C. T., and A. N. Moen. “Uterine Composition andGrowth in Pregnant White-tailed Deer.” Journal of WildlifeManagement, 39 (1972): 684–691.

Stewart, R. E. A., and D. M. Lavigne. “Uterine Compositionand Growth in Pregnant White-tailed Deer.” Journal ofMammalogy, 61 (1980): 670–680.

Squires, V. R. “Uterine Composition and Growth inPregnant White-tailed Deer.” Journal of RangeManagement, 35 (1982): 116–119.

Widdowson, E. M. “Milk and the Newborn Animal.”Proceedings of the Nutrition Society, 35 (1982): 116–119.

Worth, G. A. J., and D. M. Lavigne. “Changes in EnergyStores during Postnatal Development of the Harp Seal,Phoca groenlandica.” Journal of Mammalogy, 64 (1983): 89–96.

OtherDierenfeld, E. S. “Mammal Nutrition: Basic Knowledge and

Black Holes.” Wildlife Conservation Society.<http://www.zcog.org/>

Jasmin Chua, MS

IntroductionMammals are distributed in virtually every part of the

globe. The only extensive areas of land from which they areabsent are the Antarctic ice caps. Even in the Antarctic, sealsoccur on the coastal ice and may haul out on shore. A fewspecies live at high Arctic latitudes; polar bears (Ursus mar-itimus) have been recorded as far as 88°N and ring seals (Phocahispida) have reached the vicinity of the North Pole. Mam-mals are found on all the remaining continents, on all exceptthe most remote islands, and in all of Earth’s oceans and seas.Marine mammals are known to reach depths of 3,280 ft (1,000m) while land mammals are found from below sea level to el-evations above 21,500 ft (6,500 m). They are distributed inall biomes, including tundra, deserts, grasslands, and forests.Species in a wide range of families have adapted to an aquaticlifestyle in swamps, lakes, and rivers. Their distribution ex-tends below the surface of the earth in the case of fossorialor burrowing mammals, and above it through adoption of anarboreal mode of life or by means of flight, in the case of bats.This essay focuses on modern zoogeography (animal distrib-ution) and human effects on zoogeography in modern andhistorical times.

Mammals are classified into 26 orders, 136 families, andmore than 1,150 genera. The number of living and recentlyextinct species exceeds 4,800. This figure fluctuates as newspecies are discovered and the status of certain forms is re-vised. Advances in techniques of molecular genetic analysishave enabled taxonomists to assign taxa with increasing cer-tainty to either specific or subspecific status. During the 1990sintensive fieldwork in forested mountains along the borderbetween Laos and Vietnam revealed the existence of severalnew large mammals. These consist of a new species and genusof bovid, the saola (Pseudoryx nghetinhensis), and three speciesof muntjac, a type of small deer. These also included a newgenus, Megamuntiacus.

Fewer than 100 mammal species are either known or be-lieved to have become extinct during the last 500 years. Someof these extinct species remain virtually unknown. For exam-ple the red gazelle (Gazella rufina) of North Africa is knownonly from three specimens obtained in Algeria toward the endof the nineteenth century; no living specimen has ever beendescribed, and nothing is known of its ecology. Even more

vague is the Jamaican monkey (Xenothrix mcgregori), which isknown only from a sub-fossil jaw bone.

The order Tubulidentata contains only one species, theaardvark (Orycteropus afer), which is restricted to Africa. TheMonotremata (monotremes) and four orders of marsupials areconfined to the Australian region. Two orders of marsupialsare found only in a relatively small area of South America.The two largest orders are Rodentia (rodents), with over 2,000species and Chiroptera (bats), with almost 1,000. Both of theseoccur naturally on all continents except Antarctica, and theyare the only orders to have reached many oceanic islands. Ar-tiodactyla (even-toed ungulates) and Carnivora occur on allcontinents except Antarctica and Australia, though represen-tatives of both have been introduced to Australia. The Cetacea(whales and dolphins) and Pinnipedia (seals and sea lions) havea worldwide distribution.

Similar wide variations exist at family and species level. Nomammal species is truly cosmopolitan, that is, it occurs inevery region and every habitat, though a few species have anextensive distribution covering several continents. The graywolf (Canis lupus) has one of the widest distributions of anyterrestrial mammal and is found across North America, Eu-rope, the Middle East, central and northern Asia, and India.The common leopard (Panthera pardus) also has an extensiverange through Africa, Arabia, Turkey, the Caucasus and muchof Asia, north to the Russian Far East. In the New World,the mountain lion or cougar (Puma concolor) is distributed fromCanada to southern Chile. At the other extreme, some specieshave a distribution that encompasses only a few square miles.

Some mammals show a discontinuous distribution. Thusthe mountain hare (Lepus timidus) has its main distributionacross the polar and boreal zones of Eurasia, but a disjunctpopulation is still found at high elevations in the Alps, a relictfrom the last Ice Age when the mountains provided a refugeabove the ice sheet. That of the lion (Panthera leo) is a rela-tively recent phenomenon, and a consequence of human ac-tivity. It is now found widely in eastern and southern Africaand in a small area of western India. Well into the historicalperiod the distribution also included North Africa, the Mid-dle East, southeast Europe, and Iran but habitat loss and hunt-ing removed it from the intervening areas. In the latePleistocene the lion reached even North America, where it


• • • • •

Distribution and biogeography

attained a large size, as did other Eurasian immigrants suchas the mammoth and moose.

The diversity and richness of the mammal fauna presentat any one locality is also subject to great variation. Someplaces contain representatives of a few orders or groups andhave only a few species in total while others have an abun-dance of species from across a wide range of groups. The rea-sons for these differences are a complex combination ofevolutionary history, degree of isolation, primary productiv-ity, and habitat complexity. A latitudinal gradient is a generalpattern, with the number of species increasing from the polestowards the tropics. A similar altitudinal gradient is also com-monly observed, with the number of mammal species declin-ing with increasing elevation, though in neither of these casesis the correlation uniform. There is also a generally positivecorrelation between species diversity and habitat complexity.Smaller islands tend to have impoverished mammal faunas,which is partly a function of the species-area relationship bywhich smaller areas tend to contain fewer species of all groups.

Ancestral forms of mammals evolved at a time when thecontinents were still connected in the single land mass of Pan-gaea. This split into two large continents, Laurasia in theNorthern Hemisphere and Gondwana in the Southern Hemi-

sphere. Mammals continued to evolve as these then slowlyseparated into a series of plates that drifted apart to form thepresent continents. When plates remained isolated for longperiods of geological history as in the case of Madagascar,Australia, and South America, unique mammal faunas evolvedthat were very different from those elsewhere. In other cases,plates gradually collided or were connected intermittentlywhen lower sea levels exposed land connections, allowingmammals to mingle and disperse. Fluctuations in sea levelsalternately exposed and flooded land bridges between regions,thus permitting and preventing dispersal of mammal groupsbetween the two areas at different times. On occasions, a chainof islands formed, rather than a full land bridge, allowing somespecies to cross, but preventing others from doing so. The re-sult of these movements is that each region has a mammalfauna composed of elements that originated there and othersthat arrived subsequently and at different times from some-where else. Dispersing species interact with the existing faunaand may replace or modify the existing species.

In many cases, groups of mammals became extinct in theircenter of origin but survived elsewhere. Equids first evolvedin North America and dispersed into Asia, Europe, and Africaand also later into South America. Wild equids survive in Asiaand Africa but disappeared from the Americas around 10,000


Vol. 12: Mammals IDistribution and biogeography

Bison (Bison bison) among the hot springs of Yellowstone National Park, Wyoming, USA. (Photo by E & P Bauer. Bruce Coleman, Inc. Reproducedby permission.)

years ago until domesticated varieties were brought back bythe Spanish conquistadors in the early part of the fifteenthcentury. Tapirs also evolved in North America and dispersedsouthwards into Central and South America and northwardsinto Asia. They subsequently became extinct in North Amer-ica, leaving the current discontinuous distribution, with threespecies in Central and South America and one in SoutheastAsia.

Offshore islands can be reached by swimming mammals,and a chain of islands allows species to reach the farthest is-lands on the stepping-stone principle, moving from one is-land to another. However, the farther away an island is fromthe nearest mainland, the fewer the number of species thatsucceed in reaching them. Bats can fly to them and smallmammals may arrive by chance, carried there on logs or raftsof floating vegetation.

There are many other barriers to dispersal, such as largerivers, mountain ranges, deserts or other unsuitable habitat,the presence of predators, or competing species. Any factoror combination of factors that cause isolation may lead to fur-ther speciation (formation of new species). Variations in cli-matic conditions during the Pleistocene, especially the morethan 20 major glaciations that occurred in the NorthernHemisphere, have also had a significant effect on the distri-bution of species.

Conditions during the Pleistocene also affected marineenvironments. For example, cold Arctic and Antarctic wa-ters, rich in dissolved CO2 and O2, together with upswellingsof mineral-rich deep ocean currents generated tremendousplantation productivity, providing a foundation for the evo-lution of baleen whale diversity.

Major regionsThese differences are conventionally discussed in terms of

the division of the world into six major regions as originallyproposed in the nineteenth century and followed since with

some modifications. These are the Nearctic, Neotropics,Palaearctic, Ethiopian or Afrotropical, Oriental, and Australian.

NearcticThis region comprises North America up to northern

Mexico and Greenland. Ten orders are present, including 37families, and around 643 species. Two families are endemic,each containing a single species. These are the Antilocapri-dae (pronghorn) and the Aplodontidae (sewellel, or mountainbeaver), endemic to western North America. There are a largenumber of endemic rodents. These include the woodrats(genus Neotoma), 17 species of ground squirrel (Citellus), threeantelope squirrels, 16 chipmunks, 10 squirrels and flyingsquirrels, 12 pocket gophers, and 37 species of heteromyidrodents (pocket mice, kangaroo mice, and kangaroo rats).Characteristic larger endemic species include bison (Bison bi-son), mountain goat (Oreamnos americanus), bighorn sheep(Ovis canadensis), and thinhorn sheep (O. dalli).

The Nearctic shares many aspects of its mammal faunawith the Palaearctic and Neotropical regions. More than 80%of Nearctic families and 60% of the genera also occur in theNeotropical region. There are relatively few species ofNeotropical origin in the Nearctic fauna. Only the southernopossum (Didelphis marsupialis), the nine-banded armadillo(Dasypus novemcinctus), and some bats have survived of thosethat entered the region from the south, in contrast to themuch larger number of Nearctic species that entered theNeotropical region following formation of the Panamanianland bridge. Nearly half the families are shared with thePalaearctic region, a reflection of the length of time that thetwo regions have been connected across the Bering Strait ei-ther by a land bridge or a chain of islands. Twenty-one gen-era arrived from the Palaearctic at the end of the Pleistocene.Shared groups include several families of Carnivora (Felidae,Canidae, Mustelidae, Ursidae), deer (Cervidae), shrews (So-ricidae), and moles (Talpidae).

A number of species in high latitudes have a circumpolardistribution in the Palaearctic and Nearctic regions, such ascaribou (Rangifer tarandus), wolverine (Gulo gulo), gray wolf


Distribution and biogeographyVol. 12: Mammals I

Nearctic

Neotropical

Palearctic

Ethiopian

Oriental

Australian

Biogeographical regions of the world. (Map by XNR Productions. Cour-tesy of Gale.)

A Galápagos sea lion (Zalophus californianus wollebaecki) basks inthe sun near a brown pelican. (Photo by Harald Schütz. Reproduced bypermission.)

(Canis lupus), Arctic fox (Alopex lagopus), and moose (Alces al-ces). Musk ox (Ovibos moschatus) also once ranged all aroundthe tundra zone but is now extinct in Eurasia apart from somesmall introduced populations.

Many species in the boreal zones of both regions have anear counterpart in the other, for example pine marten(Martes martes) and stone marten (M. foina) in the Palaearc-tic and American marten (M. americana) and fisher (M. pen-nanti) in North America; European otter (Lutra lutra) andriver otter (L. canadensis); American mink (Mustela vison) andEuropean mink (M. lutreola).

Neotropical regionThe Neotropics includes South America, Central America

from southern Mexico southwards, and the West Indies. Thisregion contains a very diverse fauna. Twelve orders are rep-resented, two of them endemic. The Paucituberculata, shrewopossums, consists of three genera and five species, all foundin the Andean region. The Microbiotheria has a single species,the monito del monte (Dromiciops australis), distributed insouthern South America. The order Xenarthra (sloths, ar-madillos and anteaters) is mainly restricted to the Neotropi-cal region, with one species occurring in the southern part ofthe Nearctic. The marsupial order Didelphimorphia has 63species, all but one of which are restricted to the Neotropics.

Nineteen of the 50 families and about 80% of the almost1,100 species that occur are also endemic. These include tenendemic families of rodents, including the guinea pigs, chin-chillas, and agoutis; several families of bats; and two familiesof primates. Two genera of wild camelids (Vicugna and Lama)are endemic. The guanaco (L. guanicoe) is evidently the prog-enitor of two domesticated varieties, the llama and alpaca.

The Neotropical mammal fauna consists of three mainstrata. The ancestral fauna consisted of some very distinctiveextinct orders, the order Xenarthra and early marsupials.These were augmented by intermittent “invaders” from thenorth, such as primates, rodents, and some carnivores. Thenabout 2 million years ago during the Pleistocene, formationof the Panamanian land bridge allowed the immigration ofmany new forms from North America. These included peris-sodactyls (tapirs and horses), artiodactyls (camelids, deer, andpeccaries) and carnivores (felids, canids, and mustelids). Thiswave of mammalian invasions had a drastic effect on the ex-isting fauna and resulted in many extinctions, including thelarge herbivore orders Notoungulata and Litopterna, andground sloths. Ultimately, a unique array of mammals, per-haps as distinctive as those of Australia, disappeared alto-



Pronghorn antelope (Antilocapra americana) inhabit the Great Plainsof North America. (Photo by Joe Van Wormer. Bruce Coleman, Inc. Re-produced by permission.)

A polar bear (Ursus maritimus) swimming underwater. (Photo by MarkNewman. Bruce Coleman, Inc. Reproduced by permission.)

gether. This interchange has been mainly, but not exclusively,one-way. Many more species moved south than in the oppo-site direction. Northern species entering South America havealso proved more successful colonizers, penetrating to thesouthern tip of the continent.

The high degree of mammalian diversity is mainly a resultof South America’s isolation from other major land massesfor long periods of geological history. Climate changes dur-ing the Pleistocene and alternating wet and dry periods causedthe rainforest to contract and fragment, perhaps becoming ineffect a series of forest islands separated by dry savanna orscrub that acted as barriers to dispersal and further leading tothe development of new forms and evolution of new species.

There is considerable habitat diversity within the Neotrop-ical region. In addition to the tracts of rainforest there arealso extensive areas of dry scrub woodland, tropical savanna,temperate grasslands, desert, and high mountains. The An-des run almost the length of the continent of South Americaand reach an altitude of 22,830 ft (6,960 m) at their highestpoint. The rainforest does not cover a continuous extent butis divided into four main blocks by large rivers, mountains,and extensive areas of drier habitat types. The Atlantic rain-forest of southeastern Brazil has been completely isolated

from the Amazon rainforest for a very long time and has itsown endemic genera and species. During the Pleistocene, al-ternating wet and dry periods heavily influenced the extent ofrainforest. At times this contracted to smaller patches isolatedby expanses of arid habitats that acted as barriers to the dis-persal of rainforest mammals. Many species subsequentlyevolved in these isolated forest refugia. Large rivers also actas dispersal barriers and related but separate species occur onopposite banks. For example, the fauna north and south ofthe Orinoco in northern South America show a number ofdifferences, and the Amazon and Rio Negro also isolate somespecies.

Much of the characteristic fauna of the West Indies hasdisappeared; in fact, a disproportionate number of the mam-mals that have become extinct in recent times were endemicto the West Indies. These include an entire family contain-ing eight species of shrews (Nesophontes), a species of raccoon(Procyon gloveralleni) formerly found on Barbados, 21 speciesof rodents, and the Caribbean monk seal (Monachus tropicalis).There is still one endemic family of large insectivores—theSolenodontidae—with two extant species, one each on the is-lands of Cuba and Hispaniola (Haiti and the Dominican Re-public). These are thought to be island relicts of a formerlymuch more widespread group.



Leopards (Panthera pardus) at sunset in the Masai Mara Game Reservation in Kenya, Africa. (Photo by Mark Newman. Bruce Coleman, Inc. Re-produced by permission.)

Palaearctic regionThe Palaearctic region covers Europe, North Africa, most

of the Arabian Peninsula, and Asia north of the Himalayas,including Japan and Korea. The Palaearctic is the largest ofthe major faunal regions in terms of its geographical area andit contains a wide range of habitats. Despite this, it has thelowest rate of endemism of all the major faunal regions. Thir-teen orders and 42 families are present, none of them en-demic. About 30% of the 262 genera and 60% of the 843species that occur are endemic. The relatively low level of en-demism reflects the long periods of contact at various timeswith the Nearctic, Oriental, and Ethiopian regions. Aroundhalf the Palaearctic families also occur in the Nearctic region,a consequence of the intermittent existence of the Bering landbridge. About 60% of the families also occur in the Orientalregion.

The Palaearctic lacks the great diversity of ungulatesfound in the Ethiopian region, though a few species occur,including an endemic genus of Central Asian gazelles, Pro-capra. Groups that evolved in southern Eurasia such as deer

and caprins are well-represented, with members of the lattergroup found in virtually all the regions’ mountain ranges.

Equids and camelids both arrived from North America andstill survive in the Palaearctic, though the distributions of allthe surviving species are greatly reduced. Przewalski’s horse(Equus caballus) was last seen in the wild in the 1960s, thoughreintroduction projects aimed at returning it to the wild inMongolia began during the 1990s. Two species of wild assstill survive. Kulan, or onager (E. hemionus), is widespread inMongolia, and is still found in fragments of its former range,in western India and in Turkmenistan. Kiang, or Tibetan wildass (E. kiang), remains numerous on the Tibetan Plateau. Wildbactrian camels are now restricted to three small areas of theGobi and Takla Makan deserts.

A high-altitude ungulate fauna has evolved on the Qing-hai-Tibet Plateau, adapted to elevations above 13,000 ft(4,400 m) and prolonged periods of cold in winter. Compo-nent species include Tibetan antelope, or chiru (Pantholopshodgsonii), Tibetan gazelle (Procapra picticaudata), wild yak (Bosgrunniens), Kiang (Equus kiang), Tibetan argali (Ovis ammonhodgsoni), and blue sheep (Pseudois nayaur) with white-lippeddeer (Cervus albirostris) in the eastern third of the plateau. Thediversity of these herbivores does not approach that of theEast African savannas but they occurred in large numbers,with several nineteenth century travelers and sportsmen re-porting vast herds of thousands of animals. These numbershave since been reduced, but in the eastern steppes of Mon-golia, herds of several thousand Mongolian gazelles (Procapragutturosa) can still be seen.

Of the smaller groups, there are 19 endemic species of pika(Ochotona) distributed through the mountains of Central Asiaand the Himalayas. Two species of desmans, endemic insec-tivores, occur in the Pyrenees and Russia respectively. All butone of 20 species of dormice (Myoxidae) are endemic to thePalaearctic and there is a diverse assemblage of desert rodentsin the region: 32 jerboas (Dipodidae), and 41 gerbils and jirds(Muridae).



An American pika (Ochotona princeps) living among the rocks in Col-orado, USA. (Photo by John Shaw. Bruce Coleman, Inc. Reproducedby permission.)

The Hodgson’s brown-toothed shrew (Soriculus caudatus) inhabitsdamp areas of the forests of Bhutan, China, northern India, northernMyanmar, Nepal, Sikkim, Taiwan, and Vietnam. (Photo by HaraldSchütz. Reproduced by permission.)

In the eastern Palaearctic there are several island endemics.Japan has an endemic species of macaque (Macaca fuscata),serow (Capricornis crispus), and hare (Lepus brachyurus). TheRyukyu rabbit (Pentalagus furnessi) is endemic to two of theRyukyu Islands.

Ethiopian regionThis region includes Africa south of the Sahara, Mada-

gascar, and the southwest corner of Arabia. Its mammal faunaexhibits the greatest diversity of all the major regions and 13out of 26 orders are present. One of these is endemic, Tubu-lidentata, with a single species, the aardvark. There are 52families (18 endemic), and over 1,000 species (more than 90%endemic). Endemic families include Giraffidae, Hippo-potamidae, Chrysochloridae (golden moles), Tenrecidae (ten-recs), and Macroscelididae (elephant shrews).

Africa was once joined to the Oriental region so there aremany elements in common. One order, Pholidota (pangolinsor scaly anteaters) contains one genus (Manis) with fourEthiopian species and three in the Oriental region. There arealso many families in common, but long periods of isolation

have led to the development of unique genera, for exampleelephants, rhinos, monkeys, apes, hyenas, and cattle.

The region is noted for the impressive array of large her-bivores that occur in large numbers on the savannas of cen-tral, eastern, and southern Africa. There are also sevenendemic genera of Old World monkeys, and two out of thefour genera of great apes (chimpanzees and gorillas). Thereis also a great diversity of rodents and viverrid carnivores (23out 25 genera are endemic). There are some noteworthy ab-sences from the region, such as deer (Cervidae) and bears (Ur-sidae).

The unique nature of Madagascar’s mammal fauna is wellknown and results from its long isolation from the main-land of Africa that now lies more than 250 mi (420 km)away. Madagascar finally broke away from Africa during theMiddle Tertiary period and only a few groups of mammalsappear to have been present at that time, namely lemurs,insectivores, small carnivores, and rodents. In the absenceof competitors and later immigration, these ancestralgroups were able to radiate into diverse arrays of newspecies. The lemurs developed into three families (Lemuri-



Adult African elephant (Loxodonta africana) and calf drink water in the arid plains of Africa. (Photo by St. Meyer/OKAPIA/Photo Researchers, Inc.Reproduced by permission.)

dae, Indriidae, Daubentoniidae) containing nine genera and38 species. The tenrecs provide an excellent example ofadaptive radiation, the 27 extant species having a bewilder-ing variety of forms and occupying a great diversity ofniches. The early carnivores consisted only of mongoosesand civets and both have evolved into distinctive forms. Thefour extant mongoose species form an endemic subfamilyGalidiinae. The civets also show a remarkable development,with seven species belonging to seven separate genera inthree subfamilies. There are ten endemic rodents and anendemic bat family (Myzopodidae) containing a singlespecies. The other bats present were presumably able to flyto the island at a later stage. Almost equally striking is theabsence of so many widespread African forms such as an-telopes, zebras, larger carnivores, lagomorphs, and mon-keys. At some point, the bushpig (Potamochoerus porcus) anda small species of hippopotamus (Hippopotamus lemerlei)reached the island; the bushpig survives but the hippo be-came extinct, probably in prehistoric times.

Oriental regionThe Oriental region includes Asia south of the Himalayas,

southern China, the Philippines, and Southeast Asia up toWallace’s Line, between the islands of Bali and Lombok. Theregion has two endemic orders, Scandentia (tree shrews), with19 species, and Dermoptera (colugos). There are two speciesof colugos, often also called flying lemurs, a doubly confus-ing name as they are not lemurs and they glide, rather thanfly. There are 50 families in the region, four endemic, and260 genera, about 35% of them endemic. About two thirdsof the more than one thousand species are also endemic. En-demic families include Kitti’s hog-nosed bat (Craseonycteri-dae); tarsiers (Tarsiidae); gibbons (Hylobatidae); and treeshrews (Tupaiidae). The region has strong affinities with thePalaearctic and Ethiopian regions. There is a long landboundary with the Palaearctic along the Himalayas andthrough China, and almost 75% of the families are sharedwith the Palaearctic region. These include bears (Ursidae),deer (Cervidae), musk deer (Moschidae), and Felidae, includ-

ing the tiger (Panthera tigris). Wooded savannas formerly con-nected the Indian subcontinent with Africa, although theselinking areas now consist largely of desert. Groups in com-mon between the Oriental and Ethiopian regions include ele-phants (one species in each), rhinoceroses, big cats (lion,leopard, and cheetah), viverrids, and great apes. Orangutans(genus Pongo) occur on Borneo and Sumatra and the 14 speciesof gibbons are distributed from eastern India and southernChina through Southeast Asia. There are seven endemic gen-era of monkeys containing 26 species. Two of these are re-stricted to Sri Lanka, and two to the Mentawai Islands off thecoast of Sumatra. The Oriental region lacks the great diver-sity of antelopes and other herbivores present in Ethiopianregion, though a few species are present. Three are endemicto India, blackbuck (Antilope cervicapra), nilgai (Boselaphustragocamelus), and four-horned antelope (Tetracerus quadricor-nis). The herbivore niches are filled in part by several speciesof deer. Other artiodactyls endemic to the region include fivespecies of wild pigs, and four species of wild cattle includingthe little-known kouprey (Bos sauveli). The best-known en-demic is undoubtedly the giant panda (Ailuropoda melanoleuca),which is indigenous to western China.

Australian regionThis region includes Australia, New Zealand, New

Guinea, Sulawesi, and some islands in the southwest Pacific.The Australian fauna is the least diverse in terms of the num-ber of orders and species present, but certainly the most dis-tinctive of all the major regions. Excluding Cetacea, only eightorders of mammals are native to Australia, but five of these,Monotremata and four orders of marsupials, are endemic.The other three indigenous orders are Chiroptera, Rodentia,and Carnivora. The latter is represented only by seals, thoughone terrestrial species, the dingo (Canis familiaris dingo), wasbrought to Australia by early human inhabitants several thou-sand years ago. Further introductions have been made by Eu-ropean settlers. There are 17 endemic families, and 60% ofthe genera and nearly 90% of the species are also endemic.

This distinctive fauna is the result of long isolation afterthe region broke away from Gondwana around 55 millionyears ago. When this event took place, only the monotremes



A coyote (Canis latrans) with a fish in Texas, USA. (Photo by John Sny-der. Bruce Coleman, Inc. Reproduced by permission.)

Lion (Panthera leo) courtship in Kenya, where there is a long dry sum-mer. (Photo by Harald Schütz Reproduced by permission.)

and marsupials were present. The Monotremata are an an-cient evolutionary line composed of three species, the duck-billed platypus (Ornithorhynchidae) and two species ofechidna or spiny anteater (Tachyglossidae). Marsupials appearto have reached Australia by a filter route from South Amer-ica via Antarctica. When Australia and Antarctica separated,these original marsupials were isolated. During the 40 mil-lion years that followed they radiated to fill most of the nichesoccupied elsewhere by placental mammals. Larger species ofkangaroos and wallabies occupy the large herbivore nichefilled by ungulates in most of the rest of the world.

Rodents arrived in two separate migrations. It appears thatrodents reached New Guinea from Southeast Asia and movedon into Australia by using islands as stepping stones. Uponreaching Australia, they radiated into many species. There arecurrently around 13 genera of rats and mice. Some bats arealso thought to have reached the continent at a very earlystage, with others entering the region later from the north.There are two endemic genera.

There are four orders of marsupials. Dasyuromorphia con-tains 17 diverse genera including the Tasmanian wolf (Thy-lacinus cynocephalus), Tasmanian devil, and the numbat orbanded anteater. Order Peramelemorphia consists of smallspecies, the bandicoots and bilbies. Order Notoryctemorphiahas two species of burrowing marsupial “moles.” TheDiprodontia contains ten families and about 113 species in-cluding the familiar kangaroos, wallabies, and koala, as wellas cuscuses and possums. The Australian region contains veryfew carnivores compared with other regions, only six speciesin Australia and five in New Guinea.

In more recent times, European settlers introduced severalspecies that have succeeded in colonizing all or large parts ofthe continent. These include the house mouse (Mus muscu-lus), rabbit (Oryctolagus cuniculus), red fox (Vulpes vulpes), andferal cat (Felis catus). Several domestic herbivores have also es-tablished feral populations. Rabbits have degraded vegetationover vast areas and introduced foxes are blamed for the de-struction of much of the native fauna. House mice and feralcats are distributed across most of Australia, and the rabbitand fox over about 60%.

The island of Tasmania has many common forms and hasacted as a refuge for others. The recently extinct thylacine orTasmanian wolf (Thylacinus cynocephalus) was present here inhistoric times and is unconfirmed from the mainland. It is stillthought by some to be possibly present. The Tasmanian devil(Sarcophilus harrisii) survives only on the island but was for-merly found across Australia. Both may have suffered fromcompetition with the dingo.

Australia and New Guinea have been isolated for most ofthe last 45 million years by the 100-mi (160-km) wide Tor-res Strait, and they have been only intermittently connectedto each other. New Guinea has many marsupial species in-cluding endemic genera and one endemic monotreme species,the long-beaked echidna (Zaglossus bruijni). There are also anumber of highly endemic mice and bats. The murid faunahas evolved in isolation from that of Australia. The fauna ofthe islands at the western end of the region, lying between

the two continental shelves, is a mix of Australian and Ori-ental forms. The largest island, Sulawesi, contains a numberof endemic species. These include the babirusa (Babyrousababyrussa)—an aberrant type of wild pig, two species of anoa—the smallest of the wild cattle, and four species of macaques.

New Zealand’s mammal fauna is a special case. The islandsbroke away from Gondwana and drifted across what is nowthe Pacific about 80 million years ago. Only 11 mammalspecies are indigenous—four bats and seven pinnipeds (sealsand sea lions). However, many more have been introducedand its mammal fauna consists of 65 species. The first intro-ductions, of rats and dogs, were made by Polynesian settlerswho reached the islands around 1,000–1,200 years ago. Eu-ropean colonists arriving from 1769 onwards brought in manymore, mostly for food or game. These include 23 marsupialsand 14 ungulates (deer, chamois, and Himalayan tahr). Outof 54 known introductions, 20 came from Europe, especiallyGreat Britain, 14 from Australia, six from Asia (three surviv-ing), and 10 from North or South America (three are estab-



Red-necked wallabies (Macropus rufogriseus) are especially commonin Queensland, northeastern New South Wales, and Tasmania but alsoinhabit the coastal forests of eastern and southeastern Australia. (Photoby E & P Bauer. Bruce Coleman, Inc. Reproduced by permission.)

lished locally). Introduced species far outnumber native mam-mals and there are now more large species than small mam-mals, the opposite of the usual situation.

The smaller Pacific Islands have generally impoverishedmammal faunas reflecting the difficulties in colonizing them.The bats are the best represented order, which is unsurpris-ing in view of their ability to fly to small oceanic islands. Six-teen species of endemic bats occur on the Solomon Islandsand two more are extinct. There are five endemic species ofbats on the Melanesian Islands. One endemic species onGuam (Pteropus tokudae) is extinct, but a new species of batwas discovered on Guadalcanal in 1990. Rodents are the nextmost frequent group and there are some endemic mice. An-cestors of some of these presumably reached the islands bychance, floating on logs or rafts of vegetation.

AntarcticaWhile the Arctic is covered within the Nearctic and

Palaearctic, the fauna of Antarctica is usually omitted fromdescriptions of faunal regions. As noted above, no terrestrialmammals occur in the Antarctic but several species ofcetaceans and seals use Antarctic waters. Crab-eater seals (Lo-bodon carcinophagus) occur around the coasts and pack ice ofAntarctica and occasionally haul out on the shore. One haseven been found on a glacier at an altitude of 3,600 ft (1,100m). The Weddell seal (Leptonycotes weddellii), probably the

most southern of the world’s mammals, prefers land fast iceto pack ice and is usually found in sight of land. Ross seals(Ommatophoca rossi) also inhabit the Antarctic pack ice. Leop-ard seals (Hydrurga leptonyx) are distributed throughoutAntarctic waters where they prey on smaller species. Orcasand a few other cetaceans are regularly seen in these south-ern waters. More cetaceans and pinnipeds, including Antarc-tic fur seals and sea lions, occur farther north in subantarcticwaters and around islands such as South Georgia, MacquarieIsland, and Kerguelen. Reindeer (Rangifer tarandus) have beenintroduced to South Georgia.

The marine realmWhile seals and possibly sirenians may be included in de-

scriptions of the conventional biogeographic regions, this isnot usually the case with cetaceans. It seems worthwhile toconsider all the above in a marine realm for the sake of com-pleteness. Marine mammals are distributed from the ArcticOcean to the Antarctic and occur in the deep ocean, coastalwaters, estuaries, and in a few cases in rivers and lakes. Twoorders are fully aquatic, Cetacea (whales and dolphins) andSirenia (manatees and dugongs). The third order, the Pinni-pedia, is sometimes classified as part of the Carnivora. It con-sists of three families, seals, sea lions and fur seals, andwalruses. They are mainly aquatic but haul out onto land orice to rest, mate, and give birth.

The 76 species of whales and dolphins collectively have aworldwide distribution. Several species have extensive indi-vidual ranges in all the major oceans. Freshwater species ofdolphins live in the Amazon, Yangtze, Indus, and GangesRivers. The four living species of sirenians are found in coastalwaters, estuaries, and rivers mainly in the tropical and sub-tropical zones. Steller’s sea cow (Hydrodamalis gigas), the onlycold-water adapted species, formerly lived in the Bering Seabut was hunted to extinction by 1768.

There are 33 extant species of pinnipeds, mainly distrib-uted in temperate and polar waters but a few species are foundin the tropics. The 14 species of fur seals and sea lions aremainly distributed in the Pacific and southern oceans. Onespecies is endemic to the Galápagos Islands, and two morehave restricted distributions on Juan Fernandez and nearbyislands and islands off California. The walrus (Odobenus ros-marus), the only member of the family Odobenidae is an in-habitant of the Arctic. The 19 species of so-called true seals,Phocidae, are predominantly distributed in northern andsouthern waters. Six species occur in Arctic and subarctic wa-ters and four in the Antarctic. The Hawaiian monk seal(Monachus schauinslandi) is endemic to those islands. Isolatedspecies occur in the Caspian Sea (Phoca caspica) and in thefreshwater of Lake Baikal in Siberia (P. sibirica).

In addition, the polar bear (Ursus maritimus) and the sea ot-ter (Enhydra lutris) of western North America also spend muchof their lives in a marine environment. Taken together, ma-rine mammals amount to only about 2.5% of all mammalspecies, despite the fact that seas and oceans cover a greaterproportion of the surface of the earth than land does. This re-flects the relative homogeneity of the environment and a lackof natural barriers that allow species to evolve in isolation.



North American beavers (Castor canadensis) live in the wetlands of NorthAmerica. (Photo by Windland Rice. Bruce Coleman, Inc. Reproduced bypermission.)

The influence of humansHumans have had a profound negative impact on the dis-

tribution of the world’s mammals, through hunting, habitatdestruction, and introductions. The consequences of huntingmay have begun with early humans, as the Columbian mam-moth (Mammuthus columbi) went extinct after only 500 yearsof contact with Clovis humans. Many of the large mammalsof the Mediterranean coasts of North Africa were extermi-nated by the Romans who exported huge numbers of them toRome to be killed in public arenas. The invention of modernfirearms drastically increased the destructive potential of hunt-ing. An estimated 60 million bison (Bison bison) existed acrossNorth America at the beginning of the eighteenth century but150 years later they had been hunted to the brink of extinc-tion and their former distribution reduced to fragments. Dur-ing the nineteenth and twentieth centuries Arabian oryx (Oryxleucoryx) and gazelles were severely depleted in Arabia andNorth Africa, and the tiger (Panthera tigris) disappeared fromlarge swathes of its former distribution and from Bali, Java,and Central Asia altogether. Domestication of sheep, goats,and cattle and their subsequent spread around most of theworld have led to them becoming the most widespread of allmammals. The total biomass of domestic animals exceeds that

of wild species in many places. The domestic animals competefor grazing and through overgrazing, degrade the habitat sothat it can no longer support the original wild populationswhose ranges shrink accordingly. Some species such as ratsand mice have been introduced accidentally through transportwith ships’ cargo; others have been introduced deliberately,for sport or amenity. In virtually all cases they have had an ad-verse effect on the indigenous faunas. The effects of intro-duced foxes and rabbits on the habitats and wildlife of Australiawere mentioned above. In Great Britain, the North Americangray squirrel (Sciurus carolinensis) was released in the nineteenthcentury; since then it has steadily expanded its range in thecountry at the expense of the native red squirrel (S. vulgaris).

This generally negative trend has been partially reversedby reintroduction programs that restore former distributions.In the European Alps, reintroductions of the Alpine ibex(Capra ibex) in the nineteenth century and of lynx (Lynx lynx)during the 1980s-1990s have proven very successful. In theArabian Peninsula, the Arabian oryx (Oryx leucoryx), moun-tain gazelle (Gazella gazella), and Arabian sand gazelle (G.subgutturosa marica) have all been returned to the wild duringthe 1990s, albeit in limited areas.



ResourcesBooksEisenberg, J. F. The Mammalian Radiations. Chicago:

University of Chicago Press, 1981.

Eisenberg, J. F. Mammals of the Neotropics. Volume 1. Chicago:University of Chicago Press, 1989.

Feldhammer, G. A., L. C. Drickhamer, S. H. Vessey, and J. F.Merritt. Mammalogy: Adaptation, Diversity, and Ecology.Boston: McGraw-Hill, 1999.

Flannery, T. Mammals of New Guinea. Ithaca: CornellUniversity Press, 1995.

King, C. M. The Handbook of New Zealand Mammals. Auckland:Oxford University Press, 1990.

Macdonald, D. W., and P. Barrett. Mammals of Britain andEurope. London: Collins, 1993.

Nowak, R. M. Walker’s Mammals of the World. 6th edition.Baltimore: The Johns Hopkins University Press, 1999.

Simpson, George Gaylord. In Splendid Isolation. New Haven:Yale University Press. 1980.

Strahan, R. Mammals of Australia. Washington DC:Smithsonian Institution Press, 1995.

David P. Mallon, PhD

When asking what is typically mammalian in behavior, wemust first consider which adaptations and preconditions of amammal normally shape its life and body. Mammals are warm-blooded, or endothermic, and their system of body tempera-ture regulation through metabolism requires more energy thanwhat is needed by ectotherms. Foraging is also an importantaspect of behavior, and has to be considered as a decisive fac-tor in shaping social systems. Also, mammals in general (andfemale mammals specifically) invest a lot more in terms of time,effort, energy, nutrition, and risk, into their offspring than mostother vertebrates do. Again, this shapes social systems, in par-ticular mating and rearing, but also puts severe demands onforaging strategies. Another characteristic is the highly devel-oped brain, specifically in those areas that are necessary for be-havioral plasticity and variability, such as the highly evolvedforebrain and its hemispheres. This in turn allows the mam-mal to adapt to a diversity of ecological conditions, and also toform complex and individualized societies. In connection withthe intensive and often long periods of infant care, not only bythe parents but also other members of the group, this can lead,again, to highly variable and adaptable solutions to ecologicalas well as social problems and situations. In this chapter, wewill cover two of those areas in which mammals are special:learning and behavioral plasticity, and social systems (which in-clude mating and rearing as well as foraging and anti-predatorsystems). Each of these fields is currently the focus of scientificattention in many places, and by many different approaches. Inorder to fully understand any biological phenomenon, Tin-bergen in 1963 proposed to answer four questions, and onlyafter getting satisfactory answers to all four can we presumethat we have “explained” this phenomenon. They are:

• Where did it come from in evolution?

• What selective advantage does an individual get fromhaving this particular trait (the so-called ultimatereasons)?

• How does it work (physiology, so-called causal mech-anisms)?

• How does it develop in an individual’s life (so-calledontogeny)?

We shall use these four questions to structure our discus-sion of mammalian behavior. In order to answer these ques-

tions, a combination of different scientific approaches is nec-essary. Thus, we will draw data from long-term field studiesas well as from laboratory and zoo research, from experi-mental trials as well as from purely observational approaches,and will also need support from other biological disciplinessuch as endocrinology and molecular genetics. Behavior in it-self is at the interface of genetics and ecology, and its under-standing is central also to questions of animal welfare,conservation biology, zoo management, and our relationshipwith pets and companion animals.

Behavioral plasticityLearning in itself, of course, is by no means specific for

mammals, or even higher animals. When asking the first Tin-bergen question, we then have to look for those areas of be-havioral plasticity that distinguish mammals from theirreptilian ancestors. So-called higher forms of learning, whichrequire certain degrees of neural complexity, are (among oth-ers) spatial memory and cognitive mapping. Predators thatfollow prey, primate bands that follow certain routes betweensleeping and foraging sites, caribou that migrate over longdistances, and other mammals on the move often display anastonishing ability to cut corners, find shortcuts over ridges,circumvent deep parts in rivers after nightly rainfall, and stillarrive at their destination without delay. Caribou that are de-layed by late snowfall in spring even use these shortcuts tosave time in migration. In all of these cases, some sort of“map” must be represented in the animals’ nervous systems,and each element of the map must not only have an “address,”but also a possibility to relate it to other elements. Anotherform of behavioral plasticity is called “problem-solving by in-sight.” In typical cases, an animal is confronted by a situationit cannot immediately solve, such as bananas hanging too highto reach, or food hidden in a box. Problem-solving by insightrequires that the animal first familiarize itself with the situa-tion and then start to act in a goal-directed way (such as us-ing a tool, elongating one stick with another one, or openingthe lid of the box with a lever). Tool use has been describedfor mammals from at least six orders. A tool here is definedas a movable object that is not a fixed part of the animal’sbody, is being carried shortly before or during usage, and ispositioned in an adequate way for its subsequent use. Fol-lowing this definition, mongoose use tools to crack eggs, sea


• • • • •

Behavior

otters carry stones as anvils, elephants use twigs to swat flies,primates throw stones and branches not only to defend them-selves but also to detach fruit from trees, chimpanzees anglefor termites, etc. Remarkably, more forms of tool use havebeen described from captive than free-ranging animals, andonly in some apes do we have sufficient evidence for obser-vational learning of tool use from the field.

Even though some of these higher forms of learning andcognition can be found in some birds as well, they are not yetin any case described from reptiles, and we can thus safely as-sume that the ability for them evolved somewhere in mam-malian phylogeny. Thus, question number one seems at leastpartly answered.

What about selective advantage and survival value? It is ofcourse easy to state that animals that learn better will be bet-ter able to cope with environmental challenges and will thusbe more apt to survive. Hard evidence from carefully designedstudies, however, is scarce. In several vole species of the genusMicrotus, there is a clear correlation between spatial learningability and ranging behavior: only in species where males havelarger home ranges than females do males fare better in spa-tial learning (maze-running) tests. In food choice trials withrodents as well as ferrets and other carnivores, decision timewas significantly shorter between novel, or new, foods for an-imals reared with a more variable diet. When an animal is

quicker to reach a decision to eat something, it can eat moreper given time, and the extra amount of nutrients certainly isan advantage. Feeding can also become more efficient whensearch-images have been developed, as demonstrated withhamsters and other rodents. Animals that learn about poten-tially dangerous predators, as ground squirrels do from hear-ing other colony members giving warning calls, are anotherexample of learning with a direct survival value.

To address the third question, physiological correlates oflearning are known for at least several learning phenomena:brain areas responsible for spatial learning are larger in malesof those vole species whose spatial learning is better than fe-males, but not in those without such a sex difference. The ol-factory bulb in the brain of a young ferret during the criticalperiod of olfactory food imprinting is larger than before orafter this time. We also know that thyroxine, the hormone ofthe thyroid gland, is responsible for neurological changes dur-ing food imprinting in this species, and that oxytocin, a pitu-itary hormone, is necessary in the brain of monogamousanimals to learn who their specific partner is during pair for-mation. Several areas in the limbic system of the brain, par-ticularly the hippocampus, have been identified as beingresponsible for exploratory behavior and learning.

So, to address the fourth and last question, what data dowe have about ontogenetic influences on behavioral plastic-


BehaviorVol. 12: Mammals I

1. The silverback gorilla shows dominance through size and fur coloration; 2. Bighorn sheep posture and fight to establish dominance; 3. Wolvesuse subtle body language to show submission and dominance; 4. Kangaroos face each other, standing erect, crouching, and grooming them-selves while challenging a competitor before fighting. (Illustration by Wendy Baker)

4

3

21

ity? When observing young mammals, play behavior is amongthe most obvious patterns performed regularly. There aremany suggestions that during play, behavior is trained andgeneral reactivity and adaptability is thus improved. Again,however, there are mostly plausibility arguments for this: “Be-cause play occurs, and because it is costly in terms of time,energy, risk of injury, etc., it must have some positive effect.Otherwise, selection would have abolished it long since.”Field studies of the same species under different conditions,with different amounts of juvenile play, often find less socialcohesion in those individuals that played less. But this couldalso result from differences in other ecological conditions.

Nevertheless, we return to the question of learning and so-cialization in the discussion of social systems and social be-

havior. (There are, however, several studies on the influencesof rearing condition and environmental factors on learning andproblem-solving later in life.) From studies with laboratoryrats and mice, we know, for example, that a well-structuredenvironment, such as cages with climbing and hiding possi-bilities, is crucial to an animal’s later ability to learn how torun through a maze, explore novel situations, climb over ropes,etc. The advantage of using laboratory rodents for these stud-ies is that there are inbreeding strains that differ in learningability. Thus we have “bright” and “dumb” mice, geneticallyspeaking. However, rearing a “bright” mouse in a boring en-vironment (standard lab cage) and a “dumb” mouse in an en-riched, well-structured one leads to a near reversal of theirgenetic disposition—the “dumb” strain is now as good as, and


Vol. 12: Mammals IBehavior

Individuals of many species occupy well-defined territories and attack trespassers. 1. A white-tailed buck rubs his horns on a tree, and paws andurinates in a patch of earth to mark his territory during breeding season; 2. Howler monkeys communicate territoriality over long distances with theirvoices; 3. Wolves use voice to alert others of their location and use scat and urine to mark their territory; 4. Lemurs rub scent from their anal glandsas a territory marker; 5. Hyenas use scat, urine, fluid from anal glands, and pawing the earth to mark territory. (Illustration by Wendy Baker)

1

2

3

45

sometimes even better than, the “bright” one. Another ap-proach to ontogenetic studies of learning and problem-solving was taken in studies with juvenile macaques and vervetmonkeys. It was found that those monkeys who, as juveniles,were able to control their environment by deciding when topress a lever and get a food reward, later in life were more ac-tive in exploring and solving new situations that those thatcould press the same lever but received the same amount offood via random, computer-generated portions. Similar resultsare also described for domestic dog puppies raised in a chal-

lenging environment. Even a mild social stress, such as han-dling them a few times during early pup life, increased theiractivity levels, exploration, social initiative, and other envi-ronmentally directed activities considerably.

Social systemsSexual reproduction in animals generally puts a heavier

load on the female side. In mammals, however, this bias incost of reproduction is far more extensive due to the periodof gravidity (pregnancy) and the subsequent lactational pe-riod, both of which cannot be taken over by a male. Considera female mouse suckling six young: shortly before weaning,each young has about half her weight. Thus, she has to nour-ish and support 400% of her body weight! There is an evenhigher evolutionary pressure on mammalian females in at leasttwo aspects: females have to forage more intensively, andmore effectively, in order to cover their energetic and nutri-



A polar bear (Ursus maritimus) rolls in the snow in Cape Churchill,Canada. Polar bears keep their coats clean by swimming and rollingin the snow. Clean coats keep the bears warmer. (Photo by GarySchultz. Bruce Coleman, Inc. Reproduced by permission.)

Bottlenosed dolphins (Tursiops truncatus) leap out of the water. (Photoby Hans Reinhard. Bruce Coleman, Inc. Reproduced by permission.)

The southern opossum (Didelphis marsupialis) covers itself with a foulsaliva that discourages predators before it plays dead. (Photo by JoeMcDonald. Bruce Coleman, Inc. Reproduced by permission.)

Coyotes (Canis latrans) howl to defend their territory and inform oth-ers of their whereabouts. (Photo by Larry Allan. Bruce Coleman, Inc.Reproduced by permission.)

tional demands of reproduction. Secondly, as each young orlitter forms a rather high proportion of her total lifetime re-production, she is on heavy demand to select her potentialmating partner. Male quality is thus very important, and fe-male mate choice can be expected to be even more carefuland elaborate than in other vertebrates.

Animal social systems are supposed to evolve in the con-text of providing each individual with a so-called “optimalcompromise” regarding the demands of foraging, predatoravoidance, reproduction, and sheltering. We have to acceptthe fact that a social group (or other social unit above the in-dividual level) is not some sort of super-organism with its owndemands and evolutionary history. Instead, each social unit isbrought into existence simply and solely if it is catering to thedemands of the individual members, and will remain stableonly as long as all of its members do not have any option that,regarding this compromise, provides them with better condi-tions in total. This does not mean that the animals have tobe aware of these choices and options. For natural selectionto work, it is sufficient if they behave, based on at least somehereditary components of behavior, in the “correct” way, andtheir reward will likely be to have more, more viable, or oth-erwise advantageous young. This is the concept of Darwin-ian fitness—everyone has to put as many bearers of their owngenetic heritage into the next generation, and the one with

most young reared successfully into the next generation’s genepool is the fittest. What we as humans use to colloquially callfitness (as in going to a fitness studio) is, in the terminologyof behavioral ecology, called resource-holding power (RHP),the possibility to defend resources such as a territory, a mate,



A jackal guards a lion kill while vultures wait. (Photo by © Peter Johnson/Corbis. Reproduced by permission.)

Male lions fight for territory and supremacy. (Photo by Karl Ammann.Bruce Coleman, Inc. Reproduced by permission.)

or food, and provide those resources to one’s potential socialor mating companions.

The diversity of mammalian social systemsBefore approaching explanatory questions by means of Tin-

bergen’s questions again, a brief attempt at categorization ofsocial systems: in order to categorize the diversity of mam-malian social systems, there are several variables that need tobe described for each species. One is the degree of sociality.We find at least three types of social organization here: firstare the solitary individuals that do not regularly have any so-cial contact with conspecifics outside the narrow timespan ofreproduction. Individuals of solitary species are commonlyfound alone in periods of both activity and inactivity. Exam-ples are several species of shrews, small mustelids, and prob-ably some other small carnivores. Next are the individuals ofspecies with a dispersed social system that are also mostlyfound alone during their period of activity. They do, however,have a network of non-aggressive social relationships withneighbors (often closely related individuals) and may formsleeping groups in periods of inactivity. Examples are manyprosimian species, several small possums, some wallabies andrat-kangaroos, but also brown bears, female northern whiterhinos, female roe deer, and possibly many other species ofungulates formerly classified as solitary. Finally, gregarious or“social” species are those mostly found in groups, such as largercanids, zebras, or savanna-living bovids.

The second variable to consider is territorial defense. Aterritory is some area that is actively defended at least againstmembers of the owner’s age/sex class, where males at least donot tolerate other fully adult and reproductively active males.Territories thus cannot be “automatically” assumed as a

species’ characteristic trait, from the fact that some individu-als are solitary. Solitary species may well live in undefended,overlapping home-ranges, or even avoid each other activelywithout defending a territory, as can be seen in females ofsmaller cats as well as domestic cats in suburban areas (thereare, however, also social feral cats). On the other hand, activedefense of territories can also be found in truly social species,such as the European badger, the chimpanzee, larger canids,or the spotted hyena.

The third variable to describe mammalian social systemsconcerns the degree of overlap in the home range. This is, ofcourse, something that can only be found in species with adispersed or gregarious system. We can roughly distinguishfour types here:

• Pairs are found, when one male and one femaleoverlap in their range. This does not necessarilymean that they are found together, such as in gib-bon pairs. So-called solitary ranging pairs such astupaias, red fox, or some prosimians are a commontype of mammalian social organization. Pair-livingalso is not necessarily connected with a monoga-



An Australian sea lion (Neophoca cinerea) juvenile acknowledges anadult. (Photo by Hans Reinhard/OKAPIA/Photo Researchers, Inc. Re-produced by permission.)

A Madagascar hedgehog (Microgale longicaudata) demonstrates typi-cal prehensile tail behavior. (Photo by Harald Schütz. Reproduced bypermission.)

mous reproductive system, because extra-pair cop-ulations are not uncommon.

• Polygynous systems are those with one male and sev-eral females’ ranges overlapping. This system is oftencalled a “harem,” or “uni-male group.” Again, fromlooking purely at numbers of animals in the group,

we cannot fully describe the structure. “Harems” maybe kept together solely by the male’s herding behav-ior, such as in hamadryas baboons, or they may staytogether even in the male’s absence, such as in plainsor mountain zebra, even though the mares are not re-lated to each other. Or, they may consist of a matri-line, a clan of closely related females, such as in patasmonkeys, forest guenons, or Eurasian wild boar.

• Polyandrous systems are those in which two or moremales overlap with one female. This is found in somelarge canids, e.g. the African hunting dog, but is gen-erally more common in birds than mammals.

• Multi-male/multi-female systems where more thanone adult of both sexes overlap are typical for manydiurnal primates, large bovids, lions, or small diurnalmongooses. In these, but also in polyandrous (rarelyin polygynous) systems we cannot automatically as-sume that all adult members are reproductively active.Helpers, such as in canids or dwarf mongoose, can befully adult but reproductively suppressed individuals.The degree of reproductive cooperation and suppres-sion is thus the last variable to consider, again mostlyfor gregarious (or theoretically at least, disperse)species. There are very few truly eusocial species of



Bison (Bison bison) cluster closely when fleeing, a behavior that greatly reduces the opportunity for wolves to take down a single bison. (Photoby Erwin and Peggy Bauer. Bruce Coleman, Inc. Reproduced by permission.)

A leopard (Panthera pardus) practices fighting with its mother. (Photoby Fritz Pölking. Bruce Coleman, Inc. Reproduced by permission.)

mammals (the naked mole-rat and some other bathy-ergids), which means that reproductive suppression isirrevocable, leading to sterile worker castes and anoverlap of several generations to be found. However,helpers can be found in many families (callitrichids,canids, marmots). These helpers normally are theyoung of previous years that remain within their par-ents’ group and range, refrain from reproducingthemselves, and help in rearing their parents’ next off-spring. The degree of helping often depends on thedegree of relationship between helpers and the nextlitter (as demonstrated for the alpine marmot). Help-ing can be done by carrying them (callitrichids), feed-ing, guarding, and playing (canids), keeping the nestwarm (marmots), or taking part in anti-predator vig-ilance or defense (dwarf mongoose).

Sociality in the framework of Tinbergen’s questionsWhat do we know about phylogeny? It is not normally

possible to find behavior in fossilized form, thus we have totake another, but also reliable approach, by comparing thephenomenon in question among as many living species as pos-sible. When doing this with regard to social systems, the mostbasic one seems to be a sort of solitary or dispersed femalesystem, foraging alone in undefended home ranges. This pat-

tern can be found in members of so many different taxa thatwe may assume it to be one that their common ancestors prob-ably shared. Taking males into account as well, we can as-sume that a system of dispersed polygyny, one maleoverlapping the ranges of several females, probably was thebasic male-female system. From the basic female system, evo-



A Japanese macaque (Macaca fuscata) grooming session. (Photo by Herbert Kehrer/OKAPIA/Photo Researchers, Inc. Reproduced by permission.)

A spotted hyena (Crocuta crocuta) feeds on a young elephant that alion killed earlier. (Photo by Harald Schütz. Reproduced by permission.)

lutionary paths could have led either via territorial defense(then group defense and dispersed feeds) to social foraging ingroup territories, or without defense, via formation ofephemeral, and then later persistent groups.

What do we know about selective advantages of sociality?Behavioral ecology and sociobiology, those areas of behav-ioral biology that deal with this question, are among the mostproductive ones in about 20–30 years. Thus, only a few stud-ies should be mentioned, to cover several aspects of this ques-tion. Anti-predator vigilance in the dwarf mongoose is, overa longer period of time, only guaranteed in groups of at leastsix adults; smaller groups sooner or later fell prey to raptors.Jackal pairs with one or more helpers had more success inrearing young—the energetic demand on parents for huntingand producing milk was significantly lower, and juvenile sur-vival higher. Adult male sugar gliders that share dominancewith an adult son have a higher proportion of time spent withyoung in the absence of the mother, which is helpful in de-fending as well as warning them. Pairs of klipspringer taketurns in anti-predator vigilance, one feeding while the otherwatches out. Eastern gray kangaroos form larger groups inopen areas and also during those times of the day when theirmain predator, the dingo, is likely to hunt. Lastly, survival ofalpine marmots is higher when more young of the previousyear hibernate together with their parents.

Physiological mechanisms that regulate mammalian socialbehavior are also currently subjects of intense studies. We al-ready heard about the influence of oxytocin on developmentof social bonding, studies which have predominantly beenconducted on the monogamous vole Microtus ochrogaster. Pro-lactin has been identified as the hormone of parental care,

and, excitingly enough, is not only maternal but also elevatedin helpers, such as subordinate individuals in canid packs thathelp to rear the alpha pair’s young. Testosterone in both sexesis connected with status/dominance position. Remarkablyenough, testosterone levels often follow, not precede, an in-crease in status such as after winning a fight. Cortisole, oneof the stress-related glucocorticoids, actively lowers status-re-lated behavior and makes an individual more submissive, par-ticularly in contest-related aggressive situations. Stressfulreactions to potentially harmful or frightening situations arelower, or absent, if the situation is encountered in the pres-ence of one’s bonding mate.

Finally, some data related to the fourth Tinbergen ques-tion, ontogeny. The importance of complete socialization hasbeen demonstrated in countless studies. Guinea pig males thathad been reared in an all-female group were unable to inte-grate themselves peacefully into new colonies at sexual ma-turity due to a lack of two important behaviors: they did notbehave submissively towards adult males, and they courtedany female (even firmly bonded ones) that they might meet.However, young males reared in the presence of an adult maleperformed “correctly” immediately after introduction, andthus were integrated without any stress or aggression. Feralcats reared in the presence of other cats (or people) apart fromtheir mothers and litter-mates, and coyote pups raised in pres-ence of adult helpers at the den, became more gregarious thanthose without these influences. Monkeys reared in isolationwere unable to perform socio-sexual behavior correctly, ifthey did not get at least regular play sessions with other ju-veniles. Female monkeys without experience in baby care(prior to giving birth themselves) were less competent in han-dling their own infants.



ResourcesBooksAlcock, J. Animal Behavior. New York: Sinauer, 2001.

Broome, D., ed. Coping with Challenge. Berlin: DahlemUniversity Press, 2001.

Gansloßer, U. Säugetierverhalten. Fürth, Germany: Filander,1998.

Geissmann, T. Vergleichende Primatenkunde. Berlin: Springer,2002.

von Holst, D. “Social Stress in Wild Mammals in TheirNatural Habitat.” In Coping with Challenge, edited by D.Broome, 317–336. Berlin: Dahlem University Press, 2001.

Jarman, P. J., and H. Kruuk. “Phylogeny and SpatialOrganisation in Mammals.” In Comparison of Marsupial andPlacental Behavior, edited by D. B. Croft and U. Gansloßer,80–101. Fürth, Germany: Filander, 1996.

Pearce, J. D. Animal Learning and Cognition. New York:Lawrence Erlbaum, 1997.

Sachser, N. “What Is Important to Achieve Good Welfare inAnimals?” In Coping with Challenge, edited by D. Broome,31–48. Berlin: Dahlem University Press, 2001.

Shettleworth, S. J. Cognition, Evolution, and Behavior. Oxford:Oxford University Press, 1998.

Tomasello, M., and J. Calli. Primate Cognition. Chicago:University of Chicago Press, 1997.

Periodicalsvon Holst, D. “The Concept of Stress and Its Relevance for

Animal Behaviour.” Advances in the Study of Behaviour 2(1998).

Schradin, C., and G.Anzenberger. “Prolactine, the Hormone ofPaternity.” News in Physiological Sciences 14 (1999): 223–231.

Tinbergen, N. “On the Aims and Methods of Ethology.”Zeitschrift für Tierpsychologie 20 (1963): 410–433.

Udo Gansloßer, PhD

In 1871 Charles Darwin’s inclusion of mind and behaviorin his theory of evolution gave scientific legitimacy to the in-vestigation of animal thinking. Since that time, animal intel-ligence and cognition have been of interest to psychologists,anthropologists, ethologists, biologists, and cognitive scien-tists. The first published treatments of animal cognition wereanecdotal observations that were richly interpreted to showthe complexity of animal reasoning. Those anecdotal obser-vations were criticized for their lack of objectivity, leading tothe introduction of more objective techniques such as exper-imental studies and more careful interpretation of results. Asthe field of animal cognition has progressed, emphasis on sci-entific rigor and objectivity has characterized research. Thisessay provides an overview of animal cognition as well as sug-gesting directions that research in the early 2000s is taking.Most of the current research and theory in animal cognitionfocuses on the cognitive abilities of nonhuman primates. Thatemphasis is reflected here. The topics chosen for this reviewinclude those that are currently dynamic and are likely to showthe most growth over the next several years. This overviewprovides a point of entry for those interested in exploring cog-nitive abilities in animals.

The question of animal intelligenceIntelligence has been a difficult characteristic to define

and study in humans. Various definitions and theoreticalperspectives abound, addressing such issues as whether in-telligence is composed of one general factor or several fac-tors and, if several, which ones. Regardless of theoreticalstance, the measurement of intelligence has been difficultand fraught with controversy. As with the concept of intel-ligence in humans, intelligence in nonhuman animals hasbeen difficult to define and investigate. A definition of in-telligence applicable to nonhuman animals includes aspectsof learning, memory, social cognition, conceptual ability,problem-solving ability, and cognitive flexibility. Measuresof intelligence must include items or tasks appropriate to theorganism being studied. The determination of intelligencein animals is complicated by the lack of verbal ability in non-humans. It is difficult to pose a question to an animal whocannot respond with a verbal answer. Investigators in ani-mal behavior and intelligence have developed several tech-

niques designed to understand the animal mind through di-rectly observable behaviors. Examples of these techniquesare considered below.

Brain size and the phylogenetic scalePeople often characterize animals of different species as

more or less intelligent, and television programs delight inquestions such as “What is the most intelligent species ofanimal?” Scientists have looked to brain size as a way to pre-dict intelligence across species, but absolute brain size doesnot work, as body sizes vary so much across animal species.The encephalization quotient (EQ) was developed as a mea-sure of relative brain size. The EQ is a calculation based onthe size of a species’ brain compared to the expected sizebased on body size. An EQ of 1.0 indicates that the brainsize is the size expected for the species body size whereas anEQ over 1.0 indicates a brain that is larger than would beexpected and an EQ less than 1.0 indicates a smaller brainthan expected. Humans have the largest EQ (7.0), with mon-keys and apes (1.5–3.0) and dolphins (up to 4.5) also highon the EQ scale of living species. Although the EQ (as wellas other measures of brain complexity) is consistent with ex-pectations of relative cognitive complexity, it indicates noth-ing about the types of cognitive abilities available to animalsof different species.

Historically, the study of animal cognition began with at-tempts to arrange species along a phylogenetic scale in orderof intelligence. This approach was guided by Aristotle’s pro-posal that organisms can be arranged along a “ladder of life”with humans at the top and other animals at different rungs,or levels, down this ladder. This concept, the scala naturae, isno longer accepted in comparative studies of animal behav-ior or intelligence. Rather, evolution is perceived more as atree-like structure with individual species or groups of speciesbranching off as they evolve adaptations that distinguish themfrom ancestral forms. From this perspective, animals are stud-ied in the context of their ecological niche, the specific envi-ronment in which the organism evolved, and comparisons aremade across species that share evolutionary ancestors. Eachspecies of animal has evolved sensory capacities and a behav-ioral repertoire that allow success in that species’ particularecological niche. What is “intelligent” behavior for one ani-


• • • • •

Cognition and intelligence

mal might not be so for an animal living in a different habi-tat. In this sense of intelligence, each species has its own typeof intelligence. Investigators interested in animal intelligencehave turned from global measures of intelligence and have fo-cused research on various cognitive capacities such as basicprocesses like learning and memory, complex concepts likenumber, cognitive flexibility shown by tool use and con-struction, social cognition, and symbolic processing. The fo-cus here will be on those cognitive processes.

Why study cognition in animals?

Scientific curiosityA major reason for studying cognitive abilities in a partic-

ular species is to understand more about that species. Scien-tific curiosity drives many investigations of animal cognition.As we attempt to describe and understand natural phenom-ena, the question of the animal mind has increasingly been asubject of scientific investigation. New theoretical approachesand innovative methodologies have led to significant advancesin the past 20 years in understanding how animals think. Thestudy of animal cognition has been added to the study of an-imal behavior, ecology, and evolution as we continue to in-vestigate the biology of our world.

To understand evolutionComparing cognitive abilities across evolutionarily closely

related species can provide hypotheses about how evolutionoccurred. Darwin’s inclusion of minds in his principle of evo-lutionary continuity opened the area of nonhuman animal in-telligence to scientific scrutiny. Because there are no fossilsof behavior—only of physical structure and artifacts that im-ply behavioral capacities and inclinations—the relationshipbetween structural and behavioral capacities in currently ex-isting species is a major window into evolution. Studies ofcognitive abilities across primate species provide understand-ing of human evolution. The search for understanding of ourown species and its evolution guides much research on ani-mal cognition. Evolutionary continuity also underlies the in-vestigation of animal cognition in attempts to develop animalmodels for human phenomena. In some cases it is difficult tostudy a psychological process directly in humans. For exam-ple, although it is apparent that human memory relies on bothverbal and nonverbal processes, it is difficult to study non-verbal memory in humans, who encode almost all informa-tion linguistically.

ConservationUnderstanding the cognitive abilities of animals and how

they use these capacities to solve daily problems of finding


Vol. 12: Mammals ICognition and intelligence

Barbary macaque (Macaca sylvanus) adults grooming, with baby. (Photo by Animals Animals ©J. & P. Wegner. Reproduced by permission.)

food, evading predators, avoiding other physical dangers, andreproducing can provide important information for conser-vation. As habitat destruction continues to threaten the exis-tence of many animal species, the more information availableabout ecology and behavior, the more informed can be plansfor delaying extinction. The design and location of protectedreserves relies on understanding needs of those animals be-ing protected. Such understanding is also vital to promote thewelfare of those individuals who are housed in captivity, re-gardless of their endangered status. Providing captive animalswith cognitive enrichment by challenging their cognitive skillscontributes to their psychological well-being.

Finally, as we understand more about the cognitive com-plexity of the animals we are attempting to preserve, the im-portance of ensuring their survival is apparent. These threereasons for studying animal cognition (scientific curiosity, un-derstanding evolution, and conservation) are exemplified bythe Think Tank exhibit at the Smithsonian Institution Na-tional Zoological Park. This exhibit, which opened in 1995,is dedicated to the topic of animal thinking. As the first ex-hibit of its kind in any zoo or public forum, Think Tank com-bines basic research with cognitive enrichment for captiveanimals while educating the public about the cognitive com-plexity of animals. Daily live demonstrations of data collec-tion with orangutans (Pongo spp.) show zoo visitors howorangutans solve complex problems such as acquiring lan-

guage symbols and demonstrating numerical competence.The opportunity to observe an animal using complex cogni-tive abilities to solve a problem not only informs visitors ofthe capabilities of great apes, it also serves to illustrate the im-portance of preserving animals with such complex minds.

Basic processes: learning and memoryLearning is generally defined as a relatively permanent

change in behavior as a function of experience. Most organ-isms show the capacity to learn. Early studies of intelligencein animals used learning tasks to attempt to characterizespecies differences in capacity.

In a series of studies investigating the learning skills of rhe-sus monkeys (Macaca mulatta), Harry Harlow showed in 1949that, following extensive experience with large numbers of in-dividual problems, monkeys were able to solve a novel prob-lem in only one trial. The problems involved making a choicebetween two objects that differed from each other in severalphysical dimensions such as color, shape, material, size, andposition. A reward such as a peanut was hidden under one ofthe objects. The monkeys gradually learned to choose con-sistently the rewarded object. At that point Harlow would in-troduce a new problem with novel objects. Over the courseof many individual problems, the monkeys took fewer trialsto reach a high level of performance.

Following a few hundred such problems, the monkeyswere consistently correct on the second trial of each new


Cognition and intelligenceVol. 12: Mammals I

A chimpanzee (Pan troglodytes) uses a stick to get termites in Sweet-waters Reserve, Kenya. (Photo by Mary Beth Angelo/Photo Re-searchers, Inc. Reproduced by permission.)

A goat uses a tree stump so she can reach high vegetation. (Photo byAntony B. Joyce/Photo Researchers, Inc. Reproduced by permission.)

problem. That is, the monkeys no longer required a periodduring which they learned to choose the rewarded objectthrough trial-and-error. Rather, their response on the firsttrial of a new problem (whether it was correct or incorrect)informed them which object to choose on subsequent trials.This understanding of the solution to the problem based onone experience with two novel objects was called “learningset,” or “learning to learn” by Harlow. It is a good exampleof cognitive flexibility. Learning set is still used to study as-pects of learning and cognitive flexibility in humans and non-humans. Animals of a multitude of species are capable oflearning set, including cats, rats, squirrels, minks, sea lions,and several species of monkeys. The investigation of learn-ing set in rats demonstrates the importance of consideringthe species-typical sensory capacities of an animal whenstudying cognition. Rats, who have very poor vision but ex-cellent olfactory ability, have some difficulty with visuallearning set but easily achieve high levels of performance witholfactory discriminations.

Memory provides mental continuity across time by al-lowing information from one point in time to be used at alater point in time. That time span can be in seconds orminutes (short-term or working memory), hours, days, orlonger (long-term or reference memory). It forms the ba-sis for learning, since without memory the influence of past

experiences would not exist. Memory involves threeprocesses: encoding, storage, and retrieval. Encoding refersto the form or code in which items or events are stored;storage involves the way that memories are stored in thebrain including where, how, and how long; and retrievalrefers to the act of remembering, or accessing informationthat was previously stored in memory. Two ways of study-ing retrieval are through recall and recognition measures.In recall, an individual is asked to reproduce the items orinformation stored at a previous time. In humans recall usu-ally involves verbal reports. Recognition measures simplyask “Have you seen (experienced) this item before?” and in-volve presenting various items that were and were not inthe memory set being tested. The individual is required torespond in a way that implies “yes” or “no.” Because it canbe nonverbal, this form of retrieval is most commonly usedwith nonhuman animals.

The above distinctions and methods are relevant to labo-ratory research with animals, and they are addressed specifi-cally below. However, memory clearly plays a role in ananimal’s daily life. Food-related behaviors such as foraging orstoring food for later use require memory. To what extentmemory is used in foraging, and how that process is used, hasbeen addressed in field studies of nonhuman primates. Thequestion is whether monkeys and apes use memory to guide



An African leopard (Panthera pardus) stores its kill (an impala) in a tree. (Photo by Tom Brakefield. Bruce Coleman, Inc. Reproduced by permission.)

their travel when foraging. For animals like gorillas (Gorillagorilla) or leaf monkeys (Presbytis spp. and Trachypithecus spp.)whose sources of food are easily found and available in largequantities at one site (“banqueters”), remembering the loca-tion of particular food sources may not be a crucial aspectof their foraging activity. For species like orangutans and ca-puchin monkeys (Cebus spp.) whose food is distributed inpatches that change in availability as fruits mature (“for-agers”), memory of where particular trees are located as wellas when they fruit may be important. Researchers have in-vestigated whether foraging paths in social groups can bebetter explained by opportunistic searching or by memory-guided paths to sites that are seasonally plentiful. They havefound evidence that not only do monkeys remember whereplentiful sources of fruit are located, they also rememberwhen the trees will be fruiting.

Questions surrounding memory in nonhuman animals re-fer to capacity, duration, and organization. These questionsare addressed in laboratory experiments, some of which aredesigned to provide similar challenges to those provided inthe animal’s natural environment. A good example of this isthe radial maze, developed to study memory in rats. The mazeconsists of a center circular area to which are attached straightalleys or runways (arms) in a manner like spokes attached tothe hub of a wheel. Goal boxes at the end of each runway

provide incentives. This apparatus simulates the foragingchallenge presented to rats in their natural ecology. The ratis released into the center area and observed to see how it willobtain all the food. The rat’s task is to run down an arm, eatthe food in that goal box, return to the center area, and chooseanother arm to enter, repeating this until all the food has beenfound. Returning to an arm that was previously visited is con-sidered an error. The most efficient solution is for the rat torun down each arm only once. To do that, the rat has to relyon memory of where it has been. Rats show effective use ofmemory in the task, and researchers have demonstrated thatthis memory is based on the formation of a spatial map of themaze. Cues from the room containing the maze are used toremember the locations of the arms that have been explored.

Research with humans has shown that humans have a largecapacity for remembering items and events over long periodsof time. Monkeys and orangutans have shown that they re-member photographic stimuli over a delay of at least a year.Even more impressive, a chimpanzee (Pan troglodytes) showedmemory for symbols learned 20 years before. Memory forconcepts has been shown by squirrel monkeys (Saimiri spp.)over a five-year period, by rhesus monkeys across seven years,and by a sea lion over a ten-year period. These findings arelimited only by the test intervals imposed by researchers; thelimitations of specific or conceptual memory in animals have



A lion stalking prey near a waterhole in Tanzania. (Photo by Robert L. Fleming. Bruce Coleman, Inc. Reproduced by permission.)

not yet been demonstrated. It is likely that animals have verylong-duration memory capacity, especially for conceptual in-formation.

Many experimental studies with nonhuman primates havedemonstrated memory phenomena similar to those shown byhumans. Historically, human memory has been studied in thelaboratory by providing people with lists of items to remem-ber. When humans are provided with an ordered list of itemsto be remembered, they will show what psychologists termthe “serial position effect.” The nature of the serial positioneffect is that items early in the list and late in the list are re-membered better than those in the middle of the list. Mon-keys show this same effect with visual stimuli. The tests ofmonkey memory involve recognition memory while the typ-ical procedure with humans involves recall memory. How-ever, Lana, a chimpanzee who had had language symboltraining, was able to perform a recall memory task with a listof symbols by choosing the list items from her entire vocab-ulary of symbols. She, too, showed a serial position effect.The serial position effect is one of the most stable phenom-ena in memory research with humans. To find the same phe-nomenon in nonhuman primates suggests that memoryprocesses are similar across species notwithstanding the dif-ference in language ability.

A current area of investigation in nonhuman animals is thequestion of episodic memory. Memory can be categorized inmany different ways. The distinction between working and

reference memory was discussed previously. Reference mem-ory can also be divided into declarative (explicit, or conscious)and non-declarative (implicit, or unconscious) aspects. De-clarative memory is further subdivided into episodic and se-mantic memory. Semantic memory refers to memory forinformation, in other words, generic knowledge. Episodicmemory refers to memory for particular events or experiencesand implies that the memory involves revisiting that event orexperience. This aspect of episodic memory can be character-ized as the distinction between knowing something versus re-calling the specific event that provided the knowledge.Knowing that an incentive is located in a particular locationwithout remembering the experience of seeing it hidden il-lustrates the distinction between semantic memory (knowl-edge) and episodic memory (memory for the event). Panzee,a language-trained chimpanzee, uses language symbols to in-dicate to an uninformed human caretaker that a particular itemhas been hidden at some previous time (as long as 16 hoursbefore). Further, she will guide the human to the point wherethe item (that is outside of Panzee’s enclosure and hence un-available to her) is hidden. Panzee has shown the first attributeof episodic memory; the question is how to determine whether



After running a maze several times, a mouse takes less time to find thecheese. (Photo by © Don Mason/Corbis. Reproduced by permission.)

Chimpanzees (Pan troglodytes) are common subjects for memory andother research. Humans and chimpanzees have 98% of their genes incommon. (Photo by ©Renee Lynn/Corbis. Reproduced by permission.)

this memory involves more than simple knowledge that a par-ticular object is hidden outside the enclosure. That is, doesPanzee’s memory include “time traveling” back to the experi-ence of seeing the object being hidden? At the present time,the answer is unclear. However, the limitations on demon-strating episodic memory in nonhuman animals are likely tobe more those of procedure (how do we clearly demonstrateevidence for this capacity in nonverbal organisms?) than ca-pacity (do animals have episodic memory?).

NumberHow much do animals understand about number? Can

they count? Although many animals will choose the larger oftwo amounts of a desirable substance, can they determine thelarger of two quantities of objects? If so, what does that tellus about their understanding of number? The first animal re-ported to perform complex numerical tasks was Clever Hans,a horse that performed for audiences in Berlin during the early1900s. Hans was able to answer complicated questions, in-cluding arithmetic problems involving addition, subtraction,fractions, and other arithmetic manipulations that were rela-tively sophisticated. When a question was posed, Hans usedhis right front foot to tap out the answer, and he was quiteaccurate. A scientific panel investigated Hans’ numerical abil-ity. They found that Hans was most accurate when his ownerMr. von Osten was present, but that he could also solve prob-lems when Mr. von Osten was absent. This led them to theconclusion that Hans’ ability was not based on fraud or tricks.However, Oskar Pfungst, a student of one of the panel mem-bers, went further in an investigation of Hans’ numerical abil-ity. He noted that Hans’ accuracy depended on whether Mr.von Osten knew the answer to the question. When the an-swer was not known by the human questioner, Hans was in-accurate, usually tapping numbers higher than the correctanswer. He also noted that there were three other individu-als whose questioning of Hans was accompanied by high lev-els of accuracy in the horse.

With careful scrutiny of Mr. von Osten, Pfungst noted thatafter a question was posed to Hans, Mr. von Osten loweredhis head slightly and bent forward, maintaining this positionuntil the correct number was tapped, at which time he jerkedhis head upwards. The three other people for whom Hansperformed well showed similar behaviors. Pfungst performedexperiments in which Mr. von Osten (and the others) pro-vided these behavioral cues at appropriate times (consistentwith the correct answer) and at inappropriate times (consis-tent with a wrong answer). Hans’ performance showed thathe was responding to these cues. Pfungst suggested that Hanswas sensitive to subtle cues from Mr. von Osten, beginningto tap when Mr. von Osten bent his head and continuing totap until he detected a shift in Mr. von Osten’s body posture.Hans’ numerical ability was not based on an understandingof number, but rather on his reading of unintentionally pro-vided subtle behavioral cues from his human questioner. Theuse of discriminative cues to control his tapping ruled out ahigh-level cognitive explanation for Hans’ performance. Cur-rent studies of animal cognition include careful controls to

eliminate the possibility of a “Clever Hans” explanation forthe results obtained.

Determining what animals understand about number hasseveral levels. The simplest level of processing numerical in-formation is in making judgments of relative numerousness.Rats can learn to respond differentially to stimuli that vary innumber, responding with a particular response, for example,to the presentation of two light flashes or tone bursts and witha different response following the presentation of four lightsor tones. Rats also discriminate number of rewards and canlearn sequences of reward patterns.

Monkeys and apes make relative numerousness judgmentsshown by their choice of the larger of two quantities of food.Chimpanzees and orangutans can make such judgments evenwhen the two choices are themselves divided into two groupsof objects, suggesting some ability to combine quantities whenmaking the judgment. Discrimination is very accurate forquantities that differ widely from one another, such as five ver-sus two; the task becomes more difficult as the numbers getlarger and approach one another, such as five and six. If over-all mass is excluded as a possible solution by using items thatvary in size (such as grapes or different candies), then a number-related cognitive ability is implicated. Most explana-tions of animals’ success at such simple tasks include a non-counting mechanism known as subitizing, which refers to theability to make quick perceptually based judgments of num-ber. Subitizing is considered to be the likely way that most or-ganisms, including human children and adults, makejudgments about quantities of seven or fewer.

Understanding of ordinal relationships is a second level ofnumerical competence. Monkeys can order groups of itemspresented as abstract symbols on a video screen. They alsolearn to associate Arabic numerals with quantities up to nine(although this may not be the limit), and respond correctly tothe ordinal positions of the Arabic numerals. Apes go furtherin their use of Arabic numerals as symbols by using them todemonstrate counting.

Counting implies symbolic representation of a collectionof objects. The determination that an animal is counting in-cludes three major criteria, developed initially in studyingcounting in human children. The one-to-one principle re-quires that each item is enumerated or “tagged” individually.In the stable-order principle each tag occurs in the same or-der (e.g., one-two-three rather than two-one-three). In thecardinal principle the final number in the count refers to thetotal number of items. Additional features include that anyset of items can be counted, and that the order in which itemsare counted is arbitrary and irrelevant to determining the fi-nal count.

Chimpanzees have demonstrated all the criteria for count-ing. Several chimpanzees associate abstract symbols with spe-cific quantities and act upon the symbols as they would thequantities represented by the symbols. Sheba, a chimpanzeewho represents quantities with Arabic numerals, demon-strated tagging as she learned to assign Arabic numerals tocollections of objects. She also spontaneously added quanti-ties to report the sum of objects hidden across three locations.



She was able to add quantities regardless of whether objectsor numerals were presented. Ai, a chimpanzee who wastrained using a touch screen to respond to symbols, has shownclear understanding of ordinal positions of numerals, arrang-ing them in order even when there are numerals missing inthe list presented to her.

An interesting demonstration of the power of cognitive ab-straction with numbers was shown by chimpanzees Sheba,Sarah, Kermit, Darrell, and Bobby. The task was simple butnot straightforward. A chimpanzee was shown two quantitiesof a desirable food such as candies and was permitted tochoose one of the quantities by pointing to it. The quantitythat was chosen was given to another chimpanzee (or takenaway), and the quantity not chosen was provided to the chim-panzee who had made the choice. This procedure worksagainst the natural predisposition to choose the larger of twoquantities, and the chimps had a great deal of difficulty withthe task, even though it was clear from their behavior thatthey understood that they were not getting the quantity cho-sen. Even with much experience with the task, these chim-panzees were unable to inhibit choosing the larger quantity.When the objects presented were non-desirable objects suchas pebbles, they still could not inhibit the larger choice. How-ever, when the quantities were represented by Arabic nu-merals, the chimps, who were able to use Arabic numerals to

represent quantities, chose the smaller number and thus ob-tained the larger quantity. The animals were able to use therepresentation of the quantities to mediate their tendency tochoose the larger of two piles of objects.

This tendency to take the larger of two quantities is con-sistent with the chimpanzee’s ecology. Chimpanzees live in so-cial groups and compete with one another for desired foodobjects. The ability to judge quantities rapidly and to grab thelarger of two quantities would serve them in their natural en-vironment. The finding that orangutans Azy and Indah wereable to learn relatively rapidly to inhibit the choice of the largerquantity supports the suggestion that ecology plays a role inthis behavior. Orangutans are solitary in the wild and wouldhave little need for a food-getting strategy that requires quickchoice of larger quantities. Animals of both species can clearlydistinguish between different quantities of food, and both canlearn to inhibit the choice of the larger quantity when it is totheir advantage to do so. Orangutans are able to learn to in-hibit relatively quickly, but chimpanzees must rely on an ad-ditional, cognitive step in the procedure to be able to inhibittheir very strong tendency to choose the larger quantity.Species difference in cognitive abilities or in the way that cog-nition can mediate a response can tell much about how an an-imal is processing information and what kinds of cognitivejudgments serve the animal in its natural environment.



An orangutan (Pongo pygmaeus) uses a finger to get at ants in a tree hole. (Photo by Tim Davis/Photo Researchers, Inc. Reproduced by permis-sion.)

Tool use and constructionTools can be defined as detached objects that are used to

achieve a goal. Achievement of the goal can involve manipu-lation of some aspect of the environment, including anotherorganism. The making of tools involves modifying some ob-ject in the environment for use as a tool, but not all objectsused as tools by animals are constructed.

Instances of tool use and tool construction have been ob-served in great apes and monkeys living in captivity. Allspecies of great ape have been observed to make and use toolsin captivity. Some monkeys have been observed to use toolsand occasionally to construct tools in captivity. Observationsof tool use and construction by nonhuman primates in thewild have been less widespread. This difference betweendemonstrations of tool use in captivity and the natural envi-ronment may exist because, for the most part, evolutionaryadaptations of the animal may sufficiently address challengesin the natural environment. However, environmental contin-gencies in captivity may be unique in encouraging tool use.In studies of tool use, researchers set up problems that arebest solved using tools. In captive environments, experiencewith such problems coupled with extensive experience withtool-like objects provide the environmental and cognitivescaffolding that facilitate the demonstration of tool use by an-imals who may not so readily demonstrate such capacities intheir natural environment.

However, instances of tool use and construction have beenobserved in great apes in the wild, particularly in the chim-panzee. The most widely known of these is the chimpanzee’suse of twigs to “fish” for termites in termite mounds at theGombe Stream Reserve (now Gombe National Park) in Tan-zania, East Africa. Following the report of that first observa-tion by Jane Goodall in 1968, many instances of tool use andtool construction have been discovered in chimpanzees andother animals in their natural environment. For termite fish-ing, the choice of an appropriate branch, twig, or grass bladeinvolves judgments of length, diameter, strength, and flexi-bility of the tool. Any leaves remaining on a branch are re-moved, and the tool is dipped into holes in the termite mound.Termites attack the intruding stick, attaching themselves toit, and the chimpanzee withdraws a termite-laden stick andproceeds to eat the termites.

Additional observations of tool use include the use of leavesthat have been chewed to serve as a sponge to obtain waterfrom tree hollows, the use of tree branches in agonistic dis-plays, various uses of sticks, leaves, or branches to obtain oth-erwise inaccessible food, and the use of leaves to removeforeign substances from the body. Orangutans in the wild havebeen observed to use leaves as sponges and as containers forfoods. They use tools to aid in opening large strong-huskedfruits and to protect them from spines on the outside of fruits.

An interesting complicated instance of tool use is the useof rocks as hammer and anvil to crack open nuts reported forchimpanzees in West Africa. Coula nuts or palm-oil nuts withhard shells are placed on a hard surface and cracked open byhitting them with a hand-held rock. The supporting surface(or anvil) can be a tree root or a rock obtained from the for-

est floor by the chimpanzee. Rocks used as hammers have asize and shape that fit the chimpanzee’s hand, and rocks cho-sen as anvils have a flat surface. The nut is placed on the flatsurface of the anvil and pounded with the hand-held hammerrock. If an anvil has an uneven base that causes it to wobblewhen the nut is struck, the chimpanzee finds a smaller rockto use as a wedge under the smaller end of the anvil to bal-ance it.

Infant chimpanzees learn tool use as they observe theirmothers make and use tools. Observations of mother chim-panzees engaged in explicit teaching of tool use to their in-fants have been reported at only one site, and on only twooccasions. On one occasion, a mother took a hammer rockfrom her daughter who was holding it in an orientation thatwas not conducive to nut cracking, and slowly rotated the ori-entation of the rock to a position that was useful. After themother finished cracking nuts, her daughter used the rock inthe same orientation as her mother had used it. On the sec-ond occasion, a mother re-positioned a nut that her son hadplaced on an anvil in a position that would not have permit-ted its being opened. The son then used a hammer rock toopen the nut. Both of these observations are provocative, butin the absence of other such observations it is not clear thatthe mother’s intent was to teach the infant. Indeed, mostlearning of tool use and tool construction by young chim-panzees appears to be from observation of the mother’s be-havior and manipulation of objects used as tools in the contextin which they are used.

Culture in nonhuman primates?In 1953 a young Japanese monkey named Imo did some-

thing remarkable. Her troop lived on Koshima Island inJapan, and was provisioned by Japanese researchers who stud-ied them. Provisioning involves providing additional food tosustain the population in areas of limited resources or to en-courage animals to remain in a particular locale for observa-tion. Imo’s group was provided with sweet potatoes placed onthe sand at the edge of the water. Imo began to use the nearbywater to wash sand from the sweet potatoes. This behaviorspread through the group, with younger animals adopting itfirst and some older animals never adopting it. Four yearslater, Imo introduced another novel behavior. The monkeyswere provided with grains of wheat scattered on the sand thatwere difficult to eat because they mixed with the sand. Imoplaced handfuls of this mixture of wheat grains and sand intostanding pools of water. The wheat grain floated to the topand could be scooped up and eaten, free of sand. Years andgenerations later the monkeys of Koshima Island continue towash sweet potatoes and to place sandy wheat grains in wa-ter. The spread of these novel behaviors through individualsin the group appeared to be an instance of social transmis-sion of a novel behavior. This interpretation began a discus-sion of culture in nonhuman primate groups.

Recent analyses of behaviors shown by communities ofchimpanzees and of orangutans suggest the presence of cul-tural variations across groups within each species living in dif-ferent geographical areas. Behaviors that varied includedinstances of tool use, social behaviors related to grooming or



communicative signals, and food-related behaviors. For ex-ample, some chimpanzee communities crack nuts with ham-mer and anvil tools, but others do not, despite the availabilityin their environment of hard-shelled nuts and objects thatcould serve as tools for nutcracking. The absence of a be-havior pattern in the presence of all necessary components(e.g., nuts and potential tools) rules out ecological factors toexplain these differences. Similarly, genetic factors do not playa role in the variability of such behavior patterns. That is, asimilar pattern of tool use may be shown by two groups whoare genetically isolated from one another, or it may be pre-sent in one community but missing in another community ofthe same genetic background. Some form of social learningis thought to have promoted the spread and maintenance ofthese specific behavior patterns within certain communities.

Even in a species that is not typically group living, culturaldifferences are found across geographical areas. Orangutansobserved in Sumatra use tools constructed from sticks to prythe seeds from Neesia fruits, a fruit with a very tough huskthat also has spiny hairs protecting the seeds. Bornean orang-utans do not use tools to acquire the seeds; rather, they teara piece of the husk open to expose seeds. Only adult malescan perform this latter method because of the strength re-quired to force open the fruit. Otherwise, females and juve-niles must wait until the husk opens and older, less desirable

seeds are naturally available. Geographic isolation leading toa genetic basis for these differences in technique is not a suf-ficient explanation. At a second Sumatran site orangutans donot use tools, ruling out the genetic explanation. Neesia isavailable to and eaten by orangutans in both Sumatra and Bor-neo, eliminating an ecological explanation. Social transmis-sion through social learning is the most likely explanation forthis phenomenon, through mother-offspring transmissionand/or through social encounters among animals inhabitingthe same area.

Social learning can occur at several levels, from simple tocomplex, all based on observation of one animal by another.Most simple is social facilitation in which one animal’s inter-est in an object elicits interest in that object from another an-imal. By drawing another’s interest to an object that the otherthen explores, the first animal has influenced the behavior ofthe second but has not explicitly transferred information. Inobservational learning, the observer learns something specificabout stimuli and responses from watching another animal.Imitation is the most cognitively complex form of social learn-ing and involves the observer copying the form and intent ofa novel behavior demonstrated by another animal. Imitationis distinguished from a similar form of social learning termedemulation, in which an animal performs actions similar to an-other, with the same intent, but without mimicking the spe-



A sea otter (Enhydra lutris) uses a rock to open a clam shell. (Photo by Jeff Foott. Bruce Coleman, Inc. Reproduced by permission.)

cific actions of the model. Great apes do show imitation butthat capacity may be limited to great apes.

Whether the transmission of cultural variations within agroup is based on imitation or some simpler form of sociallearning remains unresolved. However, ongoing investiga-tions of nonhuman primate behavior in the laboratory andin the wild will provide better understanding about the ori-gin and transmission of novel behaviors through socialgroups.

Self recognition and theory of mindMirrors provide a novel and rich source of information

about social cognition in animals. The behavior of an animaltoward its mirror image suggests much about the animal’s un-derstanding of the source of that image. Many animals suchas cats and dogs, when first encountering their own mirrorimage, behave as though they have encountered a stranger oftheir own species. They may show aggressive behavior suchas threats, or they may attempt to play and to reach aroundthe mirror as though attempting to find the other animal.With time, the dog or cat will ignore the mirror image andno longer attempt to engage the reflection in social interac-tion. For the most part, monkeys behave in a similar way totheir mirror image.

Great apes, however, appear to come to understand thenature of the mirror image. That is, with experience, they be-have as though they understand that it is their own body thatis reflected in the mirror. The phenomenon is referred to asmirror self-recognition (MSR) and has been of interest to re-searchers in primate cognition for decades. Chimpanzees werethe first nonhuman species to show evidence of MSR. Whenprovided with daily exposure to a mirror outside their enclo-sure, individual chimpanzees initially responded to the mir-ror image with social behaviors suggesting that the mirrorimage was perceived of as an unfamiliar chimpanzee. Threatbehaviors such as head bobbing, charging the mirror, and vo-calizing were common. After some time, however, the socialbehaviors waned and the chimpanzees began to direct be-havior toward their own bodies while looking into the mir-ror. They groomed and investigated parts of their bodies, suchas the face, that were invisible to them without the use of themirror. Using the mirror to guide their hands, these animalsgroomed their eyes, picked their teeth, inspected their geni-tal areas, and also made faces while watching in the mirror.

The behaviors directed to their own bodies, termed self-directed behaviors, appeared to indicate that the animals rec-ognized themselves in the mirror. To test this interpretation,the chimpanzees were anesthetized and an odorless red markwas placed on one eyebrow and one ear, in a location wherethe chimpanzee could not see the mark without the use of themirror. When the animals awoke from the anesthesia theywere presented with the mirror, and all four animals touchedthe mark on their brow, using the mirror to guide their fin-gers to the mark. The importance of this response, directingtheir hand to the mark on their own body rather than to themark on the mirror image, suggests that the animals indeedrecognized themselves in the mirror.

Since the initial report in 1970 of this phenomenon inchimpanzees, individuals from the other great ape specieshave shown MSR by demonstrating self-directed behavior orby passing the mark test, but not all individuals of these speciesshow the capacity. There are clear individual differences basedpartly on age. Like humans, chimpanzees develop the abilityto show mirror self-recognition. Beginning at about 24–30months of age young chimpanzees will touch a mark on theirbrow using the mirror to guide the touch and the ability isgenerally quite evident by the age of four. Human childrenstudied under controlled conditions do not show the capac-ity for mirror self-recognition until about 15 months of ageat the earliest, with most achieving this developmental mile-stone by 24 months.

There is some evidence that dolphins are capable of mir-ror self-recognition, and gibbons also may have this capacity.However, other animals have not clearly shown evidence ofmirror self-recognition. It may be a species difference, or itmay be the case that with additional research the apparentdiscontinuity will be resolved. The implications for evolu-tionary development of self in humans are apparent, althoughinterpretations of this phenomenon are disputed. At the mostextreme, a rich interpretation of self-recognition in animalssuggests an understanding of the self as an entity, perhapssimilar to humans’ sense of self or self-concept. However, theability to understand the nature of a mirror image and to di-rect behavior back to one’s own body does not necessarily im-ply such a rich interpretation. The distribution of this capacityand its interpretation are open questions subject to ongoingempirical investigation and theoretical debate.

The ability to recognize oneself may be related to the abil-ity to understand another individual’s knowledge state, whichrepresents a more complex cognitive ability. This phenome-non is called “Theory of Mind” and refers to an individual’sability to understand the perspective or the “state of mind”of another. It forms the basis for such complex social strate-gies as intentional deception. In order to deceive another byproviding incorrect information, the actor must know some-thing about the other’s perspective and expectations and whatinformation to provide (or withhold) as deception. Many in-stances of deception have been reported from observations ofapes and monkeys in the field and in the laboratory, and theextent to which these deceptive incidents are based on theperspective-taking capacity implied in Theory of Mind is stillan open question. It is clear that animals behave in ways thatsuggest that they are taking into account the knowledge stateof others. Whether they are or not is still an active area ofresearch in animal cognition.

The initial description of Theory of Mind was based onthe ability of Sarah, a language-trained chimpanzee, to solveproblems for a human who was in some state of distress. Sarahwas experienced in many features of human life. For exam-ple, she had often observed her human caretakers using keysto unlock padlocks. She had often observed humans turninga faucet to provide water through a hose. She had observedhumans plugging a cord for an electric heater into an elec-trical outlet. Sarah was provided with videotaped instances ofhumans in situations whose solutions were related to the



above events as well as others. For example, she saw video-tape in which one of her human caretakers was apparentlylocked in a cage and could not escape despite attempts to openthe locked door. The videotape was stopped before the prob-lem was solved, and Sarah was provided with photographs,one of which had the solution to the problem (in this case, akey for the padlock on the cage door). Sarah consistentlychose the photograph with the appropriate solution to eachproblem. The interpretation of Sarah’s behavior was that shewas able to understand the state of the human in the video-tape and she was able to choose the appropriate solution tothe person’s problem. Additional studies with Sarah suggestedshe could spontaneously show deception, withholding infor-mation or providing incorrect information about the locationof a food item from a human who had previously failed toshare food with her. In contrast, she provided informationabout the location of a food object to another human who al-ways shared food with her.

Additional studies with Sarah and other chimpanzees pro-vided results suggestive that chimpanzees can take the per-spective of another and use it to solve problems. A numberof studies have been unsuccessful at providing evidence ofTheory of Mind; some that have been successful have beencriticized on methodological grounds. However, such studiescontinue. The demonstration of this capacity in apes awaits aclear methodology that will adequately address the extent towhich apes can project their understanding of states of mindto others.

Social cognitionTheory of Mind is a form of social cognition, or the abil-

ity to process cognitive information presented by social part-ners. In group-living animals species-specific social rulesguide behavior. Understanding these rules and applying themappropriately is a complicated process for individuals in thegroup. Recognition of familiar versus unfamiliar conspecifics,of particular age and sex classes, and of particular individualsare necessary skills for each member of the group. Even an-imals that spend much of their time in solitude must recog-nize social features of other conspecifics, including individualswho may be living in the same area. Social cognition involvesnot only these forms of recognition, but also understandingof species-typical social communicative signals.

In many animal species, members of the group respondquickly to alarm calls from a group member. In some cases,such response may not require much processing of informa-tion and so may be based on simple associative mechanisms.In other cases, processing of alarm calls may provide somecognitive challenge. For example, vervet monkeys (Chlorocebusaethiops) in Africa have three types of alarm calls, elicited bythree different predators. Each alarm call is followed by a par-ticular behavior by members of the group. Following a “snake”alarm call the group members stand bipedally and visuallysearch the grass around them, presumably to locate largepythons or poisonous snakes on the ground. Looking into theair and moving to the cover of bushes follow an “eagle” alarmcall. A “leopard” alarm call sends group members to trees withbranches that are too fragile to support the weight of a leop-

ard. These calls are made selectively and appropriately by adultmembers of the group, and receive selective and appropriateresponses by group members. Infants learn the appropriatecalls, sometimes making errors as they develop, for example,producing an eagle call to the sight of a harmless bird. It ap-pears that production of the calls involves some learning, andit may be that appropriate response to the calls also is learnedthrough observation of group members. These alarm calls aredeemed cognitive rather than reflexive because production ofeach type of call is voluntary and the calls are referential. Thatis, each type of predator call refers to only one type of preda-tor. The calls elicit different responses specific to each type ofcall, and production and response to each class of call show adevelopmental course.

Visual social signals provide information in social interac-tions. The simplest signals are threat or appeasement gestures.Visual social signals that guide another animal’s attention toan object or event require more complex cognitive skills. Forexample, monkeys and apes will join another animal to in-vestigate jointly an object of interest. Referential pointing andreferential gazing are social signals that call attention to anobject or event removed from the actor. Chimpanzees andorangutans can interpret pointing in humans. They also pointand vocalize to draw a human’s attention to a distant objector event. However, these apes do not typically use pointingto communicate with one another and their use and inter-pretation of pointing varies with the amount of human con-tact they have had.

Although dogs do not seem to respond appropriately topointing (the usual response by the dog is to sniff the fingerof the individual pointing), they do respond to gaze directionin humans and have been shown to use gaze as a cue for thelocation of hidden food. Similarly, chimpanzees and monkeysare able to use gaze as a cue, and monkeys will follow the di-rection of gaze of a conspecific, even one presented on video-tape. Chimpanzees and orangutans use humans’ gazedirection to locate hidden food, and as in pointing, those an-imals who have had extensive contact with humans are morelikely to use and are more adept with gaze cues than are thosewith less human contact.

LanguageOne of the major distinctions between human and non-

human animals is language. At the beginning of the animallanguage projects, the object was to show that an individualfrom a nonhuman species could acquire and use language.Apes have been the primary participants in these projects. Oneof the first attempts to teach language to an ape was that ofKeith and Cathy Hayes, who reared Viki the chimpanzee intheir home from 1947 to 1954. With much effort, Viki learnedto say four words, “mama, papa, cup, and up.” She had greatdifficulty producing these words, and they were barely intel-ligible. We now know that great apes lack vocal structuresnecessary to produce speech. However, they appear to havethe cognitive ability to acquire aspects of language using sym-bols in communicative interactions with humans.



Washoe, a chimpanzee reared by Beatrice and Allen Gard-ner beginning in 1966, was taught American Sign Language(ASL). Washoe’s acquisition and use of ASL were interpretedto demonstrate that a great ape could acquire a human lan-guage. The strong version of this interpretation was ques-tioned from two perspectives. First, H. S. Terrace, who in thelate 1970s trained a chimpanzee named Nim Chimpsky tolearn ASL, questioned the referential nature of a chimpanzee’suse of ASL. Terrace suggested that the primary basis forNim’s “linguistic” ability was not linguistic or referential inthe way that human language is used to refer to objects, con-cepts, and experiences, but was more likely based on associa-tive learning and imitation in goal-oriented situations. Thatis, Nim appeared to reply to questions posed by his teachersin a manner that was more imitative of the teacher’s gesturesthan suggestive that he was generating linguistic utterancesof his own that referred to objects, concepts, and experiencesin his environment.

A second related question addressed syntax, or grammar.Chimpanzees who learned ASL (and there were more thanWashoe and Nim involved in such studies) did not followstrict grammatical rules of word order required in human lin-guistic utterances, whether spoken or signed. Rather, thechimpanzees would repeat words or phrases, often varying theorder of words as the utterances were repeated. Such behav-ior was consistent with Terrace’s suggestion that the chim-panzees were not using signs to communicate. Beginning in1973, Duane Rumbaugh trained a chimpanzee named Lanato produce sentences through the use of a computer-operatedkeyboard containing abstract symbols that represented verbs,nouns, adjectives, and adverbs. These symbols, called lexi-grams, were composed of abstract geometric shapes combinedto form unique configurations, each of which referred to aparticular word or concept. Rumbaugh developed a languagehe called “Yerkish” named for the Yerkes Regional PrimateResearch Center where the Lana project began. Lana’s sym-bols followed rules of grammar and the results of this projectshowed that Lana and other chimpanzees in the project couldlearn rules of syntax and use abstract visual symbols in a com-municative manner. Chimpanzees Sherman and Austin latershowed the ability to use this computer-based system to com-municate information to each other.

Although for some investigators of animal cognition thequestion of ape language is still at issue, the ape language pro-jects have expanded in content and have provided importantdiscoveries about ape cognitive abilities. In such a project,Chantek, an orangutan reared by Lynn Miles beginning in1977, learned ASL. In this project Chantek’s acquisition ofsymbolic communication was studied in the context of over-all cognitive development. This project is unique in itsbreadth, providing understanding of the development of sym-bolic communication as one feature of a suite of cognitiveabilities.

In 1971, David Premack first reported results of a projectin which he trained chimpanzee Sarah to communicate usingarbitrary abstract symbols. These symbols were colored plas-tic shapes. Sarah learned concepts such as “same” and “dif-ferent,” as well as nouns, verbs, and adjectives. That these

symbols were representational to Sarah was demonstratedwhen she was provided with the symbol for apple, and askedto describe its physical features. Although the symbol for ap-ple was a blue triangle, Sarah described the object presentedto her as “red” and “round,” referring to attributes of the ob-ject rather than of the symbol. She also showed the ability toreason analogically through her understanding of “same” and“different.” The primary contribution of this language pro-ject was not Sarah’s linguistic abilities, but how Premack usedSarah’s representational capacity to show the breadth of cog-nitive flexibility and conceptual understanding available to achimpanzee provided with Sarah’s rich cognitive environ-ment.

In a similar fashion, two current ape language projects usethe animals’ symbolic ability to uncover cognitive represen-tational abilities that would be difficult to access without thismeans of symbolic communication. In 1995 Robert Shumakerbegan to work with orangutans Azy and Indah, who are learn-ing an abstract symbolic communication system presented aslexigrams on a touch-sensitive video screen. When questions



Bottlenosed dolphins (Tursiops truncatus) have a complex languagethat may eventually help humans to communicate with them. (Photoby © Stuart Westmorland/Corbis. Reproduced by permission.)

are posed, the orangutans indicate the appropriate symbolfrom an array of symbols by touching it. Shumaker is usingthe animals’ symbolic abilities as a window into other relatedcognitive processes such as number comprehension. In a pro-ject begun in 1978 by Kiyoko Murofushi, Toshio Asano, andTetsuro Matsuzawa, chimpanzee Ai continues to demonstrateher sophisticated cognitive abilities using a touch-sensitivevideo screen and a vocabulary of lexigrams and Arabic nu-merals. For example, Ai labels objects and their characteris-tics such as color and number; she clearly understandsnumbers conceptually, and counts using Arabic numeralsfrom zero to nine; and she “spells” by constructing lexigramsfrom their components. Ai’s infant Ayumu, born in 2000, islearning to use the touch-screen system, providing insightinto the development of symbolic cognitive skills as he inter-acts with his mother and observes her using the system.

The symbolic ability of great apes in the context of a lan-guage-learning setting was most strongly demonstrated by SueSavage-Rumbaugh who in 1979 extended the Lana project toanother great ape species, the bonobo (Pan paniscus). Kanzi, ayoung bonobo who lived with his mother during her trainingwith Rumbaugh’s computer-based language, surprised re-searchers when he showed clear understanding of the task andof particular symbols simply as a result of having been pas-sively exposed to the symbols while his mother was learningthe task. Following this discovery, Savage-Rumbaugh focusedon Kanzi’s ability and motivation to use abstract communica-tive symbols. Kanzi not only uses the abstract symbolic lan-guage system, he also has a demonstrated understanding ofspoken language, and Savage-Rumbaugh has reported that heappears to attempt to communicate vocally by imitatingacoustic properties of human speech. Her interpretation ofKanzi’s behavior is that bonobos appear to have not only theability to acquire abstract human-derived symbols, but thatthey may have additional communicative skills that can pro-vide insight into the evolution of human language.

Koko the gorilla has been using ASL under the tutelage ofFrancine Patterson since 1976. She is probably the most pub-licly recognizable language-trained ape. Indeed, Patterson hasextended her project into conservation efforts in the UnitedStates by promoting Koko to the public. Further, Pattersontranslated a children’s book about Koko into French to dis-tribute in French-speaking Africa as a way to educate chil-dren about the cognitive and emotional capacities of gorillasand the importance of preserving them in the wild.

The importance of the ape language projects has not beenin the demonstration of a human capacity in great apes, butrather in exposing the complex symbolic skills available to an-imals in a rich interactive environment. The cognitive skills

shown by the nonhuman participants in these projects extendbeyond the specific symbolic skills trained in individual pro-jects. They have opened a window into the minds of animalsthat enriches our understanding of the animal mind, whilealso providing new theoretical perspectives on the evolutionof human cognition and language.

Enculturation of apesMuch of the information we have about cognition in great

apes has come from research projects involving intensive studyof one or two apes, usually chimpanzees. In most of these re-search projects the apes have had extensive interaction withhumans during their early development. These interactionsnot only take the form of explicit cognitive and behavioraltests, but they also include teaching and guidance. The apesacquire sophistication with human artifacts including com-puters and other electronic or mechanical objects.

The environment for these animals is complex, and nottypical of the environment in which apes evolved. Althoughsome of the ecological challenges met by animals living in thenatural environment are missing, the early experience of theseanimals is enriched and challenged in different ways. Apeswho experience this intensive experience with humans arecalled “enculturated” apes, those who at some level have beenexposed to and integrated into certain human social/culturalexperiences. Because they have not been exposed to their nat-ural environment, some researchers question the value of theconclusions based on their cognitive abilities. Clearly, theseanimals have had enriched early experiences, including directteaching of skills by human caretakers, and are not represen-tative of chimpanzees developing with their mothers in thewild environment. This challenge has been met by the re-sponse that although the cognitive tasks provided to encul-turated animals differ from those in the natural environment,they challenge the cognitive skills required for survival in thewild.

Further, the possible enhancement of cognitive skills pro-vided by the enriched environment shows the extents and lim-its of cognitive abilities under circumstances conducive to highlevels of performance. The results of these studies tell us whatcognitive skills great apes are capable of; the extensive behav-ioral studies of great apes in their natural environment showus how they use these cognitive abilities to solve daily socialand environmental challenges. Although an enculturated apehas had a different early environment, he or she continues tobe an ape and to show cognitive skills available to an ape. In-tegration of data from field and laboratory continues to pro-vide the richest understanding of great ape cognition.



ResourcesBooksBekoff, M., C. Allen, and G. M. Burghardt, eds. The Cognitive

Animal. Cambridge, MA: MIT Press, 2002.

Candland, D. K. Feral Children and Clever Animals. New York:Oxford University Press, 1993.

Hauser, M. D. Wild Minds. New York: Henry Holt andCompany, 2000.

Matsuzawa, T., ed. Primate Origins of Human Cognition andBehavior. Tokyo: Springer-Verlag, 2001.

Mitchell, R. W., N. S. Thompson, and H. L. Miles, eds.Anthropomorphism, Anecdotes and Animals. Albany, NY: StateUniversity of New York Press, 1997.

Parker, S. T., and M. L. McKinney. Origins of Intelligence.Baltimore: The Johns Hopkins University Press, 1999.

Parker, S. T., R. W. Mitchell, and H. L. Miles, eds. TheMentalities of Gorillas and Orangutans in ComparativePerspective. Cambridge, UK: Cambridge University Press,1999.

Pearce, J. M. Animal Learning and Cognition. 2nd ed. Hove,UK: Psychology Press, 1997.

Premack, D., and A. J. Premack. Original Intelligence: TheArchitecture of the Human Mind. New York: McGraw-Hill/Contemporary Books, 2002.

Roberts, W. A. Principles of Animal Cognition. New York:McGraw-Hill, 1998.

Shettleworth, S. J. Cognition, Evolution, and Behavior. NewYork: Oxford University Press, 1998.

Tomasello, M., and J. Call. Primate Cognition. New York:Oxford University Press, 1997.

Wynne, C. D. L. Animal Cognition. Basingstoke, UK: Palgrave,2001.

Karyl B. Swartz, PhD



Migrations are mass movements from an unfavorable toa favorable locality and in plains-dwelling, large herbivoressuch as reindeer, bison, zebras, wildebeest, or elk they canbe quite spectacular. In large sea mammals migrations areno less important, but to us are merely less visible and ithas taken much effort by science to document at least a partof their extent, leaving much that is still shrouded in mys-tery. Mass-migrations occur when individuals flood to dis-tant birthing or breeding grounds, to seasonal food sources,or to escape winter storms. Close associations of large num-bers of individuals during migration is merely a securitymeasure, capturing the great advantages of the “selfishherd” against predation. Long distance movements are alsoundertaken by individuals or by small groups, particularlyin the oceans.

Migrations take their origin in minor seasonal movementsbetween habitats, such as the movements by mountain-

dwelling deer, elk, or moose between winter ranges at lowelevations and summer ranges at high elevations. By movingto lower elevations in fall the deer avoid the high snow lev-els that develop on their summer ranges at high elevation inlate fall and winter. High snow levels hamper movements, attimes severely. Also, at high elevations plants, and thereforefood density per unit, are low. When high snow levels ham-per mobility as well as increase the cost of locomotion, feed-ing in areas with low food density is uneconomical andindividuals move to where there is more food, preferably suchthat can be acquired with little cost. Movement to lower el-


• • • • •

Migration

A pod of spotted dolphins (Stenella attenuata) migrating. (Photo by ©William Boyce/Corbis. Reproduced by permission.)

Aerial view of migrating wildebeest (Connochaetes). (Photo by © YannArthus-Betrand/Corbis. Reproduced by permission.)

evations is the answer because forage density is higher andthe cost of locomotion between mouthfuls of vegetation ismuch less. There is a high cost to scraping away snow fromthe forage it covers, and snow removal is easier and needs tobe done less often at low elevations, at localities often out-side the mountains. A fourth factor is the shelter providedby trees and forests in winter, which are more likely to growin valleys than on high slopes and mountain tops. Neverthe-less, there is no rule without its exceptions! In the high moun-tains of western Canada and Alaska, once the snow hardensin late winter and its crust can support the weight of herbi-vores, mountain caribou and black-tailed deer may ascendthe mountains and feed in the sub-alpine coniferous forestson the now accessible tree lichens. Mountain sheep andmountain goats may also ascend in order to feed on highalpine ridges where the powerful winds have blown away thesnow, exposing the short, scattered, but highly nutritiousgrasses, sedges, and dwarf shrubs. Here the packed snow al-lows them to roam far and wide, be it in search of forage orto escape the occasional visit by wolves or wolverines. Also,some bull elk and bull moose may opt to stay, usually widelydispersed, at high elevation in very deep, loose snow alongcreeks because wolves are very unlikely to reach or harmthem under such snow conditions. When hard “sun crusts”develop on the snow in late winter, however, the tables maybe turned temporarily. Wolf packs can then travel freely on


MigrationVol. 12: Mammals I

Migrating killer whales (Orcinus orca) in San Juan Islands. (Photo by © Stuart Westmorland/Corbis. Reproduced by permission.)

Caribou (Rangifer tarandus) migrating in the snow. (Photo by © Ken-nan Ward/Corbis. Reproduced by permission.)

the crusted snow surfaces during the night. During the day“sun crusts” may soften, trapping all travelers temporarily indeep snow.

Elevation draws herbivores into seasonal movement andchange of venue by the fact that vegetation sprouts in spring

at low elevation and that this sprouting creeps upward asspring progresses. Herbivores follow this line of sproutingvegetation because sprouting vegetation it is the most nutritious and most easily digested forage there is. Conse-quently, there are movements by all sort of large herbivoresfrom the valley to the mountain tops in spring and summer.Less dramatic, but equally important are the movements ofherbivores in response to flooding in river valleys and thewithdrawal of the flood because the areas just flooded havebeen fertilized with silt, and rich plant growth follows thewithdrawal of water.

Migrations can become more complex if special nutritionalneeds must be met, or if social factors intervene into the move-ment pattern. American mountain sheep illustrate this well,because interspersed into the long seasonal movements be-tween summer and winter ranges are extended visits to min-eral licks in spring, to separate socializing areas of males infall and again in spring where they meet and interact socially,and to special birthing and child-rearing areas for femalesheep. These localities of increased social interaction have apowerful pull on the males, just as the lambing and lamb-rearing areas have as strong pull on females. Consequently,males and females move and live separately for all of the yearexcept for about a month during the mating season. Matingoccurs on the core wintering areas of females, which the adultmales leave right after mating, possibly so as not to competefor the limited food supply available to the mothers of theirprospective offspring. Thus the males move to separate win-tering areas of their own. The distances between sea-


Vol. 12: Mammals IMigration

Wildebeest (Connochaetes taurinus) massed at river’s edge during migration, in Kenya, Africa. (Photo by Tom Brakefield. Bruce Coleman, Inc. Re-produced by permission.)

A group of migrating polar bears (Ursus maritimus) in Churchhill, Man-itoba, Canada. (Photo by © Larry Williams/Corbis. Reproduced by permission.)

sonal ranges for mountain sheep may be tens of miles (kilo-meters) apart.

Megaherbivores such as elephants, rhinos, and giraffes maymove over huge annual home ranges between small dry sea-son ranges close to water and large wet season ranges. Thesize of these ranges may be hundreds of square miles (kilo-meters). Areas within are used opportunistically depending onforage and water availability. The ability to move rapidly overlong distances, coupled with excellent memory of locations,allows elephants to live in vast desert areas. While the wetseason areas are large, travel may be restricted at that time bythe abundance of food. Movement may be more extensive inthe dry seasons due to decreased forage density.

Food availability also dictates mass movements of Africanplains animals such as zebras, wildebeest, and gazelles in theSerengeti plains. The great productivity of the plains duringthe wet season attracts them, and they leave the woodlandsthey use during the dry season. Zebras, wildebeest, andgazelles form a grazing succession in which the zebras firstremove the coarse grasses. The re-growth of grasses then cre-ates good foraging conditions for wildebeest, which in turngraze down the grass exposing dicotyledonous plants that at-tract gazelles. The variations in timing of the rainy seasons

thus affect the mass-movements of these herbivores to andfrom the woodlands.

Migrations are most spectacular when masses of animalsunite in closely coordinated movements. As indicated earlier,the proximity of individuals to one another and the coordina-tion that keeps them together arise as an anti-predator adapta-tion in species adapted to open landscapes—be they coverlessterrestrial terrain or open oceans. In cover there is little possi-bility of group cohesion, but great opportunity for individualhiding and thus escape from predators. In the open, uniting intolarge formations has powerful advantages for prey. Joining withothers of one’s kind is a purely selfish act aimed at self-preser-vation. Consequently, this grouping has been labeled “the self-ish herd.” It is very common. To begin with, close herdingempties the landscape of the species, forcing resident predatorson alternate prey—except where the species is bunched. Herethe chances of any individual being taken by a predator dependon the number of others of its kind it is with. In a larger herdthe chances of being attacked are smaller than in a small herd.This is called the dilution effect. Thirdly, the individuals in thecenter of the herd are shielded from predator attacks by indi-viduals on the periphery. This is the position effect. Fourthly,when a herd flees there is for each individual a greater chancein a large herd than in a small herd that someone is a slower



Zebras tend to be the first species to migrate to a new area due to their toleration of tall grass. (Photo by Mitch Reardon/Photo Researchers,Inc. Reproduced by permission.)

runner. Selfish herds are thus dangerous places for slow run-ners, be they ill or merely heavily pregnant. However, for ahealthy individual of average abilities, joining with others andstaying close together is an excellent way to minimize the riskof being caught by predators. As a consequence, uniting intohuge herds is a possibility in large expanses of open landscape.

However, the very gathering into a huge mass raises severeproblems in food acquisition. A large mass of herbivores willquickly deplete the available forage and must move on. Thatis, huge herds must move just to stay fed and it matters littlewhere they go as long as they stay with food. This leads, ofcourse, to unpredictable movements, which incidentally re-duces predation risk still further as it does not permit preda-tors to anticipate the direction or time of movements. Thisrandom movement, excepting predictable occupation of grass-lands freed of snow in winter by warm katapatic winds alongmountain fronts, or of grasslands recovering from large wild-fires, was suggested to be the model of bison migration in NorthAmerica up to the late nineteenth century. That is, food avail-ability governed the mass-movements of the bison herds overthe huge expanse of prairie in the center of the continent.

The mass migrations of reindeer in Eurasia and barrenground or Labrador caribou in North America have as theirprimary focus the calving ranges in spring. Pregnant females

lead this migration, which is closely focused in both space andtime. This is the most predictable migration and it leads to bar-ren, snowed-over areas with a minimum of predators. Theselarge, dense herds also reduce predation by “swamping” exist-ing predators with a great surplus of calves on the calvinggrounds. Reindeer bulls lag behind in the migration. From thecalving grounds the herds move predictably to summer rangeswith high productivity and some protection from insects, whichin large numbers can debilitate caribou. Males and females mixon the summer ranges. From the summer feeding grounds theherds drift towards the wintering areas below the timberline.They mate during a short rutting season while traveling to thewinter ranges. Caribou can travel with remarkable speed andshift location within any seasonal range. Nevertheless, theirmovements are predictable as they follow the same landscapefeatures including favorite locations above waterfalls and rapidson large rivers. These and large lakes are no serious barrier tocaribou, which are excellent swimmers. Caribou may travel over3,100 mi (5,000 km) in their annual migrations.

A feature common to migratory terrestrial or marinespecies is that they become very fat on their summer feedinggrounds and then depart with a fat-load to subsidize theirmaintenance and reproductive activities elsewhere. Fattening—which is metabolically a very expensive process since for



An aerial view of migrating caribou (Rangifer tarandus). (Photo by Ted Kerasote/Photo Researchers, Inc. Reproduced by permission.)

every unit of fat stored, as much as another unit is lost asmetabolic heat—evolved in response to both seasonality ofclimates and high diversity of habitats within any one season.Extremes in seasonality as well as in terrestrial and marinehabitats developed during the major glaciations of the IceAges during the Pleistocene.

Some extreme examples of fattening and long distance mi-grations were evolved by baleen whales. For instance, in theshort Antarctic summer such whales congregate about theAntarctic pack ice encircling the Antarctic continent, particu-larly in regions where the cold waters rich in dissolved oxygenand carbon dioxide are fertilized by mineral-rich, warm deep-current upwellings to produce explosive plankton growth.Whales feed gluttonously on this superabundant food, mainlyon krill, which consist of small crustaceans, and lay down mas-sive fat deposits. Some whales reach about 40% body fat at theend of summer. As the Antarctic summer turns to winter thepack ice extends outward from the continent, cutting off whalesfrom their feeding grounds. The whales depart for warm wa-ters thousands of miles (kilometers) away where the pregnantfemales give birth to their young and maintain lactation whileusually fasting until the following summer. These whales thuslive by a “boom and bust” economy and their huge size and re-duced metabolism per unit mass allow them to exist without

feeding through the greater part of the year. Similar patternsof seasonal feeding and dispersal are followed by whales in theNorthern and Southern Hemispheres except that the planktonfood supply in the Antarctic appears to be richer on averageand whales reach there larger sizes. Clearly, being able to fastduring the reproductive periods allows whales to choose areasof increased security for their newborn and growing offspring.The phenomenon of gigantic migratory whales is predicted onthe existence of polar mineral-enriched waters near the freez-ing point that, unlike tropical mineral-poor waters, are su-perlative producers of phyto and of zooplankton, as well as onthe existence of fast-freezing polar ice shelves that after sum-mer exclude the gluttonous behemoths.

Terrestrial migration has not been for small-bodied crea-tures, the myth of northern lemming migrations not with-standing. Small-bodied mammals tend to deal with seasonalityby growing fat in summer and hibernating during the winter,as do some northern carnivores such as bears and badgers.Hibernating is a withdrawal in time from severe climatic andforaging conditions; migration is a withdrawal in space. Thusthese are both adaptations that deal with the severity of sea-sonal winter climates.

The presence of large, very fat herbivores must have beenan irresistible attraction to human hunters for untold millen-



Migrating blue wildebeest (Connochaetes taurinus) and Burchell’s zebras (Equus burchellii). (Photo by © Fritz Polking/Frank Lane Pictures/Cor-bis. Reproduced by permission.)

nia. To exploit such migratory species, however, requires ei-ther following them continuously—an unlikely prospect—ordeveloping a way to regularly intercept their migrations,killing in excess of need, and finding means to store the sur-plus for the future. Intercepting migratory species cannot bedone with out understanding chronologic time. Migrants tendto reappear in the same localities much at the same calendartime, particularly if migration is closely tied to reproduction.Reproduction is timed in some of the migrants by the annual

light regime which, via stimuli through the optic nerve to thehypothalamus, regulates the hormonal orchestration of re-production. The variation in annual reproduction tends to benarrowly confined about specific calendar dates, and so arethe migratory movements associated with reproduction. Thesame individuals reappear in the same locality within a fewdays of the same calendar date each year.

There is some evidence to suggest that Upper Paleolithicpeople in Eurasia discovered chronologic time and used it topredict and exploit migratory reindeer. They marked what ap-pear to be lunar calendars on tines cut from reindeer antlers.That would have enabled them to anticipate reindeer migra-tions, move to localities where reindeer were vulnerable, andprepare for the kill. Reindeer bones comprise over 90% of thebones from Upper Paleolithic archeological sites. There is ev-idence for large flint-blade processing sites. Long, very sharpflint blades were struck skillfully from large flint cores. Theselong, thin flint flakes are ideal knives for the many handsneeded to carve up reindeer meat for drying. Wood ash, idealfor smoking and drying meat, predominates in Upper Pale-olithic hearths. The pattern of bone fragments indicates thatde-boning of reindeer carcasses was done away from process-ing sites, so that meat was brought in for processing with justthe bones required to hold the meat together or those usedfor marrow fat or tools. The superlative physical developmentof these large-brained cave-painters indicates that they enjoyedabundant food of the highest quality. Caribou meat has bal-anced amino acids for humans and caribou fat has an optimumessential fatty acid balance for brain growth. Caribou are val-ued highly as food by indigenous people and Arctic travelersand their fur is unsurpassed as a material for clothing and shel-ters in Arctic climates. Eventually salmon replaced some of thereindeer in the Upper Paleolithic, but salmon runs are alsochronologically timed and can be predicted by calendar dates.To exploit a reindeer or salmon run it is crucial to be at theright place in the right time. And the same applies to migra-tions of bowhead whales along the coast, an important tradi-tional food source for northern coastal people. Without anidea of chronologic time and how to keep track of it, no large-bodied mammalian migrants could be hunted systematically.With the discovery of chronologic time, however, these veryrich, predictable, high-quality food sources became availablefor exploitation, leading to the spread and dominance of mod-ern humans from the late Pleistocene onward.



Walruses (Odobenus rosmarus) migrate by following the ice packs.(Photo by Tui De Roy/Bruce Coleman, Inc. Reproduced by permission.)

ResourcesBooksGeist, V. Deer of the World. Mechanicsburg, PA: Stackpole

Books, 1998.

Geist, V. Mountain Sheep. A Study in Behavior and Evolution.Chicago: University of Chicago Press, 1971.

Irwin, L. L. “Migration.” In North American Elk: Ecology andManagement, edited by Dale E. Toweill and Jack WardThomas. Washington, DC: Smithsonian Institution Press,2002.

Maddock, Linda. “The ‘Migration’ and Grazing Succession.”In Serengeti: Dynamics of an Ecosystem, edited by A. R. E.

Sinclair and M. Norton-Griffiths. Chicago: University ofChicago Press, 1979.

Owen-Smith, R. N. Megaherbivores. Cambridge: CambridgeUniversity Press, 1988.

Slijper, E. J. Whales. Ithaca, NY: Cornell University Press, 1979.

PeriodicalsFancy, S. G., L. E. Pank, K. R. Whitten, and W. L. Regelin.

“Seasonal Movements of Caribou in Arctic Alaska asDetermined by Satellite.” Canadian Journal of Zoology 67(1989): 644–650.

Valerius Geist, PhD

What is domestication?Domestication is a process by which certain species of wild

animals have been brought into close relationship with hu-mans and thereby significantly changed the animals’ ways oflife. The process of domestication has been long and com-plicated, with unforeseeable consequences for both concernedsides. The consequences resulted in significant economic, so-cial, cultural, and political changes.

The process of domestication is similar to that of evolu-tion, except that the natural choice was made with artificialselection. Humans violently separated the ancestors of do-mestic animals from their wild relatives and step by step, gen-eration after generation, also changed their appearence andfeatures. This selection probably proceeded at first only ac-cidentally. Only later, when humans noticed certain connec-tions, did they start to use purposeful selection for differenteconomic, cultural, or aesthetic reasons.

Which species were domesticated?One of the main questions is why only a few species were

domesticated from such a huge number of wild animal species.For example, only 14 species were domesticated from thelarge group of terrestrial mammalian herbivores and omni-vores. The horse and the donkey were domesticated, but fourzebra species and the Asiatic ass were not. There are manyexisting testimonies that people almost 20,000 years ago werekeeping bears in captivity. The ancient Egyptians (in the OldKingdom 2500 B.C.) were keeping tamed addax antelope,hartebeest, oryx, gazelle, and cheetahs (for hunting). The an-cient Romans kept and bred dormice (for meat). None ofthese animals, however, was domesticated.

The answer is as follows. Wild animals must match sev-eral important conditions to be domesticated. If one of theconditions is not met, domestication will not occur. A candi-date for domestication must not be a narrow food specialist(e.g., the anteater or panda) because nourishment must beeasy to supply. It should also have a strong herd or pack in-stinct, which secures authority recognition and therefore sim-plifies comunication with a human. A social carnivore like awolf is much easier to tame than a solitary hunter like a leop-ard. Likewise, sheep and goats, which have a social system

based on a single dominant leader, are much easier to tamethan deer and most antelopes, which live in herds withoutdominance hierarchies. And the candidate animal should be“in the right place at the right moment.”

A distinctive barrier to successful domestication is foodcompetition (one of the reasons why the bear was not domes-ticated was that humans were not able to feed both themselvesand the bear). Other obstacles are nasty disposition, reluctanceto reproduce in captivity (cheetah), and the tendency to panicin enclosures or when faced with predators (antelopes, deer),or a long reproductive cycle and slow growth rate (which ob-viously has prevented real elephant domestication). The rea-son why zebras were not domesticated, even though thecolonists tried it in South Africa from the seventeenth centuryonwards, was due to their biting habits and dangerous behav-ior (they kick a rival until it is killed).

When and where?The beginnings and the progress of domestication of most

“classical” domestic animals are not known in detail becausethey depend on archaeological discoveries of human settle-ments, for example, bone fragments from waste holes, cavepaintings, or statuettes of animals. In the latest periods, it ispossible to obtain domestication information using geneticcomparative analysis. According to archaeologists, the begin-nings of domestication were at a period when human gather-ers and hunters became sedentary farmers, a period in whichthe domestication of wheat, barley, and peas also occurred.This change occured at the turning point of the Stone Age(Paleolithic and Neolithic) and it was so radical that it is referred to as the “Neolithic revolution.” It is a temporal bor-der that occurred more than 12,000 years ago. In archaeo-logical findings from western Asia, which are 11,000 and 9,000years old, it is possible to clearly follow changes in the wayof life according to the structure of food, which changed verydistinctively during that interval. While the remains of wildanimal species including cattle, pigs, gazelle, deer, foxes, ro-dents, fish, and birds predominate in the older findings, thereis a distinct predominance of sheep and goats in the more re-cent findings. It is very difficult to determine if the bone re-mains come from already domesticated animals or wild onesbecause at the beginnings of domestication the skeletal


• • • • •

Mammals and humans: Domestication and commensals

changes were very small. If there are predominatly male bonesin the findings (females were left for the production of off-spring) or if the bones are markedly smaller than those of wildanimals, archaeologists assume that they belonged to domes-tic animals.

The domestication of the majority of the traditional do-mestic animals usually occurred in areas where the humanpopulations had reached a certain level of cultural develop-ment and where there was a suitable wild ancestor. These ar-eas are designated as a “center of domestication.” The oldest(10,000 to 6000 B.C.) domestic centers were located in west-ern Asia and in the Middle East (the area of the “Fertile Cres-cent”) and were related to the beginnings of sedentarysettlements and the first successful experiments with breed-ing grain. In that area, goats and sheep were domesticated forthe first time, followed by cattle and pigs. Nevertheless, a verynarrow relationship was created a few thousand years earlierbetween tamed wolves and humans, so that the first domes-tic animal was a dog. This period became a sort of “start” and“instruction” period for the next domestication processes.The next significant domestic centers occurred in the Indian

continent (zebu), in China (goose, duck, pig, silkworm moth),in Central Asia (horse, camel), and in Southeast Asia (domesticfowl, pig, buffalo). In these areas the common domestic ani-mals of today were domesticated. A small percentage of do-mestic animals were bred on the American continents, inMiddle America, the turkey and musky duck, and in the west-ern part of South America, the llama and guinea pig. Fromthese centers domestic animals spread to other areas. Somespecies expanded all over the world (dog, cat, cattle, horse,sheep, goat, domestic fowl) while others remained only in theoriginal area of domestication (yak, Bali cattle, llama).

Why and how?We have to appreciate that the first breeders of domestic

animals did not have any instructions and they were not ableto imagine where domestication would lead. It is assumed thatthe initial reasons motivating domestication were frequentlydifferent from the animals’ subsequent use. However, themain reason was very simply to access a supply of food. Ex-ceptions are cats and dogs, which became partners to people,and later assumed many other roles, such as dogs becomingguardians. Even though of various origins, the domesticationscenarios of most animals were analogous and evolved in threemain steps. First came capturing and holding a wild animalin captivity (mostly young animals, when their mothers werekilled in the hunt), followed by gradual taming and herding.The third phase was breeding, where humans started to gen-erate animals according to their needs or beliefs that they wereimproving certain desirable qualities (intensive livestock hus-bandry). Sometimes it was a spontaneous process when theanimal connected to a human on a voluntary basis (dog, cat,pigeon), or when the human connected to the animal (rein-


Vol. 12: Mammals IMammals and humans: Domestication and commensals

The Yorkshire is a common breed of domesticated pig. It was createdby crossing the large white pig with the smaller Chinese pig. (Photoby Lynn M. Stone. Bruce Coleman, Inc. Reproduced by permission.)

Black miniature donkey and foal. People have used donkeys for rid-ing, driving, and pulling for centuries. (Photo by Animals Animals ©Re-nee Stockdale. Reproduced by permission.)

deer). Other species were barely tamed (wild ox, horse, ass).Domestication was a lengthy process; it is generally believedthat the shorter the developmental cycle of an animal, thequicker the change of generations and, therefore, the shorterthe domestication process.

What is a domestic animal?A domestic animal can be defined as one that has been bred

for a long time in captivity for economic profit in a humancommunity that maintains total control over its territorial or-ganization, food supply, and breeding, which is the most im-portant issue. Because domestic animals did not develop in aprocess of natural evolution, they are not considered distinctanimal species, and in the zoological terminology they arecatergorized as forms.

Humans breed and use many other animals that have notpassed through the domestication process. A typical exampleis the elephant. The working elephant has been used for some5,000 years and is still an important part of the work force inSoutheast Asia, even though they were never domesticated.Every individual is caught in the wild, violently tamed, andeducated to perform specific work. It almost never reproducesin captivity. The Indian elephant (Elephas maximus) is usedmostly for work, but the ancient martial elephants, for exam-ple those in Hanibal’s army, were African elephants (Loxodontaafricana). Other nondomesticated animals humans have em-ployed include birds of prey used for hunting (falconry), cor-morants used for fishing, macaques used to pick cocoa nutson the beaches, and dolphins and pinnipeds used by some mil-itaries.

Laboratory animals used for investigative and experimen-tal purposes are also a special group. Even though they havea shorter history of coexistence with humans than the morecommon domestic animals, these other species are also con-sidered domestic. Almost all domestic animals have been usedas laboratory animals, but not all laboratory animals are do-mesticated. In the last decades, the spectrum of animals usedfor laboratory purposes has expanded to include wild ani-mals.

A special group of domesticated animals is pets. Peoplehave been breeding them in their surroundings for severalcenturies or millennia, for example, the peacock or the danc-ing mouse.

Species that humans breed and change also include semi-domesticated animals, such as the fallow deer kept in enclo-sures. They reproduce with no problems and have severalcolor forms. Animals used for fur also belong to this group(mink, fox, coypu, chinchilla), as do ostriches, which are bredin farms.

Another group of animals called “commensal,” live withhumans. Commensalism is defined as the reciprocal coex-istence of two or more organisms. One of them benefitsfrom this relationship and the other is neither harmed norbenefits (“no harm parasitism”). This relationship is veryfree, close to symbiosis. Humans provide many opportuni-ties for commensalism. For example the house mouse (Mus

musculus) exploits human hospitality, and obtains food profitfrom human coexistence as well as a safe hiding place. Rats,rooks, seagulls, and many other animal species benefit fromrich food allocation in human wastedumps. Another exam-ple of commensalism is the pariah dogs in Asia and Africa.These live by scavenging around human towns, settlements,and roads. They are tolerated because they contribute totidiness.

Domestic changesWhen a given species of animal is bred in isolation from

its wild habitat and at the same time protected against unfa-vorable conditions, specific traits start to appear that disad-vantage the animal in a natural environment and would keepit out of the reproductive process in the wild—either becausemarkedly different individuals are easier victims for predatorsor because no partner will accept them. These different traitsare not kept in the wild populations or are very rare. Con-versely, these individuals were of interest to humans becauseof their different appearance or their submissive nature. Aftersome time, the changes in the nature, behavior, and in the re-production cycle become distinctive in domestic animals. Theyalso become stratified in their genetic make-up.

ColoringOne of the first signs of domestication is variability of

color. The individuals all have white spots or all white or allblack. It is interesting that white coloring is usually connectedwith lower performance (there are few white racing horsesand even fewer winners) or with different defects (white no-ble cats have a high incidence of deafness).


Mammals and humans: Domestication and commensalsVol. 12: Mammals I

Sometimes mammals are used for entertainment, such is the casewith horse racing. (Photo by © Kevin R. Morris/Corbis. Reproduced bypermission.)

Changes in hair and feathersThe quality of hair also markedly changes with domesti-

cation—the difference between guard hair and undergrowthvanishes. Long, wavy, or curly hair appears (sheep, donkey,horse, rabbit, cat, pig, goat, dog) or conversely the individu-als lose hair (dog, cat). In horses, the hair of the tail and manebecame visibly longer—wild horses have a short standingmane, and domestic horses have a mane that falls down to the neck.

Changes in the size and proportions of the bodyDwarf and giant forms have developed as a result of do-

mestication. In the early phases of domestication the overallsize of the body decreased (cattle, goat, sheep). This changeis attributed to premeditated selection (easier control andhousing of smaller individuals) combined with inadequatefood. Extra long ears also appeared (dog, sheep, pig, cattle,cat, rabbit), curled tails (dog, pig), or very short tails (dog, cat,sheep). Horns also became variable in size and curvature, to-tally disappearing in some species (cattle, sheep, goat).

Changes in the skeleton and internal organsStriking changes occurred in the skull; for example, there

was a shortening of the snout and jaws and at the same timea reduction of the number of teeth (dog, cat, cattle, pig). Theshortened snout and accentuated rounded eyes induced thejuvenile appearance of the “eternal cub.” It also resulted inlower brainpower and smaller brain volume. The skeleton be-came less resistant than that of wild animals as a consequenceof the “comfortable life” with its lack of movement. For thesame reasons, the size of some of the physical organs de-creased, for example, the heart (35% lower by weight in thedomestic rabbit when compared to its wild ancestor). Ofcourse there are exceptions. The English thoroughbred,trained for several centuries for racing, has a heart about onefifth heavier than that of other horses of the same size. Thefat storage mechanism has also been modified by domestica-tion. In wild animals, fat is stored in the surroundings of the

internal organs and under the skin, while in domestic animalsit is stored among muscle filaments and around the tail, es-pecially by pigs or sheep.

Physiological changesThere have been changes in the reproduction cycle, pro-

longed lactation (cattle, sheep, goats), and more numerous litters or eggs. Domestic animals reproduce themselves prac-tically throughout the whole year, and sexual adolescencestarts earlier that it does in wild animals.

Behavioral changesDomesticated animals lost shyness and many of them lost

totally the ability to survive in the wilderness (sheep). Someinstincts have changed or totally vanished and the rhythm ofgiven activities has completely changed. For example, somedusk animals and night animals have become strictly day an-imals (pig) while some changed from monogamous to polyg-amous (goose). Many domestic offspring are not taughtbehavior because they are quickly weaned from their parents,



Sheep have been domesticated for both their meat and their wool.(Photo by Andris Apse. Bruce Coleman, Inc. Reproduced by permission.)

A quadriplegic woman with a capuchin monkey as an aid. Monkeyhelpers perform simple, every day tasks such as getting food and drink,retrieving dropped or out of reach items, turning lights on and off, andother chores. (Photo by Rita Nannini/Photo Researchers, Inc. Repro-duced by permission.)

if they come in contact with them at all. They are denied thelearning that parents teach their offspring in the wild.

What is the breed?The basic category of domestic animals is the species, as

is the case with wild animals. The species of domestic ani-mals are differentiated into breeds, while that of wild animalsare differentiated into subspecies. A breed is defined as agroup of animals that has been selected by humans to pos-sess a uniform appearance that is inheritable and distin-guishes it from other groups of animals within the samespecies. Domestication and selective breeding have changedsome species of domestic animals (camel, reindeer) very lit-tle. But in others, including the oldest and the most impor-tant species of domestic animals, tens and hundreds of breedshave been developed; compare for example the pocket-sizedChihuahua with the huge mastiff or Saint Bernard dog. Somespecialized breeds are not able to carry out an independentexistence. Others become wild without any problem and areable to set up feral populations under suitable conditions.People used artificial selection from the early days of breed-ing even though they did not know the rules of heredity andthe selection of features was varied. For example, Europeancattle were bred to increase milk and meat production andworking capacity, while African pastoralists preferred to in-crease the size of horns.

Threatened breedsEnormous numbers of different breeds have developed dur-

ing many millenia, most very well acclimatized to local con-ditions. It is estimated that 5,000–6,000 breeds exist today.Four thousand belong to the so-called “big nine” (cattle, horse,donkey, pig, sheep, goat, buffalo, domestic fowl, duck). How-ever, the trend has moved to renewed selection efforts duringthe latest decades, for example, the present specialized dailymilk production capacity of a Holstein Friesian averages 10.6gal (40 l) of milk compared to the African N’Dama, produces1.1 gal (4 l). These highly productive but very vulnerablebreeds are now found all over the world, and in many placesthey have totally replaced the original breeds or have beencrossbred with them. In this way, the original breeds disap-pear, and with them go extremly important genetic variations.In 1993, the Food and Agriculture Organization (FAO),started a project called Global Strategy for the Managementof Farm Animal Genetic Resources, which is responsible forthe preservation of livestock of no economic value. The cate-gories “extinct” or “critically threatened breed” have been in-troduced, as has been done for wild animals.

Disadvantages of domesticationThe number of domestic animals greatly exceed the num-

ber of wild or related species. In some cases, their wild ances-tors have been completely exterminated. The breeding ofdomestic animals has provided people with many indisputableadvantages, but it has its downside. The grazing of large live-stock herds diminishes food and water resources of local wild

animals in Africa and leads to the total devastation of the land-scape. Bison almost became extinct because pasture lands wererequired for domestic cattle in North America. Large areas ofrainforest in South America are being converted to pasture forcattle today, presenting conservation difficulties. Herds ofsheep and goats completely devastated large areas of Mediter-ranean and central Asia. The infestation by domestic rabbitsnearly devastated the breeding of sheep, another domesticatedanimal, in more than half of the Australian continent. Enor-mous ecological damage was committed by wild populationsof goats and pigs that were abandoned by sailors in manyMediterranean islands. Together with feral dogs and cats theyliquidated enormous amounts of local fauna and flora. Theyare responsible for more than a quarter of extinct species andsubspecies of vertebrates. Feral goats present a similar prob-lem on a number of the Galápagos Islands, threatening thewildlife there.

Domestic horse (Equus caballus f. caballus)The horse was the last of the five most common livestock

animals to be domesticated. After a short period when it wasused only as a source of meat, it became established as a per-fect means of transport until the recent past.

The history of the wild horse in Europe and Asia fromthe end of the Pleistocene until its domestication in perhaps4000 to 3000 B.C. is poorly understood. According to pre-vailing opinion, wild horses during the domestication be-longed to two species. These were the Przewalski horse (E.przewalskii) from semidesertic central Asia and the tarpanhorse (E. caballus, syn. E. ferus) with two subspecies, the for-est tarpan (E. c. silvestris) and the steppe tarpan (E. c. ferus),which lived in an area ranging from western Europe to theUkrainian steppes. The two species are the only ancestorsof all recent breeds of domestic horse. The last tarpan wasexterminated in 1879 in the Ukraine and the Przewalskihorse was no longer found in the wild as of 1960, survivingonly in zoos. However, its breeding is so successful now thatthe process of its reintroduction has started in Mongolia.



Domesticated cats have helped people keep homes free of rodentsfor many thousands of years. (Photo by Ernest A. James. Bruce Cole-man, Inc. Reproduced by permission.)

It is assumed that the area of steppes between the Dnieperand the Volga Rivers is the oldest domesticating center forhorses. The region was populated by a culture called the SredniStog in the years 4000 to 3400 B.C. The horses were breddoubtless not only for meat but also for riding. It is also as-sumed that, in the same period, horses were domesticated byother people who lived in the steppe corridor of Eurasia fromsoutheast Europe to Mongolia. From the second milleniumB.C., the combative tribes of nomadic Skyt, Kimmer, Hun, andMongol started out from Asian steppes in regular intervals onthe backs of their hardy and tough ponies to the west, east, andsouth and, until the fifteenth century, propagated not only ter-ror and dread but also the fame and genes of their horses. Inancient civilizations, horses were first considered “luxurygoods.” However, they spread very quickly and at the turningpoint of the second and first millenium B.C. they we’re a com-mon phenomenon. During the first millenium B.C., horses werealso commonly used for farming, transportation, and sport.

After almost 6,000 years of human service, the appearanceand many features of the horse have changed, though less thanthat of other domestic animals. The first primitive horsebreeds developed naturally with the influence of different cli-mate, food, and prevailing working usage. Today there aremore than 200 breeds of horses, in a range of different sizes.The smallest horse is the Falabella, at 28 in. (71 cm) high and

with a weight of 44 lb (20 kg), and the largest is the Percheron,which is 6 ft (1.8 m) and 2,600 lb (1,180 kg). All the breedshave unique performance, working abilities, and stamina. Inthe sixteenth century, horses went back to the American con-tinent, where they had lived more than 10,000 years ago. Mostof them ran wild and constituted large feral populations ofmustangs (North America) and cimmarons (South America).Correspondingly, the same situation occurred later in Aus-tralia, where feral brumbies live today.

Domestic donkey (Equus africanus f. asinus)It is said that the donkey is the horse of the “poor people”

and undeservingly it remains in the shadow of its more famousrelatives. It is not actually headstrong, dumb, and lazy. It hasonly a more evolved instinct of self-preservation, which allowsit to preserve itself from human service. The donkey does notas a rule bond emotionally to humans as horses do. If it hasgood treatment and a warm stable, it is a priceless helper, es-pecially in stony terrain. It does not mind hot weather or mis-erable food, it hates only dirty water and rainy weather.

The domestic donkey is the descendant of two subspeciesof the African ass. The Nubian wild ass (E. a. africanus) wasdomesticated in 5000 B.C. in the Nile Valley and in the area



Draft horses have made it possible for farmers to plow much larger fields. (Photo by Animals Animals ©Charles Palek. Reproduced by permission.)

of Libya, today it is assumed extinct. The second subspeciesis the Somali wild ass (E. a. somaliensis). It was also domesti-cated in the area around the Persian Gulf, and is today nearlyextinct. The descendants of both subspecies crossbred andquickly spread, thanks to military expeditions and lively mer-cantile bustle, through Palestine to western Asia and fartherto the east through Morroco to the Pyrenean Peninsula,where they arrived in the second millenium B.C. It is knownthat during the first millenium, the Celts were breeding don-keys. The Asiatic ass (Equus hemionus) was for some time anobject of interest but domestication did not succeed due toits uncontrollable nature.

Donkey breeds have never reached the number of varietiesthat horse breeds have. They differ in height (from 2 to 5 ft[0.6–1.5 m]), in weight (175 lb–990 lb [80–450 kg]), in color,and in the quality of hair. The donkey is still a common com-ponent of country life in the Mediterranean, the Balkans,south Asia, South America, and other subtropical and tropi-cal areas. Feral donkey populations live for many generationsin the southwest United States and in Australia.

Humans have used horses and donkeys to breed hybridspecies. The most famous is the mule, the offspring of a fe-male horse (mare) and a male donkey (jackass). A second hy-brid is less known, the dunce hinny, whose parents are afemale donkey (jenny) and a male horse (stallion). Hybrids in-herit more traits from the mother. Another interesting inter-species hybrid is the zebroid. It is the offspring of some zebraspecies and a horse, or rarely a donkey.

Cattle (Bos primigenius f. taurus)Cattle are the oldest domestic animals. Their importance

lies in giving meat, milk, and working power. Leather, fat,hooves, and horns are also valuable, and dried excrements areused as fuel, building material, and fertilizer. Cattle were firstused as draft and riding animals, allowing people to drasticallychange their way of life. Some African people, for example theHottentots, use them for riding even today. Cattle are the mainsource of meat and milk and the second most numerous do-mestic animal in the world, after domestic fowl. Under thecattle category, we can include the descendants of the aurochs,and those of other domestic cattle such as the yak, gayal, Balicattle, and buffalo. They come from areas with extreme cli-matic conditions (high in the mountains or from the tropics),where they are used as domestic cattle. The kouprey (Bossauveli) from the forests of Cambodia occupies a special placeamong cattle, for it may be the last surviving form of the wildox, which went through an early form of domestication andthen ran wild again.

The aurochs (Bos primigenius) was a progenitor of domes-tic cattle. It occupied the forests of the whole temperate zoneof the Old World from Europe to north Africa and west Asiato the China Sea at the end of the last glacial period. In thislarge area, it developed more subspecies. The wild ox had sur-vived almost until the end of that glacial period in Asia andnorth Africa, and in the middle and west European forests,until the end of the Middle Ages. The last individual becameextinct in Poland in 1627. The domestication of the wild ox

began in 7000 B.C. and it is assumed that it started almost atthe same time in several places—Greece, Macedonia, the Fer-tile Crescent (Mesopotamia, Egypt, Persia), and later (5000B.C.) in the Indus Valley. It is possible (according to new ge-netic research) that an independent domestic center existedalso in north Africa and could even be the oldest.

Why did people try to domesticate such massive and dan-gerous animals? They already bred sheep and goats at thattime, which were sufficient as a source of food. It is possi-ble that at first there were religious reasons. Wild cattlesymbolized fertility and power for many cultures and theywere significant sacrificial animals. Cattle derived from au-rochs include some 450 breeds today and are divided intotwo basic groups. One is humpless cattle, which are the Eu-ropean descendants of the aurochs (B. p. primigenius, syn.Bos taurus). The second group includes cattle with a hump(zebu) whose progenitor is assumed to be the Indian sub-species of the aurochs (B. p. namadicus, syn. B. indicus).

The oldest known bone findings, which confirm the exis-tence of humped zebu (thorny projections of neck vertebraedistinctly bifurcated) are almost 6,000 years old and comefrom Iraq. However, the domestication of the zebu probablyoccurred in the Indus Valley. The zebu adapted to sub-tropical and tropical climates and became resistant to tropi-cal diseases. After domestication, it spread quickly to Malaysia,Indonesia, and China and to the west to Africa. Today it isone of the most plentiful cattle in the African tropics and sub-tropics and in the Indian subcontinent.

Domestic yak (Bos mutus f. grunniens)The yak was domesticated in Tibet from 3000 to 1000 B.C.,

and its progenitor is the wild yak (Bos mutus). It is almost one



The goat (Capra hircus) has many uses to humans, such as a foodand clothing source. (Photo by Hans Reinhard. Bruce Coleman, Inc.Reproduced by permission.)

third smaller than its wild progenitor and it has markedlyweaker horns or no horns. It moves without any problems ataltitudes of 9,800–19,500 ft (2,990–5,940 m). It is an indis-pensible helper for the mountain inhabitants and the basicsource of livelihood. The yak provides milk, meat, and wool.Dried excrement is used as fuel. The yak is a great workinganimal. It bears around 330 lb (150 kg) very easily, it servesas a riding and draft animal, and is used for plowing. Twelvemillion yaks live in the mountains areas of Tibet, China,Nepal, Mongolia, and southern Siberia. It is bred to a smallextent in North America and in the Swiss Alps.

Gayal (Bos gaurus f. frontalis)The gayal or mithan is the domesticated form of the wild

gaur (B. gaurus). For a long time, it was not clear if the gayaland gaur were the same separated species or if the gayal haddeveloped by crossbreeding of a gaur with bantengs or zebu.The gayal is noticeably smaller than the gaur, it has shorterconical horns, a markedly shorter skull, and a wider and flat-ter forehead. It has a large double dewlap on the chin and neck.It is most commonly brown and black but can also be spottedor white. The gayal is not a typical domestic animal; it usuallylives in small groups in the jungle at the periphery of a villageand comes back to the village only towards evening, lured bysalt. The economic use of the gayal is insignificant. Sometimesis it used for field work or for its meat; its milk is not drink-able. The gayal was used by many people as a sacrificial ani-mal or as currency. Sometimes the animals escape and run wild,

but the domestication influence is still seen in their calm tem-perament. Feral populations live in northern India.

Bali cattle (Bos javanicus f. domestica)Bali cattle is the domestic form of wild banteng (B. ja-

vanicus), which lives in the forests of Java, Borneo, Malaysia,and Thailand today. Its domestication took place in Javaaround 1000 B.C. Wild bantengs were caught and tamed inthe Middle Ages, in Bali, Sumatra, and Java until the eigh-teenth century. Bali cattle are smaller than banteng, the hornslack the characteristic curvature, and the skull is smaller. Theexternal sexual signs are weaker than in the wild species. Thedomestic species grows more rapidly and matures earlier. El-egant Bali cattle have adapted to life in tropics better thanthe zebu. It was never bred for a specific purpose and be-cause of that it has no major economic value. Approximately1.5 million individuals are bred today. It is used as other do-mestic cattle for field work and riding. Milk utility is low butmeat has excellent quality and taste. Bali cattle are crossbredwith the taurine cattle, and with the zebu, but male descen-dants are infertile. Bali cattle often run wild, and feral pop-ulations live in savanna in the south of Sulawesi and inAustralia.

Sheep (Ovis ammon f. aries)Sheep and goats are assumed to be the oldest domestic

livestock. Sheep are bred in different areas around the worldfrom lowlands to mountains and from tropics to cold northmoorlands. They are exceptionally acclimatized to extremeconditions. They are also very useful, providing meat, milk,tallow, wool, fur, leather, horn, lanolin, dung, and they carryloads in Tibet. No culture or religion forbids killing sheepor eating sheep meat.

The exact origin of the domestic sheep is not clear becauseall wild sheep in the genus Ovis are fertile when bred togetherand zoologists still do not agree about their taxonomy. Twogroups of wild sheep are considered as having first undergonedomestication. They differ in the size of the body and in theirhabitats. The arkhar or argali sheep (O. ammon) is the repre-sentative of the “mountain” group. It has six subspecies and itlives in central Asia in altitudes ranging from 16,500 to 19,500ft (5,030–5,940 m). The Asiatic mouflon (O. orientalis) and theurial sheep (O. vignei) are members of the “steppe” group ofwild sheep. They also have several subspecies and live in lowerregions from west Asia to northwest India. The European mou-flon (O. musimon syn. O. ammon musimon) is a special case. Itcomes from Corsica and Sardinia and it was assumed to be theprogenitor of domestic sheep for a long time. However it is it-self a feral form of the early Neolithic domestic sheep, whichcame with humans to Corsica 9,000 years ago. The questionof domestic sheep progenitors is still debated. With certaintywe can eliminate only the species that were not domesticated.These are the American bighorn sheep (O. canadensis), Dall’ssheep (O. dalli), and the Siberian snow sheep (O. nivicola), whichwere not “in the right place at the right time.” All other speciesare good candidates.



This domesticated dog has been trained to help hunters retrieve game.(Photo by St. Meyers/Okapia/Photo Researchers, Inc. Reproduced bypermission.)

Almost 14,000-year-old paintings from the La Pileta cavein Spain show sheep and goats in a corral. It takes a long timefor wild sheep, which were kept in simple corrals, to becometruly domestic animals. The oldest findings of domestic sheepcome from the north Iran mountains (Zawi Chemi Shanidar)and date from 9000 B.C. However, there were certainly moreareas of domestication in western Asia at that time. In 4000B.C., domestic sheep were bred throughout the civilized world.At first they gave only meat, milk, and leather, and only laterdid wool sheep appear, though only with short and rough wool(in Mesopotamia around 3000 B.C.). In the first millenium,sheep spread all over Europe, Africa (except in primeval for-est areas), and Asia (to Sulawesi). At that time sheep with white,longer wool were common, with four horns or without horns(known from ancient Egyptian frescos). Sheep from antiqueGreece and Rome resembled modern breeds. The number ofsheep breeds today ranges between 550 to 630. They are cat-egorized according to wool type, tail length, fat deposits, orutility. There are no existing feral sheep populations exceptthat of the European mouflon and the Soay sheep.

Goat (Capra aegagrus f. hircus)Goats live throughout the world but they flourish in hu-

mid tropical forest areas. Their number is still increasing, es-pecially in the desert and the semi-desert areas where it is notpossible to keep other domestic animals. Goats give meat,milk, leather, hair, wool, horn, and dung and have very lowfood requirements.

The domestic goat progenitor is the bezoar goat (C. aega-grus), which lived in western and central Asia. According to ra-diocarbon dating, the sheep was domesticated first but goatswere more numerous than sheep in the early domestic period.The oldest domestic center of both species was Sierra Zagrosat the border of Iraq and Iran. Determination of whether re-mains belong to wild or domestic goats is possible accordingto horn shape. Archaeologic findings show that the originallyscimitar horns of wild goats changed during several hundredyears (8000 to 7000 B.C.) to the twisted horns of domestic goats.We do not know why people preferred these animals withtwisted horns or if the horn shape related to the behavior ofgoats, or their productivity.

The domestic goat quickly spread to all inhabited areas ofEurope, Asia (to Sulawesi), and Africa. It preserved its ani-mation, shrewdness, and obstinacy from its progenitors,which passes for happy malevolence. There are many feraldomestic goat populations, for example, in New Zealand, inAustralia, and unfortunately in the Galápagos and other is-lands where they cause severe ecological problems. There arenow some 200 to 350 goat breeds.

Pig (Sus scrofa f. domestica)The domestic pig was likely domesticated after cattle. It

is omnivorous (as humans are), and is exceedingly intelligent.The number of domestic pigs is estimated at nearly 913 mil-lion worldwide. The only places they are not bred are in un-suitable climate areas (tropics, polar areas) and in Israel and

Islamic countries, where eating pork is forbidden by religion.The pig is bred only for its meat and fat, although leather isa secondary product.

The progenitor of the domestic animal is the wild boar(Sus scrofa), which lived in a large area from western Europeand north Africa to Southeast Asia. A range of subspeciesevolved, of which two were domesticated, the European wildboar (S. s. scrofa) and the Asian banded boar (S. s. vittatus).The next two species domesticated in Southeast Asia were theSulawesi wild boar (S. celebensis) and the Philippine warty pig(S. phiilippensis).

Wild boar domestication dates from 7000 to 6000 B.C. Oneof the important preconditions of this process was sedentarycivilization because, unlike sheep, goats, and cattle, pigs arenot able to live a nomadic life. Pig domestication occurred in-dependently in two or maybe more places, partly because ofhow relatively easy pigs are to tame. The first domestic cen-ters (6500 B.C.) were in western Asia, India, and some islands.From there, domesticated pigs were moved into China, Egypt,and farther into Africa. The second center of domesticationfrom 5000 B.C. lies in northern Europe by the Baltic Sea. Thethird important area was the Mediterranean.

Domestic pigs came to the New world with European set-tlers. Sailors also left them on islands. Other feral populationsdeveloped in South and Central America, Australia, and NewZealand. As feral goats do, the pigs destroy specialized islandfauna and flora.

Camels and llamasThe camel was and is an excellent transport vehicle in

desert areas where horses and donkeys cannot survive. Indeserts, camels can survive ten times longer than humans andfour times longer than donkeys. They provide meat, milk,blood, leather, and hair, and excrements are used as fuel. Thewild Bactrian camel (Camelus ferus) is the ancestor of the Bac-trian or two-humped camel (C. ferus f. bactrianus). It comesfrom east and central Asia. The remaining populations live inthe periphery of the Gobi Desert. It was domesticated by no-madic tribes, probably in the second or first millenium B.C.in Iran or in the Gobi Desert.

There is no known evidence about the wild progenitor ofthe dromdary or one-humped camel (Camelus dromedarius). Itwas proposed that the progenitor could be the extinct Camelusthomasi, which lived in the interface of the Tertiary and Qua-ternary periods in north Africa and in adjoining areas of Asia.The one-humped camel was probably domesticated in 3000B.C. in the Arabian Peninsula or in the steppe areas of west-ern Asia. The oldest testimonies of domestic camels comefrom Egypt and the Sinai, 5,000 years ago. Almost 19 milliondomestic camels are bred worldwide, of which almost 90%are one-humped camels. They live in desert areas from thewestern Sahara to India and as feral populations in Australia,where they were introduced one hundred years ago. The two-humped camel is bred in Mongolia, China, Afghanistan, Iran,and Turkey.



Two species of camelids live in South America: the gua-naco (Lama guanicoe) from semidesert mountain areas, and thevicuña (Vicugna vicugna) from high mountain areas. Only theguanaco was domesticated, perhaps in 3000 B.C. Its descen-dants are the llama (Lama guanicoe f. glama) and the alpaca (L.guanicoe f. pacos). The llama has been used as a transport animal, and for meat and wool, and the alpaca primarily for wool.

Reindeer (Rangifer tarandus)Not much is known about the domestication of the rein-

deer. It is assumed that it was domesticated at only one placein the Sayan mountains from 3000 to 1000 B.C. Chinesesources from the sixth century describe the reindeer as a do-mestic animal. The reindeer may have become used to hu-mans when it came to human settlements to lick salt fromhuman urine. It served in place of cattle and horses in harshnorthern conditions. Domestic reindeer live in northernEurasia and Canada. The Canadian caribou (R. tarandus cari-bou) was never domesticated. Domestic reindeer do not dif-fer from wild reindeer, except that they may vary in size andcoloring. Those who keep reindeer must live the nomadic wayof life because the reindeer still migrate along ancient paths.The domestic reindeer serves as a riding and draft animal,and provides milk, meat, leather, hair, and antlers.

Dog (Canis lupus f. familiaris)The dog was the first domestic animal; however, the be-

ginning of its coexistence with humans is still unclear. The wolf(Canis lupus) is the progenitor of all domestic dog breeds andferal populations. Fifteen thousand years ago, the wolf lived inall of Eurasia, in north Africa, and in North and Central Amer-ica. It evolved into many subspecies, which differ in size andcolor. The small Indian wolf (C. l. pallipes) and the largerEurasian wolf (C. l. lupus) are the most likely dog ancestors.

Humans were interacting with wolves in the end of Pleis-tocene. They were hunting the same type of prey and in theareas where they coexisted, both species got used to eachother over thousands of years. Food lured the wolves to hu-man settlements and humans counted on the watchfulness ofwolves. Taming an adult wolf is almost impossible, but smallcubs are easier to tame. The problem of feeding the cubs wassolved very simply: women nursed them. If the cubs were tooaggressive, the humans killed them for food. Only submis-sive individuals were allowed to reach adulthood and repro-duce. The ease of this domestication process was confirmedby recent experiments with foxes. Individuals were selectedaccording to their level of aggressiveness. The behaviorchanged during a mere twenty generations and the whitespots and curled tail present in domestic dogs appeared inthat time as well.

The skeletal remains of the first domestic dogs come fromdifferent places around the world, from Israel, Turkey, Iran,Japan, England, Denmark, Germany, and North America.The oldest findings verifying the existence of the domesticdog is an 11,000-year-old grave, found in northern Israel in

the Ein Mallaha settlement. Feral populations of dogs devel-oped in places where wild populations of wolves never lived.The dingo (C. l. dingo) spread in Australia at least 4,000 yearsago. The forest dingo (C. l. halstromi) spread over New Guineaand Timor. Feral dog populations exist in many other placesall over the world. Around 420 domestic dog breeds are reg-istered but that number may still change.

Domestic cat (Felis silvestris f. catus)The cat is one of the most recent domestic animals. In

spite of its coexistence with humans, it still has an indepen-dent nature and the perfect hunting instincts of a solitaryhunter. It is highly individualistic and should not have un-dergone successful domestication at all.

The progenitor of the domestic cat is the African sub-species of wild cat (Felis silvestris lybica). Domestication of thecat occurred in Egypt from 4000 to 2000 B.C. Preserved catmummies provide dometication evidence. The oldest are oftamed cats from the 4000 B.C. period while mummies fromthe end of the Middle Kingdom period are of domesticatedcats. The domesticated cats have shortened skulls and oftenirregular denture. The cat likely started its coexistence withhumans voluntarily and to the benefit of both sides. Wild catswere drawn together into the Nile Valley because of the num-ber of rodents that accompany human settlements. Theyquickly became common domesctic animals and theyachieved the status of sacred animal of the goddess Bastet.The domestic cat has spread from Egypt throughout theMediterranean and reached southern Europe in 500 B.C. Thecat came to the east with merchants to Turkey, Persia, andalong the silk road to China and Southeast Asia. It penetratedCentral Europe at the beginning of the Middle Ages. Bene-dictine monks were the first true cat breeders (they also bredthe first rabbits and pigeons in Europe). Feral cat populationsexist on many islands and threaten the populations of localinsular animals.

Rabbit (Oryctolagus cuniculus f. domesticus)The rabbit is the “youngest” domestic animal. The wild

rabbit (Oryctolagus cuniculus) is the only progenitor of the do-mestic rabbit. The monks in Benedictine monasteries startedits domestication at the beginning of the Middle Ages in thesouth of France. Rabbit meat was eaten during Lent and sothe monks kept the rabbits in closed tiled monastery yards.Rabbit breeding spread from France to England, Belgium,and Holland in the seventeenth and eighteenth centuries andthe biggest boom in rabbit breeding began in the nineteenthcentury. Rabbits were already the source of cheap and read-ily available meat for a large number of people in Europe.Several hundred breeds exist today because of the rabbit’spopularity as a pet, as well as a source of food and other material.

Guinea pig (Cavia aperea f. porcellus)The guinea pig is one of the few animals domesticated in

the New World. It was a sacrificial animal and a pet for the



local inhabitants. The wild guinea pig (C. aperea) may be theprogenitor but some zoologists think the montane guinea pig(C. tschudii), which lives only in the mountainous areas ofPeru, southern Bolivia, northwestern Argentina, and north-ern China, is the progenitor. The period of its domestication

has not been determined exactly, but the remains of domes-tic guinea pig were discovered in deposits dating back to 3000B.C. in the Peruvian Andes. The guinea pig became the mostpopular and the most often bred rodent. It is very easily tamed,almost never bites, and it is able to communicate very well.



ResourcesBooksBudianski, S. The Covenant of the Wild: Why Animals Chose

Domestication. New York: William Morrow, 1992.Clutton-Brock, J. A Natural History of Domesticated Mammals.

Cambridge: Cambridge University Press, 1999.Harris, D., ed. The Origin and Spread of Agriculture and

Pastoralism in Eurasia. London: UCL Press, 1996.Hemmer, H. Domestication: The Decline of Environmental

Appreciation. Cambridge: Cambridge University Press, 1990.Serpell, J., ed. The Domestic Dog: Its Evolution, Behaviour and

Interaction with People. Cambridge: Cambridge UniversityPress, 1995.

PeriodicalsBradley, D. G. “Genetic Hoofprints.” Natural History

(February 2003): 36–41.

Diamond, J. “Evolution, Consequences and Future of Plantand Animal Domestication.” Nature 418 (2002): 700–707.

Grikson, C. “An African Origin of African Cattle? SomeArchaeological Evidence.” The African Archaeological Review9 (1992): 119–144.

Alena Cervená, PhD

Introduction

When all the crop losses and control and containment costsare added up, non-native invasive species (including weedsand insects) cost the United States alone an estimated $137billion annually. The more intangible effects of invasivespecies on natural ecosystems are also serious. Invasive speciesare sometimes termed “biological pollutants,” because preda-tion and competition by invasive species can reduce popula-tions of native species and cause extinctions. Indeed, half ofthe known cases of bird extinctions on islands are linked tointroduced mammalian predators, such as cats.

The top invasive mammal pests worldwide are rats, mice,cats, dogs, cattle, burros, horses, goats, hedgehogs, foxes, graysquirrels, coypus, pigs, possums, rabbits, deer, weasels, mink,and the mongoose. Globally, rodents like rats and mice con-sume an estimated 5–15% of grains like rice, wheat, and cornin the fields before harvest. East African countries have lostas much as 80% of the crop during severe twentieth centuryrodent outbreaks. After the harvest, the combined actions ofinsects, rodents, fungi, and other organisms may destroy an-other 5–15% of stored grains, though some areas experience20% losses. Stored grain losses are estimated at $5 billion peryear in India alone, and may run as high as $1 billion per yearin the United States. According to one estimate, rodents de-stroy enough food to feed 200 million people. These lossesmay be just the tip of the iceberg, as there is little economicdocumentation on invasive mammals.

Although they are considered invasive pests when feral inthe wild, many of the top invasive mammals in the world leada double life, as they are also desirable as pets and valuable asagricultural livestock. For example, cats, dogs, and rabbits arefavored domestic pets and companions, but can be both a nui-sance and a menace to ecosystems when turned loose in thewild. Similarly, horses and burros are used as pets and live-stock, but in the wild they can damage ecosystems and de-prive other species of food and water.

An understanding of what constitutes a pest helps clear upthis seemingly contradictory duality of an animal being bothbeneficial and a pest. The term “pest” is not an absolute term,rather it is subjective. When an organism is in the wrongplace at the wrong time and is unwanted it is deemed a pest.

When humans want the same organism around, it is nolonger labeled a pest. With the definition of a pest so muchin the eye of the beholder, reasonable people can, and oftendo, disagree about whether a particular organism is or is notan invasive pest.

For example, wild horses and wild burros, which were in-troduced on the North American continent as a consequenceof the European colonization, are viewed positively, oftennostalgically, by many people as a historical living legacy ofAmerica’s frontier days when the wild West had miners withburros and cowboys on horseback. But to ranchers grazingpublic lands, wild horses and wild burros are often viewed aslittle more than hoofed locusts, stealing valuable forage fromlivestock.

Indeed, at one time wild horses were herded into dead-endcanyons and shot, though now they are captured and adopted.Even environmentalists can alternately wax positive or nega-tive, depending upon whether the wild horses or wild burrosare befouling a sensitive area and threatening the food sourcesand drinking water of native species such as mountain sheep.

Thus, viewing an invading species in a negative light anddesignating it as pestiferous or alternatively viewing an in-vader in a positive light is the product of underlying assump-tions, ideologies, and value judgments. Sometimes theseunderlying ideologies, assumptions, and value judgments areimplicit, below the surface, and hard to discern. Other times,as with the case of the American mink (Mustela vison) in theUnited Kingdom, the rhetoric is as heated and open as themost contested political and ideological issues debated in theBritish Parliament.

In the United Kingdom, a European island nation, theAmerican mink was imported for small-scale fur farming in1929, and sometime thereafter began escaping into the wildsof England and Scotland. Being a polyphagous predator,American mink have gobbled up ground-nesting seabirds inthe firths and lochs of northwest Scotland, as well as an en-dangered native mammal whose riparian habitat is threatened,the northern water vole, Arvicola terrestris. In some countrieswater voles could easily be depicted as just another water rat,and the case for their preservation dismissed as another ex-ample of radical environmental lunacy. But in the UK, water


• • • • •

Mammals and humans: Mammalian invasives and pests

voles are a beloved icon of English literature, populatingnovels like Evelyn Waugh’s Scoop and starring as Ratty,Toad’s companion in The Wind in the Willows.

While the water vole has deep roots in English culture andsupporters in high places direct Heritage Lottery Funds itsway, getting rid of the invading American mink to aid the en-dangered vole is a cause that runs into the ideological con-cerns of animal rights activists who want to free the minks.When Great Britain passed the Mink (Keeping) Regulationsof 1975, which mandated measures to stop the further escapeof American minks from fur farms into the wild, little thoughtwas given to activists in the animal rights movement invad-ing fur farms and setting minks free. Not only have law-break-ing animal rights activists invaded fur farms and illegally setloose more American mink into the British wilds, where theythreaten endangered water voles, but many also question thepremise that the American minks are an ecological threat.

Not all invasive mammal stories are quite as dramatic orfilled with such emotional passion, even in the UK, whereduring the past century introduced North American graysquirrels, Sciurus carolinensis, have quietly displaced the UK’sonly native squirrel, the red squirrel, S. vulgaris. The redsquirrel, whose British lineage dates back to the last Ice Age,

is now rare in southern England, with only remnant popula-tions remaining in places like the Isle of Wight and PooleHarbor. The picture is equally bleak in central England, withremnant red squirrel populations in East Anglia, Stafford-shire, Derbyshire, and Merseyside. Even in their currentstrongholds of northern England, Wales, and Scotland, redsquirrels are losing territory to gray squirrels.

Local red squirrel extinctions have always been relativelycommon. But before the intentional introduction of graysquirrels began in the 1870s (an era when species were stillfreely moved from continent to continent with little concernfor ecological consequences), red squirrels almost always re-colonized areas several years after local extinctions. The out-come may have been different if there was just one release ofgray squirrels. However, there were repeated releases of graysquirrels from the 1870s until the practice became illegal in1938. No doubt these well-intentioned human releases of graysquirrels to recolonize habitats put the red squirrels at a greatdisadvantage and contributed to their relatively rapid loss ofhome range.

Nevertheless, the best explanation put forth today for thecontinuing displacement of native red squirrels by introducedgray squirrels is ecological competition. In other words, gray


Mammals and humans: Mammalian invasives and pestsVol. 12: Mammals I

The Maori may have hunted moas to extinction in New Zealand. (Illustration by Wendy Baker)

squirrels are believed to be outcompeting and thereby re-placing red squirrels in their former ecological niches such asparks, gardens, broadleaved woodlands, and conifer forests.Biodiversity and timber values (gray squirrels damage thebark) may ultimately be affected by this shift in squirrelspecies, which is still in progress.

The importation of the coypu, or nutria (Myocastor coypus),from South America to the North American continent is, likethe gray squirrel and American mink, another case of seem-ingly good human intentions gone awry. Business people orig-inally imported the herbivorous coypus from southernArgentina to the United States for fur farming in 1899. Coypufarms rapidly spread from California to Oregon, Washing-ton, Michigan, Ohio, Louisiana, and other states. But thecoypu fur craze and the demand for coypu meat eventuallycollapsed. Depending on the locale, and local stories vary, thecoypus either escaped on their own or were intentionally letloose by failed fur farmers in the late 1930s.

Coypus are now well-established in the United States, in-cluding key coastal states like Louisiana, Texas, and Mary-land. Without the predators, diseases, and other naturalfactors controlling their populations in South America, coy-pus are running amok in North America. Along Maryland’sChesapeake Bay, coypus gobble up patches of marsh plantsand accelerate the conversion of rich wetland habitats intoeroded ponds and bays. When not chewing up wetland veg-etation in Louisiana and Texas, coypus are attacking rice andsugarcane fields.

Attempts to turn coypus into gourmet fare have yet torekindle an interest in harvesting them for either their fur or

meat. In any event, trapping is not a feasible solution for theNorth American continent. Hopefully, humans will devise asolution that mitigates North American coypu wetland dam-age, which, like most mammalian invasive species problems,was created as a consequence of human activities.

Humans, the most successful invasive speciesThe magnitude of the invasive species problem in agricul-

tural and natural ecosystems prompted U. S. President BillClinton to organize the heads of eight federal agencies intothe National Invasive Species Council in 1999. Actually, hu-mans rank among the most successful invasive mammalspecies. Humans are believed to have spread from Africa toEurope and Asia over 100,000 years ago, and reached the is-land continent of Australia between 40,000 and 60,000 yearsago. But humans are apparently relative newcomers to theAmericas, having arrived between 15,000 and 20,000 yearsago. The human invasion did not reach many Pacific Oceanislands until 1,000 to 2,000 years ago. A small human pres-ence on the continent of Antarctica is a twentieth-centuryphenomenon.

Between 20 and 40 bird species have become extinct inNorth America over the past 11,000 years, a period when thepresence of humans is well documented and not controver-sial. Many of these bird species likely disappeared becausethey had narrow ecological niches dependent upon now ex-tinct large mammals like mammoths, mastodons, horses,tapirs, camels, and ground sloths. Human hunting likelyplayed a role in the extinction of large mammals like the mam-moth. But the magnitude of the prehistoric human role in ex-tinctions involves conjecture and is still being debated.

Several species of long-legged, flightless moas and an ea-gle, Harpagornis moorei, are among the birds possibly huntedto extinction by New Zealand’s first human inhabitants, theMaori. The loss of 62 endemic bird species in the HawaiianIslands is associated with the arrival of the first human in-habitants from Polynesia. In North America, more recent Eu-ropean immigrants hunted the passenger pigeon to death atthe end of the nineteenth century.

Rhinoceros species were hunted to the brink of extinctionfor their horns in Africa by the end of the twentieth century.Thanks to a new ecological consciousness sweeping theplanet, small rhino populations still exist in protected reservesat the start of the twenty-first century. Humans have also ex-tinguished species via habitat loss. This is among the prob-lems addressed in the United States by legislation like theEndangered Species Act of 1973.

Invasive mammal species seem to be most serious on iso-lated islands where the native organisms have not evolved de-fenses against the mammals common to the major continents.In Great Britain, an island close to mainland Europe, only22% of the mammal species are considered exotic. But onNew Zealand’s islands, which were only settled by humanswithin the last 2,000 years, 92% of the mammal species arerecent introductions. Indeed, New Zealand and some otherislands were free from mammalian predator pressure for solong that flightless bird species evolved.


Vol. 12: Mammals IMammals and humans: Mammalian invasives and pests

This Norway rat (Rattus norvegicus) shows how easily rats are able toboard ships and migrate from one area to another. (Photo by TomMcHugh/Photo Researchers, Inc. Reproduced by permission.)

In North America and the islands of the Pacific, othermammal species accompanied the human invasions. The firstAsians entering the Americas brought along dogs. When thePolynesians set sail for new Pacific islands, they brought alongtheir pigs, plants, and stowaways like lizards and rats. Euro-pean colonialism from the fifteenth to twentieth centuries wasa major driving force behind biological invasions of NorthAmerica, Australia, New Zealand, and other areas. Like theancient Polynesian voyagers, European colonists broughtalong their plants and animals to help settle these “newworlds.” Besides livestock like sheep, goats, cattle, pigs, andhorses, there were stowaway species like rats. Later, preda-tors like the mongoose were deliberately introduced to helpcontrol the rats.

Feral cats in AustraliaA good example of the pest/not-pest duality is the domes-

tic cat on the island continent of Australia. Between 4 millionand 18 million feral cats (Felis catus) live wild in Australia. Un-til recently most of these cats were believed to be descendantsof European cats brought to the continent in the late eigh-teenth century, with a few earlier arrivals via trading ships andshipwrecks. However, Australia’s aboriginal people regardcats as native. Genetic analysis indicates that Australian feralcats may have more in common with Asian than Europeancats, supporting the aboriginal view for an earlier arrival ofcats on the continent.

But the debate of more practical consequence is whetherferal cats threaten native species such as tammar wallabies(Macropus eugenii). If viewed as an invasive pest, then feral catsneed to be hunted down, poisoned, given birth control, orotherwise controlled. If viewed as beneficial predators help-ing control other pests such as rabbits, rats, and mice, thenferal cats should at least be tolerated.

In the late nineteenth century feral cats were viewed asbeneficial. Cats were deliberately acclimatized and releasedinto the Australian wild to hunt pestiferous (nuisance) Euro-pean rabbits (Oryctolagus cuniculus). Indeed, Australia’s RabbitNuisance Bill of 1883 supported releasing feral cats to helpcontrol rabbits that were damaging agricultural grazing lands.

But later in the twentieth century, feral cats were no longerwelcomed as rabbit killers. Feral cats began to be viewed asinvasive pests, threatening to native birds and mammals. Anti-cat forces pointed to the case of Marion Island, where fivedomestic cats released in 1949 had become a colony of over2,000 by 1975. The Marion Island feral cat colony was de-stroying nearly half a million burrowing petrels per year.

On the Australian continent and on Australian offshore is-lands, feral cats were blamed for the regional extinction ofseveral native bird and mammal species. The vanishing specieswere ground dwellers living in open habitats (favorable to cathunting) and were the right size to be cat prey. The anti-catforces also suspected that toxoplasmosis, a disease vectored bycats, may have played a role in mammal and carnivorous mar-supial population declines many years earlier.

Feral cats were suspects in Western Australia, where a redfox (Vulpes vulpes) removal program did not stop the popula-tion decline of native fauna. Feral cats were suspected of fill-ing the niche vacated by the red fox, and adding native speciesto their predominately rabbit and rodent diet. To determinewhether feral cat control is a necessary policy, researchers likeRobyn Molsher set up studies in New South Wales to eval-uate the ecological relationships among feral cats, red foxes,and other fauna.

Since feral cats are difficult to follow in the wild, their scats(fecal droppings) were analyzed for dietary clues. Rabbits werethe primary feral cat prey in New South Wales; rabbit re-mains were present in 82% of the scats and constituted over68% of scat volume. The majority of the other prey was car-rion, primarily sheep and eastern gray kangaroo (Macropus gi-ganteus). Even after rabbit populations plummeted followingapplication of a biological control agent known as Rabbit Cali-civirus Disease, rabbits remained the dominant prey of feralcats. Feral cats consumed more of the house mouse (Mus mus-culus) following the rabbit population decline.

Foxes and feral cats tracked via radio collars shared simi-lar habitats and prey. Foxes displayed aggression and killedsome of the feral cats competing for the same food resources.When foxes were present, feral cats ate mostly rabbits and leftthe carrion for the foxes. In fox removal experiments, feralcats ate more carrion and hunted more at night in the sameprey-rich grassland habitats favored by foxes.

Molsher concluded that integrated rabbit control pro-grams needed to also consider fox and cat control to preventnative fauna from becoming prey in the absence of rabbits.However, rabbits are so well established across such a vast



The hedgehog (Erinaceus europaeus) often invades hen houses to takeeggs. (Photo by Hans Reinhard/OKAPIA/Photo Researchers, Inc. Re-produced by permission.)

area that the goal of rabbit eradication in Australia has beenabandoned in favor of long-term population suppression. Thisseems to vindicate a continuing beneficial role for feral catsas rabbit and rodent predators in Australia.

Integrated rabbit controlProlific reproductive potential has helped the European

rabbit become a very successful invasive species. Originallyfrom North Africa, the European rabbit spread north throughItaly to the British Isles and then around the world, causingecological havoc in some countries. On the Hawaiian islandof Laysan, the rabbit is credited with wiping out 22 of 26 na-tive plant species at the beginning of the twentieth century.

Since its mid-nineteenth century introduction into Aus-tralia, the European rabbit has been a major plague. Vegeta-tion is grazed from vast stretches of land that become moredesert-like and less suitable for livestock grazing despite thekilling of millions of rabbits every year. Over a century afterstarting rabbit mitigation programs, Australia still spends anestimated $373 million per year on rabbit control.

Eradication is deemed feasible only on small islands or insmall localized areas where rabbit populations are newly es-tablished. The few small islands off the coast of Western Aus-tralia where rabbits have been eradicated are the exception,not the rule. More typical is 46 mi2 (120 km2) Macquarie Is-land and the main Australian continent, where rabbits are sowell-established that eradication has been replaced with themore realistic goal of population suppression.

Population suppression is accomplished using a suite ofvaried biological, mechanical, and chemical control tech-niques. This integrated pest management approach includespredators, microbial control agents, warren ripping, and elec-trified and wire-net fences. Wild rabbits are also hunted and

“harvested” as a commercial product. Barrel or soft catch trapsare still used against small isolated rabbit populations. (Hu-mane considerations have largely precluded continued use ofthe traditional steel-jawed leg-hold trap.) But rabbit popula-tions are so high and the species is so prolific that shootingand trapping have no significant impact on populations.

A variety of poisons and fumigants are still used againstferal rabbits, though safety, environmental, and humane con-cerns have been raised. The most widely used vertebrate con-trol pesticide is 1080 (sodium monofluoroacetate), which isformulated into paste, pellet, food cube, grain, and carcassbaits to poison animals such as rabbits, feral pigs, wallabies,wombats, dingos (wild dogs), possums, rats, mice, and foxes.Food chain risks are inherent in poison baiting, particularlywhen individuals lack baiting expertise. Another drawback isthat sheep, cattle, horses, goats, cats, dogs, some nativewildlife, and humans are also very susceptible to 1080, andthere is no known antidote to the poison.

Destroying warrens by ripping or plowing is a less con-troversial alternative to poisons, though the two techniquesare sometimes combined. Sometimes rabbit kill is maximizedby using dogs to drive rabbits into their warrens before bur-row destruction commences. But rocky areas, riversides, andsteep sandbanks with rabbit warrens are impossible to rip upand destroy, short of explosives.

In some locales rabbits prefer surface refugia rather thanwarrens. This means habitat management may be needed.However, the same shrub, blackberry, and log debris habitatsfavored by rabbits are also home to desirable species of birds,reptiles, amphibians, and other small mammals. So, it is notalways desirable to modify the habitat to fight rabbits.



A striped skunk (Mephitis mephitis) invades home garbage. (Photo byJoe McDonald. Bruce Coleman, Inc. Reproduced by permission.)

Common house rats (Rattus rattus) drinking milk in a temple in In-dia. Though often considered pests, some religions consider rats tobe holy. (Photo by M. Ranjit/Photo Researchers, Inc. Reproduced bypermission.)

Biological control using predators, parasites, or microbescan be part of integrated rabbit control programs and helpovercome the limitations of poisoning and habitat modifica-tion. One of the more famous instances of biological controlwas the introduction of the myxoma virus to fight rabbits.

Viruses for rabbit controlThe myxoma virus was imported into Australia in 1936,

and extensively studied before being released into the envi-ronment in 1950. The virulence of the myxoma virus is ratedon a scale of one to five, with one being most virulent. Theoriginal myxoma virus strain released into the environmentwas rated one, and provided a spectacular 99% rabbit mor-tality when first released into the environment in the early1950s. Without rabbits grazing on the landscape, the amountof forage available for sheep production soared and farmerswere very happy with the financial windfall.

But the spectacular success did not last. There is an eco-logical interaction over time involving the pathogenicity orvirulence of a microbe and the genetic suseptibility or im-munity of the host population. A microbe that is 100% suc-cessful in killing its host would go extinct along with itshost. So, ecological theory favors the evolution of a less vir-ulent microbe that does not kill the entire host population.Indeed, the evolution of reduced myxoma virus virulenceand increased rabbit immunity became a classic epidemio-logical case.

Over time the virus attenuated, and the virulence of fieldstrains of myxoma virus declined from one to three. At the

same time, the rabbit population developed greater immunityto myxoma virus. Releasing the highly virulent myxoma virusstrain rated one into the environment no longer produces the99% rabbit kill seen in the 1950s. At the end of the twenti-eth century, myxoma virus was producing a more sustainablerabbit kill of between 40% and 90%. This reduced rabbit killis still very important to integrated control programs. Indeed,in the absence of myxoma virus rabbit populations can stillsoar to very high levels.

In theory, integrated pest management can incorporatemultiple techniques, each providing a percentage of pest pop-ulation suppression. In practice, studies in both central andsouth Australia demonstrate the advantage of combining mul-tiple techniques into an integrated pest management programfor rabbits. When myxoma virus is used alone, as is typicallythe case, rabbit populations rebound to high levels in subse-quent years. However, when rabbit warrens are ripped orplowed after myxoma virus has already reduced the rabbitpopulation, the area can remain almost devoid of rabbits formany years.

Bolstered by the half century of continuing success withmyxoma virus, it has only been natural to look for additionalrabbit pathogens to introduce into the environment. In 1984Chinese scientists identified an acute infectious rabbit diseasecalled Rabbit Calicivirus Disease (RCD). RCD was subse-quently identified in Europe, Asia, Africa, and Mexico. Aus-tralia began studying RCD on wild and laboratory rabbits andnon-target species in 1991. Several months after a 1995 fieldtrial on South Australia’s Wardang Island, RCD was detectedon the mainland. In 1996, RCD was officially recognized as



The eastern mole (Scalopus aquaticus) eats helpful invertebrates suchas earthworms, which turn and aerate the soil. (Photo by L. L. Rue, III.Bruce Coleman Inc. Reproduced by permission.)

Brown rats converge at a garbage dump. Rats can spread diseasesthat affect livestock and people. In addition, they eat and/or contam-inate feed and their gnawing destroys buildings. (Photo by Jane Bur-ton. Bruce Coleman, Inc. Reproduced by permission.)

a biological control agent under the Commonwealth Biolog-ical Control Act.

In some parts of South Australia RCD has killed over 90%of the rabbits, and longer term rabbit populations are down17%. RCD has been spreading at the rate of 250 mi (400 km)per month. An insect vector traveling in the wind is believedresponsible for this rapid spread. However, humans and im-plements in contact with carrier rabbits may also spread thedisease. More time is still needed to see how well the combi-nation of myxoma virus and RCD work against rabbit popu-lations.

Less lethal fertility control agents, a humane solution fa-vored by animal welfare groups, are also under developmentfor rabbits, foxes, and mice. One idea is to engineer a viruslike the myxoma virus with an antigen causing animals toproduce antibodies that reduce fertility. An estimated 60%to 80% of female rabbits need to be stopped from breedingin order to reduce rabbit populations. Immunocontraceptionwill likely be tested on wild rabbits sometime before 2010.

Even if not wildly successful by themselves, new tech-niques like immunocontraception will likely play a role in in-tegrated pest management systems targeting rabbits andother pest mammals. It is clear from over a century of rab-bit control efforts that no single pest control technique byitself will work everywhere. Even myxoma virus, whichlooked so promising with its initial 99% rabbit control, is nolonger viewed as a stand-alone solution. The integrated pestmanagement paradigm of combining multiple control tech-niques and ecological principles is the wave of the future forcombating invasive pests.

Invaders in paradiseThe 6,393 mi2 (16,558 km2) Hawaiian Islands chain, a col-

lection of 132 islands, reefs, and small shoals, has only onenative land mammal species, the Hawaiian hoary bat (Lasiu-rus cinereus semotus). Thus, the Hawaiian Islands are a good“laboratory” for the studying the ecological effects of intro-duced mammals.

Even such usually ubiquitous land organisms as ants andmosquitoes were absent from the Hawaiian Islands’ nativefauna. For much of its geological history the world’s largestocean, the Pacific Ocean, acted like a giant moat, keeping theHawaiian Islands relatively isolated and deterring invadingspecies. The winds, ocean currents, and migrating birdsbrought species to the Hawaiian Islands, but very few becameestablished. On average over the last 70 million years, onlyone invading species per 35,000 years successfully establishedin the Hawaiian Islands.

However, a diverse topography, a warm tropical climateand an absence of predator species during most of the past 70million years made the Hawaiian Islands a good evolutionarylocale for new species formation via adaptive radiation. A spec-tacular example of new bird species formation by adaptive ra-diation in the Hawaiian Islands is the 54 species of Hawaiianhoneycreepers (Drepanididae). Compared to the Galápagos Is-lands and its 14 Galápagos finch species that inspired CharlesDarwin’s theory of evolution, the Hawaiian Islands have morehabitat diversity and a longer evolutionary history.

A mammalian invasion began transforming the Hawaiian Is-lands approximately A.D. 400, when the first Polynesian sailingcanoes arrived. The Polynesian voyagers brought animals and



The Mexican ground squirrel (Spermophilus mexicanus) destroys crops while foraging in the spring. (Photo by Anthony Mercieca/Photo Researchers,Inc. Reproduced by permission.)

plants with them, and changed the landscape with their agri-culture. New species in the Hawaiian Islands increased to threeto four per century after the Polynesians arrived, a huge increasefrom the pre-human one species per 35,000 year average.

Even before the Europeans arrived in the late eighteenthcentury, the Hawaiian Islands had a few hundred thousandpeople of Polynesian descent. The fauna introduced by hu-mans included the Polynesian (or Pacific) rat (Rattus exulans),dogs, pigs, fowl, and reptiles. The Polynesian rat is a nativeof Southeast Asia that spread across the Pacific Ocean islandsto the Hawaiian Islands with the Polynesians, but neverreached the mainland of the United States.

Polynesian rats attract a lot of attention as pests of plan-tation agricultural crops like sugarcane and pineapple, thougha broad range of crops are attacked. Polynesian rats are om-nivorous, and studies show adverse impacts on coastal treeand lizard species in New Zealand and on seabirds on severalPacific islands. There are little data available on Polynesianrat ecological effects on now extinct Hawaiian Island birds.

In the Hawaiian Islands, about half the land bird speciespredating human arrival have vanished. Direct human impactsfrom hunting and gathering and indirect human impacts are

strongly implicated in the decline or extinction of nativespecies, particularly flightless birds and ground-nestingwinged species. The magnitude of ancient human impacts onspecific species is still the subject of vigorous debate and in-quiry. However, there is little doubt that the rate of world-wide ecological change and species extinctions directly andindirectly attributable to human beings began increasing inrecent centuries.

The European ships of the eighteenth and nineteenth cen-turies brought exotic mammals from around the world to theHawaiian Islands, including new rat species, European piggenotypes, cattle, goats, sheep, the house mouse, and themongoose. Goats and cattle trampled and grazed native plantsand generally degraded habitats. Hawaii’s native bird speciessuffered additionally when early nineteenth century whalersintroduced the first mosquitoes and avian malaria. New dis-eases like smallpox and syphilis were transferred from the Eu-ropean arrivals to the Polynesian population. Clearly, as thetop mammal species, human impacts increased as human pop-ulations increased and spread.

Globalization and the expansion of ship and airplane com-merce in recent centuries accelerated the rate of new species



Raccoons (Procyon lotor) have adapted to urban living and thus become pests to humans. (Photo by Steve Maslowski/Photo Researchers, Inc.Reproduced by permission.)

introductions. When all the newly introduced plant and ani-mal species were added up, the rate of new species introduc-tions into the Hawaiian Islands was estimated to haveaccelerated to several dozen species per year in the twentiethcentury. Ecological upsets and pest problems from introducedmammals became more noticeable in the Hawaiian Islandsduring the nineteenth and twentieth centuries.

Black rats, also known as roof rats (Rattus rattus), and Nor-way rats (Rattus norvegicus) disembarked on Pacific islands asstowaways aboard European sailing ships and spread rapidlyin the nineteenth century. Norway rats and black rats are om-nivorous, attacking agricultural crops and feasting on theyoung and eggs of seabirds like petrels, shearwaters, gulls,terns, and tropicbirds.

Birds on isolated islands like New Zealand and Hawaiievolved in pre-human times when there was no need for de-fenses against mammalian predators like rats. Bird depreda-tions by rats are less common nearer the equator. Oneuntested hypothesis is that birds nearer the equator developedbetter predator defenses useful against rats, because of landcrabs preying on eggs and chicks.

Black rats are suspected in the demise of many nativeHawaiian birds during the nineteenth century. But the bio-

logical documentation from that period is not considered con-clusive by modern standards. Very recent technological ad-vances like night vision videos provide more conclusiveevidence. For example, night vision videos revealed beyonddoubt that black rats were a major predator of New Zealand’sendangered Rarotonga flycatcher (Pomarea dimidiata). Con-sequently, rat control became part of the program to save thatendangered forest bird species.

Mongooses for rat controlThe Indian mongoose, Herpestes auropunctatus, was deliber-

ately introduced into Pacific and Caribbean islands in the latenineteenth century for biological control of rats in plantationcrops like sugarcane. This was a rare attempt at biological con-trol by introducing a mammal to prey on another introducedmammal. One of the more colorful stories from the HawaiianIslands is that a man known as “Mongoose” Forbes sold mon-gooses to sugar plantations as rat catchers in the 1870s. Morescientific accounts suggest that the Indian mongoose was in-troduced to the Hawaiian Islands via the West Indies in theearly 1880s. Whatever the story, the deliberate introductionof the mongoose for rat control was a badly flawed idea.



Invasive animals damage local ecosystems. 1. Wooded area; 2. Wild pigs root and wallow in the wooded area; 3. The pigs uproot plants andleave the area open to erosion; 4. New growth in the disturbed area includes invasive plants such as briars, burs, and other species carried asseeds in the pigs’ manure. (Illustration by Wendy Baker)

1 2

3 4

1 2

3 4

Modern twentieth century biological control programsscreen potential introductions to make sure that desirableflora and fauna are not destroyed. This was not part of thescientific protocol in the nineteenth century when the mon-goose was introduced for rat control. Even though mongooseseat rodents in sugarcane fields, they do not provide adequaterat control. One problem is that the mongoose is a diurnalhunter, whereas the rats they were introduced to control arenocturnal. Also, mongooses do not stay put in agriculturalplantations. So there have been serious consequences for na-tive species in native ecosystems.

From the islands of Fiji to the Caribbean, mongooses arepredators of a wide range of native wildlife and a potentialreservoir for diseases like rabies and leptospirosis. Theground-nesting quail dove (Geotrygon mystacea) was nearlyeliminated from the Virgin Islands by mongoose predation.Hawaii’s endangered state bird, the nene or Hawaiian goose(Nesochen sandvicensis) is attacked by the mongoose, as are theendangered Hawaiian dark-rumped petrel (Pterodromaphaeopygia), Newell’s shearwater (Puffinus newelli), and theHawaiian crow (Corvus hawaiiensis). Turtles, native lizards,snakes, and poultry are also mongoose prey. Live traps, hunt-ing, and poison baits are among the mongoose control meth-ods available.

The bad experience with mongooses did not extinguishHawaii’s interest in biological control of rats. In the late1950s, Hawaii introduced barn owls (Tyto alba) for rodent bio-control. Even dogs have been used to hunt rodents in sugar-cane fields. Trapping tends to be too labor intensive for largeoutdoor areas with rats. Early in the twentieth century almost150,000 rats were trapped annually in Hawaii’s sugarcaneplantations with no noticeable effect on rat populations orcrop damage. Shooting is also of questionable value for ratcontrol. So, poison baits have been the fallback for keepingrat populations under control.

Feral pigsFeral European pigs, a late eighteenth century intro-

duction, may be the largest mammalian threat to native for-est ecosystems in the Hawaiian Islands. Feral pigs dig upyoung trees to eat the roots and spread weed seeds. Nativeplants and crops like sugarcane are attacked. From NewZealand to the Galápagos Islands, feral pigs also have a rep-utation for digging into burrows to consume seabirds likepetrels. Feral pigs also feast on the eggs and young of sur-face-nesting seabirds like boobies, shags, and albatrosses.

The original pot-bellied pigs introduced from Polynesiainto the Hawaiian Islands in the fourth century are smaller,more docile animals and a different genotype than the larger,much more aggressive European pigs. Polynesian pigs are alsoless inclined to roam and go feral, and are less of a threat tothe native ecosystems of the Hawaiian Islands.

Most popular accounts date the arrival of the Europeanpig genotype in the Hawaiian Islands to the arrival of Britishships under the command of Captain James Cook in 1778.Apparently the British were disappointed by the small sizeand tougher texture of the meat of the Polynesian pig, and so

introduced the larger, more succulent European pig to theHawaiian Islands.

In the nineteenth century, the introduction of newspecies was viewed as a positive and encouraged. Indeed,mid-nineteenth century advertisements exhorted sea cap-tains to import and release their favorite songbirds in theHawaiian Islands. Even in the mid-1800s, settlers in theHawaiian Islands noticed forest habitat destruction and na-tive bird losses, and felt that the introduction of their fa-vorite European species would help compensate. Nevermind that previous introductions like European pigs andgoats were among the culprits destroying the habitat. It wasan age when feral European species were welcomed byhunters, albeit opposed by agricultural interests sufferingcrop damage.

By the early twentieth century European pigs had com-pletely displaced Polynesian pigs in the wild, and an eradica-tion program was started because of feral pig damage to theHawaiian Islands’ native rainforests. By the mid-twentiethcentury, 170,000 feral pigs were killed. But feral pig popula-



The opossum (Didelphis virginiana) has adapted to life near humans,and has been known to raid hen houses and attics of homes. (Photoby Steve Maslowski/Photo Researchers, Inc. Reproduced by per-mission.)



tions were still trampling, uprooting, eating, and otherwisedestroying the Hawaiian Islands’ native ecosystems.

Though damage by goats, feral pigs, and other grazingmammals seemed obvious to observers, there was little quan-titative baseline data against which to measure the ecologicalimpacts. Near Thurston Lava Tube in Hawaii Volcanoes Na-tional Park, the National Park Service set up an experimentin which some forest plots were fenced to keep out feral pigs.Compared to unfenced plots where pigs roamed freely, fencedplots had fewer exotic plant species and more native plantspecies. Fenced plots also had less pig damage, as measuredby fewer exposed plant roots and less exposed soil. Not sur-prisingly, fencing is used as an integrated control measure tokeep pigs out of sensitive areas.

The National Park Service has also been following thespread of feral pigs from lower to higher elevations on theHawaiian island of Maui. Feral pigs were removed fromMaui’s Kipahulu Valley in the 1980s. Removing the pigs al-lowed the forest understory to recover and slowed the inva-sion of exotic plant species, a positive ecological outcome.Nonetheless, there has been opposition to using snares andhunting to remove the pigs. Indeed, one person’s invasivemammal pest may have redeeming positive qualities for an-other person. Hunting groups want the pigs to remain asgame, and some indigenous groups oppose eliminating thepigs for cultural reasons.

Pigs threaten foxesThe case for removing feral pigs (Sus scrofa), has less op-

position in the Channel Islands National Park and other is-lands off the coast of southern California. This is a casewhere one invasive exotic mammal species, the feral pig, haschanged the ecological relationships among several native

predators. On four islands, feral pigs introduced into theecosystem are indirectly leading to the extinction of foursubspecies of island fox (Urocyon littoralis), a tiny animalsmaller in size than a house cat. The smallest member of thefamily Canidae in North America, island foxes show littlefear of humans and were probably once kept as pets by Na-tive Americans.

There are no island foxes left in the wild on San Migueland Santa Rosa Islands, where captive breeding programs areaiming to save the island fox subspecies from extinction.Fewer than 200 island foxes are left on Santa Catalina Island,in part because of canine distemper virus vectored by domesticdogs. The island fox subspecies on Santa Cruz Island has seenits population decline from 1,300 to fewer than 100. The U. S. Fish and Wildlife Service proposed the four rare islandfox subspecies for protection under the Endangered SpeciesAct, and eliminating feral pigs from the Channel Islands ispart of the plan to save the island foxes.

Feral pigs and other introduced grazing mammals like rab-bits, sheep, goats, cattle, deer, elk, and horses contribute todegradation of the island habitat. The presence of feral pigsalso introduces an indirect ecosystem food chain effect con-tributing to the demise of the island fox. Feral pigs serve asprey, allowing golden eagle (Aquila chrysaetos) populations toflourish. Historically, golden eagles are a mainland speciesthat has neither bred nor overwintered on the islands. Theislands have historically been nesting grounds for the bald ea-gle (Haliaeetus leucocephalus), which preys mostly on marinemammals and fish.

Basically, the introduction of feral pigs allowed the goldeneagle, a mainland species, to become established on the is-lands. Unlike bald eagles, golden eagles prey on island foxes.One study found that with 90% golden eagle predation, is-land fox numbers declined to zero. Released from competi-tion with island foxes, island spotted skunk (Spilogale gracilisamphiala) populations also increase as an indirect consequenceof feral pigs supporting golden eagle populations. In otherwords, feral pigs feed the golden eagles which eat the foxeswhich frees up space for the skunks.

Golden eagle removal and relocation is part of the plan tosave the island fox and restore the ecosystem. However, satel-lite telemetry studies indicate that golden eagles relocated tothe mainland will try to return to the islands as long as feralpigs are available as a food source. Reintroduction of the baldeagle is also being considered to help restore the ecosystem.The bald eagle is very territorial, and may deter the goldeneagle from nesting. However, removing feral pigs as a foodsource is the more important factor in preventing reestab-lishment of golden eagle populations, restoring the ecosys-tem, and saving the island fox.

ConclusionThere are many more stories of invasive mammals to tell,

and more details untold about feral pigs, foxes, rabbits, cats,squirrels, rats, mice, horses, burros, and other invasive mam-mals than can easily fit on the printed page. But this overview

A house mouse (Mus musculus) raids a sack of seeds. (Photo byStephen Dalton/Photo Researchers, Inc. Reproduced by permission.)

of mammalian invasions contains many of the basic principlesneeded to better comprehend the plethora of media storieson invasive mammals.

Many of the invasive mammal examples have been fromislands, as scientists prefer to study the simplest possible fi-nite systems before venturing forth to tackle larger conti-nental problems. In other words, the island serves as alaboratory for studying invasions at their simplest. Even inAustralia, many rabbit control solutions were first tested onsmall islands to perfect them before introducing them to themainland continent.

The invasive mammal problems in some areas are likely togrow worse before they get better. But knowing that many ofthese invasive species are so successful in their new homes be-cause they left behind the predators, parasites, diseases, andother natural control factors that kept populations under con-trol in their native lands suggests one avenue of control.Namely searching the native lands of the pestiferous mam-mals for natural control factors that can be safely introducedelsewhere, like the myxomatosis virus introduced successfullyinto Australia for rabbit control.

However, if nothing else is learned, it is that great caremust be taken so that the cures introduced are not worse thanthe original invasive mammal problems, as was the case withthe introduction of the mongoose for rat control. Since hu-mans created most of the invasive mammal problems, it mightbe reasonable to expect that humans can collectively atone byresearching new solutions that minimize the possibility of eco-logical harm.

In the future, look for clever ecological manipulations ofpopulations, like on the Channel Islands, as well as more mol-

ecular, biotechnology solutions like immunocontraception forrabbits. But rather than expecting the newest technologicalsolution to be the ultimate answer, remember that organismscan and often do adapt, just as the rabbits in Australia builtup immunity to the myxomatosis virus and the virus attenu-ated over time.

If nothing else, the half century of experience with rabbitsin Australia points to the need for a control strategy inte-grating multiple techniques (like the myxomatosis virus plusripping rabbit warrens) to achieve the best and longest-last-ing results. Hopefully, the magic bullet approach of the pes-ticide era will be replaced with this more comprehensiveintegrated pest management approach.

However, the human side of the equation must never beforgotten when dealing with invasive mammals, as many ofthese animals in other non-pest contexts are highly valued.Hence, pestiferous feral cats, rabbits, wild horses, burros, pigs,and other mammals causing problems cannot be treated asthe object of extermination like cockroaches or termites.Every mammal seems to be loved by some group, be it huntersand indigenous people who favor wild pigs or animal rightsgroups who champion freedom for minks. Right or wrong,good or bad, these varied human sensibilities need to be takeninto account in designing any integrated pest managementprogram to control invasive mammals. For example, in thewestern United States, capturing wild horses and letting peo-ple adopt them has replaced the old practice of herding thehorses into canyons and shooting them. This type of solutionmay have more to do with politics or social science and con-sensus building than with biological or ecological principles,but ignoring the human species behind the invasive mammalproblems is to invite failure.



ResourcesBooksCrosby, Alfred. Ecological Imperialism: The Biological Expansion of

Europe, 900-1900. Cambridge: Cambridge University Press,1986.

Kirch, Patrick, and Terry Hunt. Historical Ecology in the PacificIslands: Prehistoric Environmental and Landscape Change. NewHaven, CT: Yale University Press, 1997.

Perrings, Charles, Mark Williamson, and Silvana Dalmazzone.The Economics of Biological Invasions. Northampton, MA:Edward Elgar Publishing, 2000.

Staples, George, and Robert Cowie. Hawaii’s Invasive Species: AGuide to the Invasive Alien Animals and Plants of the HawaiianIslands. Honolulu: Mutual Publishing and Bishop MuseumPress, 2001.

U.S. Congress, Office of Technology Assessment. HarmfulNon-Indigenous Species in the United States, OTA-F-565.Washington, DC: U.S. Government Printing Office, 1993.

Vitousek, Peter, et al. Biological Diversity and Ecosystem Functionon Islands. Heidelberg, Germany: Springer-Verlag, 1995.

PeriodicalsFlux, J. E. C. “Relative Effect of Cats, Myxomatosis,

Traditional Control, or Competitors in Removing RabbitsFrom Islands.” New Zealand Journal of Zoology 20 (1993):13–18.

Molsher, Robyn. “Trappability of feral cats (Felis catus) incentral New South Wales.” Wildlife Research 28 (2001):631–636.

Pimentel, David, et al. “Environmental and Economic CostsAssociated With Nonindigenous Species in the UnitedStates.” Bioscience 50 (2000): 53–65; 309–319.

Roemer, Gary W., et al. “Feral Pigs FacilitateHyperpredation by Golden Eagles and Indirectly Causethe Decline of the Island Fox.” Animal Conservation 4(2000): 307–318.

Joel H. Grossman


There are two general reasons for studying mammals inthe field. The first is to provide numbers that are needed forbiodiversity measures or population management; the secondis to provide natural history information that is needed to bet-ter understand species’ requirements or their roles within thenatural community. This chapter provides broad guidelinesthat would assist someone in selecting appropriate field tech-niques. References provided at the end of the chapter providemore details on both study design and specific techniques.

Biodiversity surveysBiodiversity measures are based on the ability to accurately

count the number of species within a given area and usuallysome measure of their relative or absolute abundance. Popu-lation management of both common and rare species relieson accurate measures of population numbers or at least a wayto measure population trends. Most mammal populations orcommunities are too complex for every individual to becounted, therefore a sample is often taken of the populationand the number is estimated based on that sample. Unfortu-nately, obtaining these estimates is not an easy task. Morethan other vertebrate groups, mammals occupy a wide arrayof habitats and possess a broad range of body sizes. These fac-tors make them difficult to survey as a group, and survey tech-niques have to be tailored for a specific species, or suite ofspecies. Planning a biodiversity survey is a two-step process:the first step is to determine the level of information neededto meet objectives, and the second step is to tailor a surveyto fit the attributes of the species.

Three levels of information that can be obtained from asurvey include a species list, a relative index of abundance foreach species, and an absolute density for each species. Gen-erally, there is increasing cost and complexity as the level ofinformation increases. For some mammal species, it is pro-hibitively expensive to estimate absolute density because ofthe habits of the mammal or the habitats it occupies. Solitarybats, which live in trees under strips of bark or in crevices,are a good example of a suite of species whose density esti-mate is logistically difficult to obtain. When planning a sur-vey, the first consideration should be how necessary theincreased information is to the management or research ob-jectives. The initial survey of a park would not start with a

density estimate of each mammal species, but rather a list ofspecies found in the park. Often a mammal’s relative densityis adequate information to track changes in abundance withina park, and the saved money can be used for other conserva-tion tasks such as patrolling. Within broad conservation plansfor an area, mammal surveys should reflect a nested subsetdesign. For example, following a complete species list for thearea, some species from this list are monitored through anabundance index, and select animals from this group are tar-geted for detailed population and ecology studies that mightinclude a density estimate.

If field technicians are working with a rare species or a har-vested species, they might not be concerned with the higherlevels of organization and start with a focal study on the tar-get species. However, even under these circumstances, an in-dex survey over a larger area may be more appropriate thana density estimate at one site. Project goals and financial lo-gistics usually produce a compromise in how much informa-tion can be gathered. It is important the data collected arenot stretched beyond their purpose, when compromises aremade. Unfortunately, the scientific literature is full of indexesused to calculate densities and species lists used as indexes.Surveys are powerful tools in wildlife conservation and man-agement, but when stretched beyond their ability they con-vey more confidence in the trends then the data warrant.

Species listSpecies lists can be as complex as a complete mammal sur-

vey or as simple as presence/absence of a focal species. Specieslists are composed through use of multiple means. Traditionalfield surveys that use traps, cameras, or transects can be sup-plemented by sociological techniques such as examination oflocal markets, discussions with local hunters, and inspectingkitchen remains in villages. When using traps or cameras, theyare usually placed in a line to traverse as many habitat typesas possible. The distance between the traps would be less thanthe smallest home range of the animal targeted. The largerthe home range, the longer the traps should remain in onespot in order to account for the time it takes an animal to tra-verse its entire home range. For a rodent, traps might be inplace for a few days; for a large predator, a few weeks wouldbe more appropriate.

• • • • •

Mammals and humans: Field techniques for studying mammals


Mammals and humans: Field techniques for studying mammalsVol. 12: Mammals I

Sociological techniques offer their own challenges, as thebarriers to an effective survey tend to be cultural rather thantechnological or biological. For example, who is interviewed,who does the interview, and even what dialect is used for theinterview all affect the survey results. There are strong cul-tural pressures on the interview process that are difficult tocomprehend or anticipate without extensive experience in thetarget community. Interview methods are effective for rela-tively large species that are regularly encountered or eaten bylocal people. Paying a bounty for local hunters to producespecific animals is tempting, but not recommended withoutconsideration of the long-term impact of creating a marketfor wildlife.

Creating a species list is an open-ended activity; the longerresearchers look, the more they find. A species accumulationcurve, which graphs the number of new species detected forevery additional unit of time or effort, can be used to gaugewhen a species list is complete. It should be noted that themethod used to measure the number of species may only pro-vide the number of species that can be detected.

Beyond the need to do a thorough survey, the most diffi-cult component of a species list is comparability. If lists areto be compared between areas or to lists collected previously,there must be a way to measure the amount of effort used inthe survey. Two biologists will not conduct surveys exactlythe same way, and differences in lists are always subject to in-dividual protocols.

Population indexPopulation indexes are usually species-specific and are

based on the number of animals, or their sign, detected foreach unit of effort. The effort can be measured in many ways,including number of miles/kilometers walked, number oftraps set, number of trees examined, or number of hours ob-served. The index itself is usually tied to specific traits of thespecies: for example, claw marks on trees made by Asiatic

black bears (Ursus thibetanus), calls by howler monkeys(Alouatta spp.), night nests of gorillas (Gorilla spp.), and la-trines of rhinos are indexes that are not broadly applicable toother species. Indexes based on sign are conducted along tran-sects of known length, with all sign within a set distance oftransect recorded, or a predetermined area is searched forsign. When interpreting signs, one must have observed howsuch signs are actually created by the animal, as well as whichactivities do not leave any signs at all (i.e., a deer feeding ondead leaves shed by trees or small bits and pieces of coniferbranches or lichen or small fruit leaves no trace at all). Whenthe signs are not permanent, such as fecal pellets or tracks,and the area is to be resurveyed at a later date, the bound-aries of the area can be marked and all sign cleared from thearea at the end of each survey. When traps or cameras areused during a survey, the measure of effort is usually expressedas trap-nights (or camera-nights). This is the number of traps(or cameras) set each night multiplied by the number ofnights. Using this criterion, a small number of traps used fora long period would be roughly equivalent to the effort of alarge number of traps used for a short period.

It is the rare index for which the number of signs can bedirectly converted into the number of animals. This is be-cause there are assumptions that must be used for each con-version. For instance, to convert the number of pellet groupsdetected to the number of deer, there must be estimates ofhow many pellet groups each deer produces daily and howrapidly the pellet groups degrade. Both these measures havea variance that is so large any resulting density estimate ismeaningless. For most indexes, it is also difficult to determineif increased signs indicate increased numbers or increased ac-tivity. For example, would the detection of six pellet groupsmean six deer used the area once, or that one deer used thearea six times?

As it is tailored to a specific species, a good index can bequantified and it is likely that two biologists can compare re-sults. The power of an index is to give relative comparisonsbetween sites or periods for a minimal amount of work. Someeffort must be made to verify that the index used reflectschanges in density over the range measured. There is also thedanger that an increased number of sign does not reflect moreanimals but rather shifts in habits such as diet or habitat. Onemust question whether seasonal increases in deer pellet groupsin an old field represent an increase in the number of deer ora shift in habitat use by the same number of deer. If all habi-tats are being monitored simultaneously, it is possible to dif-ferentiate between shifts in habitat use and shifts in abundance.

No index can work under all circumstances, so a pilot studythat measures both density and the index is preferable to mak-ing assumptions of correlation. Few indexes have a linear re-lationship with density over its entire range, as usually anindex flattens out as density increases beyond a certain range.For example, an increase in the number of subadult or non-reproductive individuals may not be reflected in an indexbased on the number of morning calls by adult howler mon-keys. It is important for the research or monitoring to demon-strate that the index is responsive to changes in density overthe range. For many species, verification of an index has al-ready been accomplished and a review of relevant literature

Researchers use low flying planes to do aerial surveys and to countanimals. (Photo by Rudi van Aarde. Reproduced by permission.)

is recommended before undertaking an index survey. In short,good preparation by observing animals is required before col-lecting data and making inferences from them.

Density estimate

Density estimates have two components, and both causedifficulties to biologists: the amount of area surveyed and thenumber of animals. As opposed to an index, the density esti-mate relies on a measure of area surveyed and not on effort.If the survey area is a true island, then the measurement isstraightforward. If the survey area has an arbitrary boundarybetween “inside” and “outside,” assumptions have to be madeas to how the animals move with respect to the boundary. Ifthe area surveyed is a mosaic of favorable and unfavorablehabitat for a species, sampling protocol must take this intoaccount. Placing survey lines to estimate the number of ani-mals within the favorable area while using both favorable andunfavorable habitat to estimate the survey area will overesti-mate the number of animals. Unfavorable habitat may notcontain a large number of animals during the survey, but maybe used at other times of the year or when environmental con-ditions change.

It is difficult to estimate density from a line of traps, as itis difficult to estimate the distance that animals are drawn intothe traps. Removal trapping suffers from this handicap, as re-moval of animals creates a vacuum that will eventually be filledby immigrating animals. Most studies that rely solely on trap-ping to estimate density construct trapping grids or webs toestimate the size of the survey area. Without prior knowledgeof an animal’s home range size and movements, it is difficultto accurately calculate the area sampled using most capturetechniques.

The second component of the density estimate is the num-ber of animals. To obtain a density estimate, a species usu-

ally needs to be observable or caught on a regular basis. Italso helps if natural or added markings allow individuals tobe identified. The two main techniques to estimate absolutedensity without changing the density are either mark/recap-ture or distance sampling. Mark/recapture uses an initial cap-ture period that results in a known number of marked animals.A second capture period then looks at the ratio of marked tounmarked animals and estimates how many animals the pop-ulation contains. Mark/recapture is based on the two as-sumptions that all animals can be captured and capture doesnot influence the probability of future captures and that ani-mals can be marked and the marks will not fall off or influ-ence the probability of the animal to be recaptured. There isalso an assumption that no mortality, natality, or immigrationoccurs between capture sessions, but it is possible to relax thisassumption and still estimate density.

For species that are readily captured, such as terrestrial ro-dents, it is a matter of trapping the animals in live-traps on aregular basis and estimating density. Commercial traps areavailable and techniques are well developed for small mam-mals. With all trapping, it is important to minimize trauma


Vol. 12: Mammals IMammals and humans: Field techniques for studying mammals

A biologist weighs a bear cub to record its weight. (Photo by © Ray-mond Gehman/Corbis. Reproduced by permission.)

A veterinarian examines a sedated chimpanzee (Pan troglodytes). (Photoby © Martin Harvey/Gallo Images/Corbis. Reproduced by permission.)



to the animal not just because it is humane but also so thatthe initial capture does not influence the probability of re-capturing the animal. When the intent is to recapture the an-imal, some period of pre-baiting (with the trap baited butlocked open) will increase the probability of capture. By pro-viding adequate food and bedding and checking traps regu-larly, most small mammals can be trapped repeatedly and theirdensity estimated. If the first priority is to ensure that allspecies have been detected, then using a variety of traps, bothlive and kill, would result in a better survey.

There is no terrestrial mammal that cannot be capturedand released in a humane manner. However, for many ani-mals such as large predators, the first trapping is traumaticenough to preclude the animal being recaptured by the samemethod. This does not necessarily preclude density estimates,as there is no assumption in the capture/recapture model thatthe capture method is the same for each period. The animalscan be captured with snares, affixed with a mark, and then re-captured by cameras at bait stations. The first capture can beas a neonatal in the nest, and the recapture in a trap. For in-stance, an animal’s DNA can be obtained in a blood sampleattained at the initial capture in a snare, and the DNA laterrecaptured in a hair sample snagged on barbed wire strungaround a bait station. If the animal has unique markings, asdo many large cats, both the initial capture and subsequentrecaptures can be with trip-cameras.

Removal sampling allows the observer to estimate a pop-ulation’s density post-hoc. The number of animals removedfor each unit of effort, or a change in the ratio of two classesof animals (i.e., antlered and antlerless deer), is the basis formost surveys of harvested large mammals. For both calcula-tions, the advantage is that the researcher is not necessarilythe one doing the removal. Large areas and large populationscan be estimated using volunteer hunters that agree to followsimple rules such as harvesting only antlered animals. Thedisadvantage is that there are limited species that attract alarge number of volunteer hunters and the removal is limitedto populations that are robust enough to sustain a harvest. Itis possible to use the catch-per-unit-effort technique without

harvesting animals, but the observer must be able to identifyanimals that have been previously sighted. There are severalstatistical programs that are commonly used to analyze thistype of data and details of the programs and their assump-tions are available at <http://www.cnr.colostate.edu/~gwhite/software.html>.

For animals that are readily observable, or at least easierto observe than catch, strip transects or distance samplingtechniques are used. In a strip sample, one counts all animalsalong a strip of known length and width. An assumption ofthis method is that all animals within the strip are counted.For most species, if the strip is wide enough to encounter asignificant number of animals it is also wide enough to missanimals at the boundaries of the strip. There are ways to es-timate the number of animals missed, such as double count-ing, but they do not solve the problem. Aerial surveys ofteninvolve strip samples where all animals within a strip along aside of the plane are counted by observers. These surveys arediurnal and usually occur in grassland or open habitats.Thermal imaging allows the heat signature of animals to beused to count animals at night. Use of thermal imaging for

Scientists study rodents as surrogates for assessing vegetation con-dition in conservation areas. (Photo by Rudi van Aarde. Reproduced bypermission.)

Scientists put a radio collar on a caribou (Rangifer tarandus). (Photoby © Natalie Fobes/Corbis. Reproduced by permission.)

density estimates is problematic because abiotic objects canradiate heat and be misidentified as animals. Also, canopy clo-sure in forest settings is often dense enough to block the sen-sor’s view of animals.

Distance sampling takes into account the assumption thatanimals can be missed along the transect, and the farther theanimal is from the transect the more likely it is to be missed.If the researchers know how far they surveyed, the numberof animals observed, and their perpendicular distance to thetransect line, they can estimate the area that they surveyedand the number of animals that they did not see within thatarea. The number of animals seen plus the number of ani-mals missed per unit area is a density estimate. The assump-tions are that all animals along the line are observed; animalsare randomly distributed relative to the line; and no animalsare counted twice along the same line. This technique wasoriginally developed to survey marine mammals, but hasquickly been adapted for many large terrestrial mammals.There are many nuances to distance sampling, and it is diffi-cult to cover them all in this space, but additional informa-tion is available <http://www.ruwpa.st-and.ac.uk/distance>.

Natural history informationBefore a species can be managed, it must be understood.

A species has requirements for food, shelter, and habitat thatdirectly impact management decisions. Understanding socialstructure, interspecific competition, predator pressures, move-ments, disease transmission, mating, and behavior help hu-mans realize the impact of their actions on mammals. Most,though not all, of these factors cannot be determined fromlaboratory studies of captive individuals. Effective means forstudying natural populations is a key ingredient to effectivemanagement of wild mammals.

Direct observationThe most straightforward means to derive natural history

information is direct observation. Its value should not be un-derestimated, as direct observation is often the most effectiveway to place the trait in context of the animal’s physical andsocial environment. The observer might be able to learn moreabout a species from a few hours of direct observation, thanfrom a year of examining trip-camera photos or radio teleme-try locations.

When designing a direct observation study, all terms mustbe understood and quantified, especially when more then oneobserver is used. The term “feeding” is readily understood ata basic level, but there are often many types and gradationsof feeding in a natural setting. As with village interviews usedto create a species list, the attitude and background of the ob-server sometimes influences how a behavior is recorded. Anobserver has to guard against anthropomorphic biases and alsoagainst interpreting events through preconceived theories.For example, which animal is considered dominant during aninteraction should not be a qualitative measure, but based onquantifiable criteria.

As with indexes, direct observations often have a unit ofeffort. How many attempted matings, bark strippings, or so-

cial grooming events observed is always a function of howmuch time was spent observing the animal. This is compli-cated when animals are part of a social group. Time spentmonitoring the entire group is not the same as time spent ob-serving one individual in the group. Usually too many activ-ities are being conducted simultaneously to watch an entiregroup and researchers identify focal individuals that are mon-itored for a set period of time. This set period of individualobservation might be punctuated by a sample of the behav-ior of each group member, referred to as a scan sample.

Direct observations are usually inexpensive; a good pair ofbinoculars or spotting scope and a watch are the main expenses.However, time is usually the limiting factor with direct ob-servations. Many hours can be spent to obtain a few minutesof direct observation. With more cryptic or more diffuse an-imals, there is a point at which the observations are not worththe time spent to obtain them. Video cameras and recordingequipment can be used to continuously monitor a location,with the tapes reviewed by the researcher at a later date; but



A research scientist funded by Conservation International to conductresearch in Madagascar on the elusive fossa (Cryptoprocta ferox).Fossa are trapped to gather information on their movement patternsand population sizes. (Photo by Rudi van Aarde. Reproduced by per-mission.)



this would only be effective at feeding or watering sites thatattract animals. In addition to time considerations, there is alsothe issue of how the observer’s presence impacts the animal’sbehavior and movements. If the behavior being recorded is theresult of the animal’s movements away from the observer, ortoward a concentrated food site, then the value of the obser-vation is reduced. A period of habituation of an individual orgroup to the observer is standard practice. But this needs tobe considered with some care. For instance, too much famil-iarity can trigger attacks, or habituated animals may be vul-nerable after the study is terminated.

Indirect observationsMany behaviors can be indirectly inferred from sign in-

dexes and density estimates. Habitat selection is often mea-sured through indexes that compare an animal’s use betweenhabitats or seasons. When indexes are used as a surrogate fordirect observations, the closer the index is to the target be-havior the less chance of error. For example, a browse indexbased on the number of buds clipped per tree is directly re-

lated to ungulate feeding, while pellet or track counts are moreindirect indexes.

Radio telemetry, a means of indirect observation, is themost important advance in the last 50 years for the study ofwild mammals. Before radio telemetry, researchers were lim-ited by their ability to follow animals or detect their presence.Indirect indexes of activity and movement, such as sign counts,were the best means to measure habitat selection. Behavioralobservations were often limited to sites near feeding or wa-tering holes where animals could be observed from establishedblinds; when an animal disappeared it was often impossible toknow if it had died, dispersed, or merely stopped coming tothe observation site. Radio telemetry allows a researcher tolocate a specific animal when it needs to be recaptured, ob-served, or its movements monitored. Radio telemetry allowsa researcher to remotely track a specific animal’s movementsand survival with a minimal disturbance to its behavior. Theseabilities have opened observations into animal ecology thatwere unavailable to earlier workers.

Two components of radio telemetry are the receiver andtransmitter. The receiver can pick up a range of frequenciesand can be set to detect each unique transmitter. Tradition-ally, the animal carries the transmitter and the receiver is ei-ther a hand-held device or an orbiting satellite. The hand-heldreceiver can be moved on foot, by car, boat, or plane. To lo-cate the animal, it can be approached directly, triangulatedfrom a number of bearings from known locations, or by us-ing the principles of the Doppler effect in the case of the satel-lite. More recent global positioning system (GPS) collars havethe animal fitted with the receiver and the transmitters areaboard orbiting satellites. The receiver calculates its positionbased on the known position of the satellites and the time ittakes a signal to travel between the satellite and receiver. Theoptimal arrangement is a package that contains a combina-tion of units, so the animal’s position can be determinedthrough multiple means.

Traditional tradeoffs in radio telemetry are between poweroutput and battery weight. Attempts to increase the range orduration of the signal are matched by increases in unit weight.Combining types of radio telemetry units into one collar alsoincreases package weight. A general rule is that a packageweight’s should be less than 5% of the animal’s body weight,but there are enough exceptions to this rule to warrant a pi-lot study before attaching packages to wild animals. Advancesin battery technology and computer software have madeweight considerations less important, especially for largermammals. When the battery power cannot be sustained forthe length of the project, microchips can regulate when theunit is active. Weight limitations are still serious concerns forspecies weighing less than 2.2 lb (1 kg).

A limitation of radio telemetry is that the observer mustcapture the animal to attach the telemetry unit. Most animalscan be captured, but the time and labor involved can consumea large part of a project’s budget. Once a telemetry unit is at-tached, the logistics of recovery are simpler. The telemetryunit can lead to the animal for application of anesthesia, or aremotely triggered tranquilizer dart can be inserted in the col-lar. When the study has terminated, the unit can be released,

Conservation scientist from South African national parks place a col-lar fitted with a GPS unit onto an elephant to study movement pat-terns. (Photo by Rudi van Aarde. Reproduced by permission.)

either by providing a weak link or a remote-release magneticmechanism in the collar.

Once locations have been collected for an animal, it is possi-ble to determine its home range, habitat use, and multiple othernatural history parameters. An additional benefit of radio-collared animals is the ability to construct life history tables.It is difficult to determine if wild animals have died or mi-grated when they stop being detected by other means. How-ever, which fate occurred is very important for most modelingof animal populations. With radio-collared animals, it is pos-sible to differentiate between mortality and migration, and todetermine the timing and cause of mortality.

LimitationsOf the two considerations when designing a field study,

the level of information needed and the limitations imposedby the animal itself, it is the latter that usually dictates whatis possible. When deciding the proper field technique, con-sideration has to be given to the size of the animal, its niche

(i.e., arboreal, volant, terrestrial, subterranean, aquatic), andits behavior (i.e., cryptic, nocturnal, social, vocal). Generalguidelines can be given to the limitations imposed by eachtype of mammal.

Large terrestrial mammalsVisible, large mammals can have density estimates derived

from distance sampling techniques. When large mammals arenot easily visible due to dense habitat, nocturnal activity, orlow density, they all leave sign that is observable and can beused as an index. Bears leave claw marks in trees, gorillas cre-ate nightly nests, elephants deposit conspicuous dung, and un-gulates leave tracks in most soils. Removal techniques aresuitable for large mammals that are harvested. Large animalsare also most easily captured with trip-cameras. Indeed, cam-era surveys of large predators are the norm in most foresthabitats. It is difficult to convert these camera indexes intodensity estimates, with the exception of animals with uniquemarkings that are surveyed using trip-cameras. Most largemammals have large home ranges, which make it difficult toestimate the area being sampled by any technique. Direct ob-servations are most frequently used with large mammals, andtelemetry units can be large enough to contain most featuresneeded. A limitation might be that the capture of the animalfor attachment of telemetry unit will take special skills andequipment.

Volant mammalsAll volant mammals are relatively small and most are noc-

turnal. The most readily surveyed are the communal speciesthat can be found in caves for all or part of their annual cy-cle. Bats can be counted in the roost, or individuals capturedwith nets, or counted visually when the bats enter or exit thecave. For bats with solitary roosts or to sample foraging sitesof communal species, nets that span natural passageways orwatering holes are the norm. However, it is difficult to erectmist-nets and harp-nets to match the space being used by the



A sonogram of a northern minke whale (Balaenoptera acutorostrata).(Photo by Flip Nicklin/Minden Pictures. Reproduced by permission.)

A game warden collects fluids from a dead elephant bull to determineits cause of death. (Photo by Rudi van Aarde. Reproduced by permis-sion.)



bats, particularly bats that forage above the canopy or withincomplex foliage.

Direct observation is usually not possible, especially dur-ing foraging. An exception is small light tags that can be placedon bats to observe short-distance foraging. It is possible toobserve maternal behavior in communal nesting species ei-ther directly or with video equipment. Radio telemetry unitsare just reaching the size where movements can be monitoredfor longer than a day, but weight is still a serious concern.

A technique with potential is using the bats’ ultrasonic callto identify species and possibly individuals. Devices can recordand catalog the calls to a computer where a number of callparameters can be measured. At this time, there are quantifi-able means to differentiate some, but not all bat species basedon call parameters. Usually the calls can be used to predictwhich suite of species generated the call, but not the exactspecies. There is individual variability in the calls and it maybe possible in the future to capture calls, as one would pic-tures of animals with unique markings. At this time, notenough call parameters can be measured to recommend use.

Aquatic mammalsAll are relatively large and most are cryptic, in that a good

portion of their time is spent below the surface of the water.Most marine mammals are too large for extensive trappingand are best surveyed with distance sampling, though trap-ping can be conducted on some dolphin, manatee, or otterspecies that inhabit coastal waters. Direct observations arelimited to the animal’s time above the surface of the water orusing scuba equipment. Radio telemetry can provide impor-tant movement data, but difficulties include the loss of sig-nals when the animal is below the surface of the water. Sonarcan be used to track movements and sounds of larger whales.

Freshwater mammals are generally smaller and more read-ily trapped. These mammals also usually spend some portionof their time on land and leave obvious sign such as gnaw-ing on trees or construction of homes, nests, and dams. Ra-dio telemetry and direct observations are more effective withthis group because of their time out of water. Small semi-aquatic insectivores are cryptic, difficult to capture, and leaveno observable signs. With this subgroup, neither direct observations or radio telemetry have proven effective. Theycan best be sampled with pitfalls or some form of kill trap.

Small terrestrial mammalsMost of these species are too cryptic to be observed reli-

ably, and live or kill trapping are the most common surveymeans. Traps can be obtained from several commercialsources and can be scaled to the size of the animal. Food baitsare used to lure animals into traps. If done properly, animalscan be captured repeatedly and all segments of the popula-tion can be sampled. Direct observation has not been effec-tive, with the exception of those species at the larger end ofthe range, such as ground squirrels. Radio telemetry units aresmall enough for most species, but the range of the small unitsis below the dispersal distance of most rodents and limits theirutility in some studies. For species less than 0.4 oz (12 g),most commercial traps are ineffective and radio transmittersare short-lasting due to weight considerations. Pitfall arraysare often used to record a species presence; pitfalls are buck-ets that are either deep enough that the animal cannot jumpout or are partially filled with liquid to kill the animal. Ani-mals are not lured into the buckets with bait, but rather bar-riers funnel all passing mammals into the buckets.

Subterranean mammalsAs with terrestrial small mammals, subterranean mammals

are cryptic, but unlike terrestrial small mammals they are usu-ally difficult to capture alive. Commercial killing traps can beobtained and modified to capture most species. Evidence of dig-ging activity can be used to indicate a species’ presence, butthese signs of activity are not often correlated with density andare a poor index. Some subterranean mammals have a portionof the year, or day, that they spend aboveground and this is theperiod during which they are most easily captured and surveyed.Direct observations and radio telemetry are ineffective becausethe soil blocks both sight and radio signal transmission.

Medium-sized mammals:Most can be captured in traps, but only a few can be cap-

tured repeatedly, either due to large home range or behav-

Researchers measure the head of a Tasmanian devil (Sarcophilus la-niarius) during a study in Australia. (Photo by © Penny Tweedie/Cor-bis. Reproduced by permission.)

ioral wariness. Traps are either large holding traps or snaresand leg-holds. Wariness prevents some species from readilyentering box traps. With proper training, snares with springsand leg-holds with padding can humanely capture animals forrelease. When animals are not captured, most are largeenough to be readily detected through tracks, sign, or cam-eras. For predators, animals can be attracted to specific siteswith food baits or scent lures, which, derived from glands orurine, are commercially available and can be used to bring an-imals over a site prepared for tracks or monitored with a trip-camera. These lures were originally developed for snare orleg-hold trapping and are still effectively used for that pur-pose. Radio telemetry is used extensively with this group; theunit is attached during the first capture.

Arboreal mammalsIt is difficult to capture arboreal mammals because of the

logistical complications in working in the canopy. As withsubterranean mammals, if arboreal species have a period ofthe day or year that they use the ground or come close tothe ground, they can most readily be sampled at that time.Sometimes species can be anesthetized with drugs deliveredin a dart, but still there is the problem of the animal fallingfrom the canopy when the drug takes affect. Diurnal speciescan be surveyed with distance sampling, or mark/recapture

techniques when there are unique markings. Nocturnalspecies are more difficult to survey visually because thedarkness increases their cryptic ability and there is difficultyin estimating distance; indexes can be derived from calls andvisual detections along transects. For nocturnal species, useof a spotlight to detect “eye-shine” makes transect surveysfeasible. Many species do have unique calls that can be usedfor index surveys. Radio telemetry can be used if the ani-mal can be captured. For animals that forage high in thecanopy, the utility of radio telemetry is diminished becauseit is difficult to estimate the third dimension in an animal’sspace use.

Clearly, one technique cannot be used to study all mam-mals. A study that attempts to record the density and behav-ior of all mammal species within an area has a daunting taskthat will take time and money to accomplish. A populationstudy for a single species or suite of species must be tailoredto match the habits and attributes of the animal. An advan-tage to mammal studies is that there is a rich literature ofmammal field research conducted over the past 100 years thatcan provide guidelines. With increasing human densities, theaffairs of mammals and humans can no longer be separated,and understanding wild mammals is the first step to ensuringtheir survival.



Resources

BooksBookhout, T. A., ed. Research and Management Techniques for

Wildlife and Habitats. 5th ed. Bethesda, MD: The WildlifeSociety, 1996.

Boitani, L., and Fuller, T. K., eds. Research Techniques inAnimal Ecology: Controversies and Consequences. New York:Columbia University Press, 2000.

Buckland, S. T., D. R. Anderson, K. P. Burnham, J. L. Laake,D. L. Borchers, and L. Thomas. Introduction to DistanceSampling—Estimating Abundance of Biological Populations.Oxford: Oxford University Press, 2001.

Elzinga, C., D. Salzer, J. Willoughby, and J. Gibbs. MonitoringPlant and Animal Populations. Oxford: Blackwell Publishing,2001.

Feinsinger, P. Designing Field Studies for BiodiversityConservation. Washington, DC: Island Press, 2001.

Laake, J. L., S. T. Buckland, D. R. Anderson, and K. P.Burnham. DISTANCE User’s Guide V2.1. Fort Collins, CO:

Colorado Cooperative Fish & Wildlife Research Unit,Colorado State University, 1994.

Southwood, T. R. E., and P. A. Henderson. Ecological Methods.3rd ed. Oxford: Blackwell Publishing, 2000.

Sutherland, W. J., ed. Ecological Census Techniques: A Handbook.Cambridge: Cambridge University Press, 1996.

White, G. C., and R. A. Garrott. Analysis of Radio-trackingData. New York: Academic Press, 1990.

Wilson, D. E., F. R. Cole, J. D. Nichols, R. Rudran, and M. S.Foster, eds. Measuring and Monitoring Biological Diversity:Standard Methods for Mammals. Washington, DC:Smithsonian Institution Press, 1996.

Periodicals

“Guidelines for the Capture, Handling, and Care of Mammalsas Approved by the American Society of Mammalogists.”Journal of Mammalogy 79 (1998): 1416–1431.

William J. McShea, PhD


A brief historyEvidence from cave wall drawings suggests that wild mam-

mals were kept in the company of humans as early as the StoneAge. In fact, this was probably the beginning of animal do-mestication. By 2500 B.C. Egyptian kings were keeping an-telopes for amusement and to impress foreign visitors. Onlyruling classes could afford to keep and care for exotic mam-mals. Queen Hatshepsut of Egypt could be credited with or-ganizing the first mixed collection of exotic mammals. Inapproximately 1500 B.C., she sent collectors to Somaliland.They imported greyhounds, monkeys, leopards, cattle, andthe first giraffe into captivity. In 1000 B.C., Emperor WuWang of China assembled the first zoological park. This wasa sophisticated 15,000 acre (6,070 ha) Ling-Yu or “Garden ofIntelligence.” It included tigers, rhinos, and rare giant pan-das. Between 1000 and 400 B.C., many small zoos were cre-ated in north Africa, India, and China and domestication ofmammals had become an art. These collections were mostlysymbols of power and wealth, definitely not for public en-joyment. By 400 B.C. the ancient Greeks established a zoo-logical garden in most if not all Greek cities. They used theircollections for serious scientific study. Only students andscholars were allowed to visit these collections. It was at thistime that Aristotle wrote The History of Animals. In this en-cyclopedia, he described hundreds of species of exotic verte-brates from these collections.

The Romans were perhaps the first to open exotic mam-mal collections to the public at large. From about 100 B.C. toA.D. 600 the Romans used these collections for scholarly studybut they also used many of these animals for entertainment.Much of the entertainment consisted of cruel and bloodyspectacles in public arenas, with large carnivores attacking orbeing attacked by men as well as other mammals. Often thesewere slow, agonizing and gruesome battles to the death. Withthe fall of the Roman Empire zoos went into a decline. Most exotic mammal collections consisted of small privatemenageries and traveling exhibitions.

By A.D. 1400 global exploration sparked public interest inzoos once again, with strange creatures from the New World.During this time, Hernando Cortes visited the zoo of Mon-tezuma, chief of the Aztecs. It was a huge collection and em-ployed over 300 zookeepers. Over the next few hundred years

many European zoos opened and the collections grew larger.Most of these collections consisted of individual specimens ofas many species of mammals as possible. The animals werefrom many different countries and represented many conti-nents. They were often called postage stamp collections. Theywere open to the public and attracted many visitors. Althoughthey have been renovated and have updated their policies,some of these zoos are still open today. The oldest is theSchonbrunn Zoo in Vienna, Austria. It was built in 1752 byEmperor Franz Josef for his wife. It opened to the public in1765. Others that still exist are the Madrid Zoo in Spain, whichopened in 1775 and the Jardin des Plantes collection in Pariswhich opened in 1793. For comparison, the oldest zoos in theUnited States are the Philadelphia Zoo, which opened in 1874;the Central Park Zoo in New York, which opened in 1862;the Lincoln Park Zoo in Chicago, which opened in 1868; andthe Cincinnati Zoo, which opened in 1875.

Why do we keep mammals in zoos?Zoos have been popular for centuries and this trend con-

tinues today. In an urban setting, a zoological park offers arare opportunity for visitors to view and learn about exoticmammals. This is the only type of opportunity many peoplehave in their lifetime to see living specimens in person. Manyof these mammals would be difficult and costly to see in thewild.

The goals of many zoos are the same. Usually they involveentertainment and education for the community they serve.Conservation and scientific research have also become majorconcerns for modern zoological parks. In an annual survey,the American Zoo and Aquarium Association reported thatalmost 135 million people visited 194 member facilities in2001. By comparison, this attendance is greater than all pro-fessional sporting events combined in the United States for2001.

EntertainmentEntertainment is a major goal for every public zoo. These

attendance numbers indicate that indeed zoos are fun to visit.There are many theories as to why people enjoy zoos. It couldbe that current human cultures feel isolated from nature andobserving exotic wildlife in zoos bridges a primal connection

• • • • •

Mammals and humans: Mammals in zoos


Vol. 12: Mammals IMammals and humans: Mammals in zoos

and meets our psychological needs. Mammals are certainlyinteresting to watch and their exotic shapes and colors appealto our artistic nature. The whimsical behavior of primates orthe grace and power of elephants, appeal to visitors of all agegroups.

Education

Perhaps the greatest service a zoo offers to the communityis education. Most zoos have programs that teach basic zool-ogy, animal behavior, geography, and natural history. Theclassroom setting sometimes involves safaris, campouts, scav-enger hunts, and participation in animal care. Usually stu-dents have the opportunity to observe, interact with, and oftentouch exotic mammals about which they are learning. Anotherunique educational and emotional experience is outreach pro-grams that target audiences unable to physically visit the zoo.Examples include the transport of education animals and staffto audiences in nursing homes or hospitals. Increasingly im-portant are programs teaching responsible use of habitat andconservation of natural resources. These programs often tar-get younger audiences, in an effort to sustain the long-termquality of life for all life forms.

Conservation

Zoological parks are becoming important conservation or-ganizations. They contain a large resource base in both stafftraining and fund raising. Thousands of staff members em-ployed by zoos participate in numerous in situ and ex situ con-servation projects worldwide. Some of these projects haveresulted in saving wild populations of mammals from certainextinction. Good examples of this are the golden lion tamarin(Leontopithecus rosalia) and Arabian oryx (Oryx leucoryx) pro-grams. Both wild populations lacked enough animals for longterm survival. A consortium of zoos working together movedand released captive born animals back into their historicalranges in hopes of re-establishing wild populations. Both ofthese re-introductions have succeeded and these now wildpopulations continue to reproduce and their numbers are in-creasing.

Scientific study

Zoos are often called “living laboratories”; this term rein-forces the fact that animal observations and experiments incaptivity can be very valuable. In fact, most of our knowledgeof mammals has come from captive studies. For instance,black-footed ferrets (Mustela nigripes), extinct in the wild, arebeing re-introduced through artificial insemination. The oryxhave also recently been poached to near extinction again andtheir numbers are just starting to increase in the wild. Also,it is often more practical, easier to control external factors,and more scientifically useful to study mammals in captivity.In an effort to encourage scientific study in zoological parksand provide funding for these programs, the American Zooand Aquarium Association and Disney’s Animal Kingdomhave established the Conservation Endowment Fund. It paysfor many conservation and research studies in captivity andin the wild each year. The Zoological Society of London inthe United Kingdom has supported research since the latenineteenth century.

Exhibit design conceptsEarly zoos consisted of numerous animals exhibited in

small cages made of concrete or wood with metal bars for se-curity. These were usually large charismatic mammals exhib-ited mainly for shock value. While a few zoos remain withthis type of exhibit design, the majority of modern zoo ex-hibits are one of two types. A third philosophy is included be-cause it could represent the future of mammal exhibits inzoological gardens.

The Hagenbeck conceptCarl Hagenbeck was an animal entrepreneur. He supplied

animals to zoos and was also an animal trainer. He pioneeredmany display and exhibit techniques. Hagenbeck initiallygained his reputation by exhibiting people and animals in trav-eling exhibits. On October 6, 1878 over 62,000 people visitedthe Berlin Zoo to see his traveling exhibit of Nubians fromthe Sudan, Laplanders, Eskimos, Kalmucks, Tierra del Fuegonatives, and Buddhist priests. There were also elephants,camels, giraffes, and rhinos, but it was the people who weremost popular. These human zoos made Hagenbeck a fortune.In 1900 he bought a potato farm on which he wanted to builda wild animal park. Hagenbeck is credited as being the inven-tor of the cage without bars. He put his animals in moated en-closures. The enclosures were planted with trees and shrubsand decorated with artificial rockwork which was very pleas-ing to the visitor and gave the illusion that the animals werefree-ranging. Their captivity was well hidden. Hagenbeck wasa master at the placement of moats and hedges to create anexhibit illusion that placed predator and prey together. He wasnot that concerned with scientific study or educating the au-dience, his priorities were aesthetics and beauty. These ex-hibits showcased large mammals with a geographic theme.Hagenbeck’s concepts are still used in exhibit design today.

Rehabilitation pools are built to temporarily house ill or injured marineanimals, such as this killer whale, for treatment. The intent is to returnthe animals to the wild once they have recovered. (Photo by © SteveStarr/Corbis. Reproduced by permission.)


Mammals and humans: Mammals in zoosVol. 12: Mammals I

Immersion conceptThis philosophy was an attempt to involve or place the vis-

itor in a naturalistic backdrop for a specific theme. These typesof exhibits are often characterized by paths that wind throughareas built to resemble natural habitat. Small mammals andbirds are sometimes free-ranging in the entire exhibit, in-cluding public areas. Species of similar geographic origin andhabitat are mixed in the exhibit, interacting with one anotherif they peacefully cohabitate. Larger mammals are housedwithin the same space, but for safety and function are enclosedwithin the exhibits with visually hidden barriers. Therefore,some of Hagenbeck’s techniques are used in immersion ex-hibits. The primary purpose of this exhibit is to give the vis-itor an appreciation of an animal’s natural habitat and educatethem on the natural history and need for conservation of thathabitat. One of the first good examples in the 1970s was thegorilla exhibit at Woodland Park Zoo in Seattle; more recentexamples of this technique can be found in the Congo exhibitat the Bronx Zoo and the Amazonia exhibit at the NationalZoo.

Biopark conceptThis technique is beginning to attract interest. The basic

idea is to create exhibits that explain, elucidate, and exemplifythe interconnectedness of life. More specifically, it is the idea

of putting humans and our biology in the context of the restof life. Robinson (1996) describes this technique as empha-sizing “the complex specializations in a host of dependencies,interdependencies and interactions with invertebrates, plants,protozoa, bacteria, viruses and so on to which mammals haveevolved.” He further states “it is time to end the isolationismof simply exhibiting mammals against a naturalistic back-drop.”

Management of captive mammal populations

Why manage zoo populations?Gone are the days of extensive collecting expeditions to

replace mammals that have died during transport or exhibi-tion. Zoos must now manage their captive populations to thefullest. It is no longer ecologically responsible or ethical tocapture wild mammals for the sole purpose of entertainment.In fact in 1992, 82% of the worldwide mammal populationliving in zoological parks was born in captivity, according todata collected in 2002 by the International Species Informa-tion System (ISIS).

When compared to wild mammal populations, most cap-tive populations are very small. Small populations tend to be

A zoo educator teaches children about endangered cats. (Photo by © James L. Amos/Corbis. Reproduced by permission.)

biologically unstable and their long-term survival is unlikelyif events occur at random. Genetically only one-half or 50%of a mammal’s alleles are passed to its offspring. Alleles aremutable genes that are responsible for inheritable traits.Therefore, genetic diversity is reduced by 50% with each gen-eration. In other words, the relatedness or mean-kinship ofthese individuals increases by 50% with each generation. Thisincrease in relatedness also increases the chance that allelesthat produce a fatal birth defect or reduced survivability willbe expressed. These are often called lethal genes. Demo-graphic factors also influence the long term survival of smallpopulations. If an excessively disproportionate number of fe-males or males occurs in a population, only a limited numberof animals will be represented in the population. This will re-sult in a reduction of genetic diversity and increased meankinship. This may eventually cause a small population to crashwithout the addition of new founders (genetically unrepre-sented animals in the population). Therefore, a populationwith a sex ratio that is nearly equal has a better long-termchance for survival. Age distribution in a small population isalso very important. If there is an excessively disproportion-ate number of older post-reproductive or younger pre-reproductive mammals in a population, reproduction will intensify in a single cycle and decline in a single cycle. With-out the addition of new founders, this will also reduce geneticdiversity and cause a small population to crash.

Frankham (1986) and Foose (1986) very eloquently docu-ment two extreme reasons for managing captive zoo popula-tions. Individuals are either intentionally selected to be well

adapted to captive environments, or they are managed to pre-serve genetic diversity.

Record keepingAnimal record keeping is the foundation of captive animal

management. Zoo professionals depend on detailed directionfrom animal records. Mammals with missing or unknown an-cestry or other life history information are of very limited usein long term management strategies. The InternationalSpecies Information System (ISIS), first developed in 1973,collects animal data from over 560 institutions in 72 coun-tries on 6 continents and stores them in a computerized data-base. These data are kept by a computerized program calledARKS (Animal Record Keeping System). Much of the dataare entered into a computer software program called SPARKS(Small Population Analysis and Record Keeping System) bya studbook keeper, in order to produce a studbook. A stud-book is an inventory of the life history and ancestry of an an-imal and SPARKS can perform mathematical analyses ofstudbook data. From SPARKS one can get age class and sexclass graphs as well as survivorship and mortality data for apopulation. It can also generate many useful reproductive



In some cases, orphaned or abandoned animals are taken to andraised at zoos. (Photo by © Carl & Ann Purcell/Corbis. Reproduced bypermission.)

Modern zoos try to recreate the animals’ natural environment, as withthis cheetah (Acinonyx jubatus) cub. (Photo by © Lynda Richardon/Corbis. Reproduced by permission.)



analyses. In order to formulate a population managementplan, SPARKS data are exported to a software program calledPM2000. This is a powerful computer program that can gen-erate, among other things, target population size, generationtime, growth rate, and current percent of genetic diversity. Italso allows the user to build preferred breeding pair calcula-tions, so recommendations can be made by the populationmanager.

Techniques for small population management

Incorporating profound knowledge and documentation ofgenetics and principles of population biology, Ballou andFoose (1996) describe specific guidelines for efficient demo-graphic and genetic management of small populations. Theseguidelines are used extensively by zoological gardens in an at-tempt to achieve long-term survival of small populations.Their basic techniques are summarized here.

FOUNDER REPRESENTATION

The long-term survival of a small population depends uponobtaining a sufficient number of founders to maximize allelicdiversity and heterozygosity. The goal here is to obtainenough unrepresented animals to build a population that willrepresent a cross-section of the genotype and phenotype ofthe source population. Unfortunately, one cannot predict thequality of the sample because it cannot immediately be mea-sured. Founder numbers are considered adequate for effec-tively sampling allelic diversity based on the most likely allele

distributions. Genetic variation over the range of the sourcepopulation should also be considered, with between 25 and50 founders considered sufficient in most cases.

REACH CARRYING CAPACITY

Carrying capacity in zoos is the entire number of spacesavailable for a particular species among all program partici-pants. In order to maximize genetic efficiency the populationsize should be increased as rapidly as possible in order to meetthe carrying capacity. Genetic diversity is lost when growthrates are slow, because the chances of all animals in that pop-ulation successfully reproducing and being represented in thefirst generation decreases with time.

STABILIZE THE POPULATION

The population should be stabilized once it is near the car-rying capacity. The current population size and growth rateare used to determine the proximity to carrying capacity andthe population is stabilized by regulating birth control. Birthcontrol of mammals in zoos is achieved both biologically andby the physical separation of animals.

EXTEND GENERATION LENGTH

Mean generation length is defined as the average age atwhich the females in a population produce offspring. Sincegenetic diversity is lost with each successive generation, ex-tending the generation length reduces the degree of diversitylost in a small population over a given number of years. Inother words, if the females in a population do not breed un-til later in life the loss of genetic diversity is delayed. Risk isincurred with this strategy since the animal’s reproductive po-tential may be lost with time, due to age related fertility prob-lems, health problems, and accidental injury or death.

ADJUST FOUNDER LINEAGES

In order to maximize the genetic diversity and survivabil-ity of a captive mammal population the representation offounder lineages should be as proportional as possible to thedistribution of founder alleles surviving in that living popu-lation. Initially in a captive population some animals will re-produce well and be highly represented genetically whileothers will not. Therefore, the population will not be evenlyrepresented genetically. In order to compensate for this, pref-erential breeding pairs should be formed. Descendants of un-derrepresented founders should be preferentially bred and thereproduction of overrepresented animals should be limited.

REDUCE THE REPRESENTATION OF EXTREME TRAITS

Reproduction should be limited in animals that producetraits that are not typical or that would offer a selective dis-advantage to survival in the natural environment. Albinism isan example of such a trait.

SUBDIVIDE THE POPULATION AND REGULATE GENEFLOW

Division of a large captive population into geographicallyisolated subunits offers some advantages. The exchange of an-imals as well as gametes between these subunits should beregulated. This method offers increased protection to the

This lar gibbon (Hylobates lar) takes advantage of the climbing systeminstalled in its zoo habitat to allow more natural behavior. (Photo by© Robert Holmes/Corbis. Reproduced by permission.)

population from communicable diseases and natural disasterssuch as fire, earthquake, tornado, and hurricanes. Also, iso-lated subunits of the population will be exposed to a widerrange of selective pressures. This offers the advantage of aslowed reduction of genetic diversity.

INTRODUCE NEW FOUNDERS

The addition of new founders should, in theory, increasegenetic diversity. If a program can be devised to exchangewild caught animals for captive born ones, this can sustain apopulation. However, great care must be taken to eliminatethe possibility of disease transfer between the populations.

INCORPORATE REPRODUCTIVE TECHNOLOGY

Emerging advances in reproductive technology can be usedto increase genetic diversity and sustain a captive population.Genetic material such as semen, ova, embryos, and tissues canbe stored and used at a latter date. This can increase thechances of a genetically underrepresented animal being uti-lized in a population. It can also increase the practical aspectof introducing new founders from wild populations. It is mucheasier and safer to move an animal’s gametes rather than tophysically transfer the entire animal.

Types of populations to manageFrankham (1986) documents four types of captive popula-

tions of interest to zoos. They are summarized in the follow-ing groups:

COMMON DISPLAY SPECIES

The goal for these species is to selectively breed for traitsadapted to captivity in an effort to establish a tractable, eas-ily managed population. This could include animals that aredocile and do not stress easily.

ENDANGERED SPECIES IN CAPTIVITY FOR LONG TERMCONSERVATION

The goal for these species is long-term maintenance of aviable population and the preservation of genetic diversity.Species of this designation require extensive genetic planningand captive management.

The North American gorilla population is one example. In2002 there were 361 animals in that population, of the 171potential founders, 111 are represented by living descendants.The population is doing very well, in fact 99% of genetic di-versity has been retained.

ENDANGERED SPECIES BEING PROPAGATED FORRELEASE INTO THE WILD

Reproduction for these species should be maximized forrapid population growth. Also, the captive environmentshould be as similar as possible to the natural environment inwhich the species is designated for release. External disrup-tion should be held to an absolute minimum.

The golden lion tamarin population is a classic example.This captive population has been overseen by an internationalcommittee since 1981. Nearly all of these animals are ownedby the Brazilian government. In 1990, the government of

Brazil gave the committee jurisdiction over the managementof both the wild and captive populations. Therefore, this com-mittee establishes policy for and manages the wild and cap-tive populations of golden lion tamarins by makingrecommendations to the Brazilian government. The com-mittee has no implementation authority but the governmenttends to accept its recommendations. As a result, the captivepopulation supplements the survival of the wild populationthrough reintroduction and management policy.

RARE SPECIES NOT CAPABLE OF SELF-SUSTAININGREPRODUCTION IN CAPTIVITY

Intensive efforts should be made with these species to de-velop successful husbandry and propagation techniques in or-der to achieve self-sustaining populations. When this isaccomplished, genetic diversity should be maximized in thecaptive population.



Zoos that promote breeding programs for rare or endangered animals,such as the giant panda (Ailuropoda melanoleuca), help to defendagainst the extinction of a species. (Photo by AP Photo/Xinhua, WuWei. Reproduced by permission.)



There are great advances being made in exotic mammalhusbandry as of this writing, but much work is still needed.The reproduction and birth of captive elephants is becominga major priority. Both the African (Loxodonta africana) and theAsian (Elephas maximus) populations are aging and withoutmore success both captive populations could be in trouble.Efforts are currently underway by numerous institutions toproduce captive born animals. The silky anteater (Cyclopes di-dactylus) is another animal that does poorly in captivity. Theaverage life span in captivity is approximately thirty days.Their has never been a silky anteater born in captivity. Thewild caught animals usually arrive very weak, dehydrated, mal-nourished, and heavily parasitized. Also, it is unclear if dietsused for other species of anteaters in captivity are sufficientfor silky anteaters.

Population management programsZoos worldwide have intensive conservation programs for

mammals. Although the names and acronyms vary by the ge-ographic region of zoo associations, their functions are verymuch the same. In North America, that plan is called the

Species Survival Plan (SSP), a copyright name and programimplemented in 1981 by the American Zoo and Aquarium As-sociation (AZA). The Species Survival Plan is defined as a co-operative breeding and conservation program designed tomaintain a genetically viable and demographically stable pop-ulation of a species in captivity and to organize zoo and aquar-ium-based efforts to preserve the species in captivity and innatural habitats. SSPs participate in a variety of other coop-erative conservation activities, such as research, public edu-cation, reintroduction, and field projects. Currently, 108 SSPscovering 159 individual species are administered by the AZA.

Most SSP species are endangered or threatened in the wild,or “flagship species.” These are well known animals thatarouse strong feelings in the public for their protection andthat of their habitat. For an animal to have an SSP there mustbe qualified professionals with time to dedicate to conserva-tion. Each SSP has a coordinator and management commit-tee. They use tools such as population management, scientificresearch, education, and reintroduction to formulate a mas-ter plan. This plan outlines the goals of the program, basedon what is most appropriate and attainable based on the cur-rent captive population.

Animal husbandryNo day at the zoo is the same as the previous; each day

brings new events and challenges. A rigid work schedule willnot survive. Disruptions and chaos are inevitable, requiringflexibility and an open mind. The management of zoo busi-ness and animal husbandry is in itself constantly evolving. In-ternal and external ideas from both local and global politicalgroups, scientists, the general public, and environmentalemergencies interact and contribute to change, while thehealth and biological status of animals determines the over-all degree of success.

Basic needs of mammalsThe basic needs of a mammal are food and shelter. A

zookeeper’s primary responsibility is to satisfy these basicneeds. However, their duties are usually much more complex,and with their daily responsibilities, a profound bond betweenhuman and the other mammal occurs. Early diagnosis ofhealth problems in the zoo population can often be done bysimply paying close attention to condition of the skin. Theskin should be free of rough areas or exposed tissue. The furshould also be somewhat silky and shiny rather than dry anddull in appearance. The health maintenance of elephants andrhinos is one example. The skin of an elephant or rhinocerosis a good indicator of their overall health. It should be free ofwounds and have a firm condition, a loose skin texture can beindicative of serious health problems. These animals are alsovery susceptible to foot problems. This is due to the fact thatthey do not walk as much in captivity as they do in the wild.Zookeepers provide all required health maintenance whilealso concerning themselves with the following subjects.

EnrichmentIn addition to physical needs, a captive mammal has psy-

chological needs that must be satisfied. “Enrichment” meansthe application of environmental stimuli in an attempt to cre-

A hamadryas baboon (Papio hamadryas) at the Phoenix Zoo in Phoenix,Arizona. Zoos attempt to educate the public about animals and theirhabitats. (Photo by G. C. Kelley/Photo Researchers, Inc. Reproducedby permission.)

ate psychological and physiological events that improve theoverall quality of life of an animal in captivity. Enrichmenthelps to overcome stereotypical and undesirable behavior, aswell as encourages mental and physical exercise in captivemammals. It usually involves adding novel items to an animalenclosure or providing visual or olfactory cues to a novel item.The desired behavior is curiosity or investigation, which re-sults in mental and physical stimulation or exercise. Zookeep-ers benefit from developing enrichment programs for thesame reasons. They stimulate themselves to rethink and re-duce the stagnancy of routines. In some facilities, visitors par-ticipate in enrichment as well. Many institutions have“enrichment days” in which the public participates in makingenrichment items. The safety and suitability of each item fora specific animal must always be the primary concern. For ex-ample, the Minnesota Zoo uses fir trees as enrichment tool.The animals love to investigate and move around them, andtear branches apart. Snowmen are also a popular enrichmentitem with many of the animals at this zoo. The bison love to

bash theirs, but the gibbons aren’t really sure what to do whensnow shows up in their enclosure.

The types of enrichment and the applications are limitless.Some groups of mammals have been documented to have spe-cific preferences. For example, exotic cats in captivity aredrawn to spices such as cinnamon, nutmeg, and paprika sprin-kled in their enclosures. Perfume sprayed on surfaces in theirenclosure also arouses their curiosity and excitement. Forother mammals, cardboard boxes and objects that they canroll are enjoyed. Enrichment can be used to elicit “natural”behaviors in captivity as well as improve overall physicalhealth through exercise. Food is also frequently used as anenrichment tool because it solicits the natural hunting andforaging behaviors of animals. Food with interesting texturesor new flavors, and food that is hidden in hard to reach places,all make good enrichment items. Many animals love “popsi-cles,” blocks of ice with food or bone inside. One of the Min-nesota Zoo tigers is reported to put her popsicles into thetiger pool to make the ice melt faster.

Health careMost facilities employ staff veterinarians who specialize in

exotic animal medicine. Zoological medicine has been iden-tified as a distinct and identifiable specialty of veterinary med-icine on the basis of academic programs in colleges ofveterinary medicine in the United States from the 1960s. In1972, the National Academy of Science committee on Vet-erinary Medical Research and Education first documented theneed for veterinarians specially trained to manage the healthof zoo animals. It is typical for each mammal within a zoopopulation to receive a routine health exam at least once ayear if they have no signs of illness. Care is provided as oftenas needed if health problems are suspected. Routine physicalsusually involve blood serum chemistry screening profiles, acomplete red blood cell and white blood cell count, x rays,



A gorilla (Gorilla gorilla) at the Frankfurt Zoo, Germany. The gorilla’snative habitiat has been reduced in size by human expansion. Survivalof the species is threatened, and zoos educate their visitors about theneed to protect animal environments. (Photo by BildarchivOkapia/Photo Researchers, Inc. Reproduced by permission.)

The thick glass allows these children to get extremely close to a bearat the Seattle Zoo. (Photo by © Mug Shots/Corbis. Reproduced bypermission.)



and dental cleanings. Appropriate vaccinations against life-threatening diseases are also given. A fecal analysis to checkfor the presence of parasites is usually performed every threemonths on each mammal in a zoo collection. In the event ofa serious illness, many zoos have access to and perform thesame advanced procedures on captive mammals as a humanwould being treated by a surgeon or other specialist. Veteri-narians depend on the input of zookeepers for evaluatingwhen an animal is sick and what would be the least stressfulmode of treatment.

TrainingTraining is another technique that zookeepers often use

to improve the quality of care of mammals in captivity. Al-though the term “training” probably conjures up images oftigers jumping through hoops of fire or elephants in ornatedress standing on their heads, training for the purpose of man-agement in modern zoological parks has a very different pur-pose. When an animal caregiver needs to get very close to,touch, or otherwise interact with a mammal, that specimenmust be conditioned to allow their presence. Target trainingis the method by which this conditioning behavior is learned.It can be a simple or complex program depending on thespecies and the training goal.

The training of mammals in zoos usually involves twotechniques. One is the theory of shaping. This involves theimmediate reinforcement of a desired behavior with somesort of reward to the animal. When a mammal receives pos-itive reinforcement for a particular behavior, it repeats thatbehavior. Shaping several small behaviors initially and thenforming them into a series, is the method by which a train-ing program is built. A second method often used is targettraining. In the simplest form a target is used to focus theanimal’s attention. The target is often a colorful ball on astick or a colorful card. When an animal touches the targetor performs the behavior that is required by the trainer, abridge occurs. The bridge is a form of non-verbal commu-nication and feedback between trainer and animal. Thebridge is usually a whistle, clicker, or other device that makesa sound that is audible to the animal being trained. Thebridge is often accompanied by a reward. Therefore, whenthe animal hears the bridge it knows it has performed thecorrect behavior and may get a reward. Training in zoos isvery helpful for captive management. An animal can betrained to position in a specified area or hold a stationary po-sition. This can allow a zookeeper or veterinarian to performa physical exam, and collect blood, as well as other medicalprocedures without the danger of anesthesia.

An Asian elephant (Elephas maximus) mud bathing in a zoo. Zoos provide opportunities for people to see animals that they would not typicallyhave a chance to see. Photo by Animals Animals ©Doug Wechsler. Reproduced by permission.)

Ethical considerationsKeeping wild mammals in captivity has been a controver-

sial issue since the industrial revolution created more timefor such interests. As late as the 1970s, most zoos kept speciesthat were easy to acquire at the time, in substandard condi-tions. Apes, monkeys, tigers, and bears were kept in concreteand steel cages reminiscent of prison cells. This outragedmany visitors. Animal welfare is a movement based on thedesire to reduce animal suffering and to minimize negativeimpacts that might result from human interactions. Theproblem with this philosophy is that to some degree it de-pends on humans being able to assess if they themselves arehaving a negative impact and are causing an animal to suf-fer. Suffering can be very subtle, occurring without humanshaving the capability for observation. The biology of a speciesmust be understood very well to make such a decision. Ani-mal rights is based on the philosophy that each individual an-imal has rights that morally should not be violated. Theproblem with this philosophy is that it focuses on the indi-vidual exclusively, and also requires a human judgment. Inother words, humans must decide on acceptable morals basedon human values not the values of each species being regu-

lated. These are very heavily debated subjects that will in-fluence the management of animals in captivity.

Future challengesToday, many animals and their habitats are threatened

with extinction. Most zoos use naturalistic habitats and putanimal welfare and conservation at the top of their duties.Ironically, captivity is the only hope for the survival in thewild of an always increasing number of species. Due to thisresponsibility accepted by zoos today, the famous author, nat-uralist, and zoo builder Gerald Durrell described them as “sta-tionary arks.” If the stationary ark is to remain in place, zoosmust continue to produce results in preserving the welfare ofcaptive and wild animal populations. Much of this work can-not be done within the perimeter gates of a zoo. Zoos musthouse and store healthy animal populations, and they mustalso give visitors instruction and direction on the mission soit will expand and move beyond the gates. Staff must also beactive in worldwide field missions to teach conservation mes-sages. A zoo must also be able to compete and have their voiceheard in the global political arena. Ironically, if zoos are suc-cessful enough, there will be no need for them.



ResourcesBooksBallou, J. D., and T. J. Foose, “Demographic and Genetic

Management of Captive Populations.” In Wild Mammals inCaptivity, Principles and Techniques, edited by D. Kleiman etal. Chicago: University of Chicago Press, 1996.

Coe, John C., et al. Keepers of the Kingdom, the New AmericanZoo. New York: Thomasson-Grant and Lickle, 1990.

Durrell, Gerald. The Stationary Ark. London: Collins, 1976.Hagenbeck, C. Beasts and Men. London: Longmans, Green,

and Company, 1909.Hancocks, D. A Different Nature: The Paradoxical World of Zoos

and Their Uncertain Future. Berkeley: University ofCalifornia Press, 2001.

Kleiman, Devra G., Mary E. Allen, Katerina V. Thompson,and Susan Lumpkin, eds. Wild Mammals in Captivity,Principles and Techniques. Chicago: University of ChicagoPress, 1996.

Norton, Bryan G., et al. Ethics on the Ark. Washington, DC:Smithsonian Institution Press, 1995.

Shepherdson, David J., Jill D. Mellen, and Michael Hutchins.Second Nature, Environmental Enrichment for Captive Animals.Washington, DC: Smithsonian Institution Press, 1998.

Tudge, Colin. Last Animals at the Zoo: How Mass ExtinctionMight Be Stopped. London: Hutchinson Radius, 1991.

PeriodicalsFoose, Thomas J., et al. “Propagation Plans.” Zoo Biology 5

(1986): 139–146

Frankham, R., H. Hemmer, O. A. Ryder, E. G. Cothran, M. E. Soule, N. D. Murray, and M. Snyder. “Selection inCaptive Populations.” Zoo Biology 5 (1986): 127–138

Hutchins, M. “Zoo and Aquarium Animal Management andConservation: Current Trends and Future Challenges.”International Zoo Yearbook 38 (2003): 14–28.

Hutchins, M. and W. G. Conway. “Beyond Noah’s Ark: TheEvolving Role of Modern Zoological Parks and Aquariumsin Field Conservation.” International Zoo Yearbook 34 (1995):84–97.

Hutchins, M., and B. Smith. “Characteristics of a World ClassZoo or Aquarium in the 21st Century.” International ZooYearbook 38 (2003): 130–141.

OrganizationsAmerican Zoo and Aquarium Association. 8403 Colesville

Road, Suite 710, Silver Spring, MD 20910 USA. Phone:(301) 562-0777. Fax: (301) 562-0888. Web site: <http://www.aza.org/>.

Center for Ecosystem Survival. 699 Mississippi Street, Suite106, San Francisco, 94107 USA. Phone: (415) 648-3392.Fax: (415) 648-3392. E-mail: [email protected]. Website: <http://www.savenature.org/>.

World Association of Zoos and Aquariums. PO Box 23,Liebefeld-Bern CH-3097 Switzerland. Website:<http://www.waza.org>.

Ken B. Naugher, BSc


We are living in an era of unprecedented loss in biodiver-sity. The most optimistic projections forecast the loss of sev-eral thousand species over the next few decades; less sanguineconservationists fear that almost a million species may vanishbefore the end of the present century. The earth has sufferedmass extinctions before, but the present episode is qualita-tively different for two reasons: first, it is extremely rapid; sec-ond, it is caused by one mammalian species, a large, primateof African origin. Ironically this creature has named itselfHomo sapiens, the Wise or Knowing Man.

The human activities that threaten wildlife and ecosystemsworldwide include deforestation, pollution, over-exploitationof native species, introduction of non-native species, acceler-ation of climatic changes, and spread of infectious diseases.The essential problem is that more and more people are us-ing more and more resources, leaving less and less for otheranimal species.

Threats to biodiversityFor more than 99% of its species history, H. sapiens ex-

isted in small groups of hunter-gathers, a highly intelligentprimate that learned to exploit virtually every terrestrial en-vironment that existed on Earth. About 8,000–12,000 yearsago, however, people largely ceased living within the con-straints of given ecosystems and became ecosystem-creators.The rise of agriculture drastically altered the earth’s carryingcapacity for H. sapiens, and human populations could increase.For several thousand years after our species became essen-tially an agricultural granivore, populations of H. sapiens wereheld in check by occasional famine and by the infectious dis-eases that co-evolved with densely packed agricultural hu-manity. However, beginning in the eighteenth century,scientific and technological advances led to increases in agri-cultural productivity and (temporary?) conquest of many in-fectious diseases. During the nineteenth and twentiethcenturies, human populations grew exponentially, expandingfrom approximately 1 billion in 1850 to about 6.3 billion inJuly 2003. Furthermore, at the same time that human popu-lations were increasing so dramatically, each person was, onaverage, using a greater portion of the world’s natural re-sources. As a result, Wise or Knowing Man has had a devas-tating impact on most natural systems throughout the world.

Humans dominate the global ecosystem in four primaryways:

• Direct transformation of about half the earth’s ice-freeland for human use. Houses, cities, roads, strip-mines,shopping malls, and highways involve obvious landtransformations. Even more surface area is occupiedby agricultural systems hostile to almost all living or-ganisms except the monocultural domesticates beingproduced for food or fiber.

• Alteration of the nutrient cycles within the world ecosys-tem. Globally, the release of nitrogen—through theconsumption of fossil fuels and use nitrogen-basedfertilizers—is the most critical, though introductionor extraction of other nutrients may be locally im-portant.

• Disruption of the atmospheric carbon cycle, particularlythrough the consumption of fossil fuels. This is the pri-mary cause of anthropogenic climate change.

• Introduction of pollutants into the world ecosystem. Tothis point pollution has had far less impact than thethree factors listed above. However, some scientistsbelieve that the accelerated release of pesticides, in-dustrial wastes, and other bioactive chemicals mayhave increasingly severe ecological consequences.Furthermore, in a world of economic inequality andpolitical instability, a massive infusion of nuclear pol-lutants is a possibility that should not be discounted.

Mammals at riskAlthough the least speciose of tetrapod classes, mammals

are also of particular interest to many people. Even if we leaveour own species aside, mammals dominate many terrestrialecosystems as well as some aquatic habitats. Mammals includethe largest animal the world has ever known, blue whales (Bal-aenoptera musculus). Mammals reside atop many food chains,comprise vital links in most terrestrial-vertebrate food webs,and consume primary or secondary production everywherethey occur. Furthermore, perhaps more than any other classof organisms, mammals are threatened by changes occurringat the hand of Wise or Knowing Man. World Conservation

• • • • •

Conservation


Vol. 12: Mammals IConservation

Union (IUCN) data from 2002 suggest that almost one infour mammalian species may be in danger of extinction withinthe foreseeable future.

When considering threats to biodiversity, we should re-member that different species face different threats, and many,if not most species, are menaced by multiple factors. For ex-ample, Miss Waldron’s red colobus (Procolobus badius wal-droni), an African monkey declared extinct in September 2000,suffered intensely from both deforestation and hunting forthe bushmeat trade. The black-footed ferret (Mustela nigripes)approached extinction because of habitat conversion, de-struction of its prey, and infectious diseases contracted fromdomestic animals. Sea otters (Enhydra lutris) were exploitedfor the fur trade and killed by fisherman who considered themcompetitors for shellfish. And presently, their recovery hasbeen slowed by depredations by killer whales (Orcinus orca).Despite the admitted complexity of extinction processes, wereview four principle threats to mammalian species: habitatdestruction, direct exploitation, introduction of exotics, andinfectious disease.

Habitat fragmentation and destructionDespite the potential importance of altered nutrient-cycles

and pollution, the primary immediate threat to biodiversity is

from habitat loss that results from expanding human popula-tions and their economic activities. Habitat loss includes out-right destruction as well as habitat disturbance due tofragmentation and localized pollution. In many areas of theworld including Europe, China, south and Southeast Asia,Madagascar, Oceania, and much of the United States, mostoriginal habitat has already been destroyed. Today the high-est annual deforestation rates are in developing and tropicalcountries, where a large proportion of the world’s biodiver-sity is found. The countries having the highest rates of de-forestation in the early twenty-first century are Costa Rica(3.0% annual loss of remaining forest cover), Thailand(2.6%), Vietnam (1.4%), Ghana (1.3%), Laos P.D.R. (1.2%),and Colombia (1.2%). Threats to savannas, grasslands, andfreshwater aquatic systems are less well documented, but theyare as important as deforestation—and, like deforestation, areconcentrated within economically poor countries that are richin biodiversity. This is a matter considered later in the pre-sent essay.

One typical result of environmental alteration is the isola-tion of habitat fragments, or patches. Fragmentation can re-duce or prohibit the dispersal of individuals, and local extinctionof some species becomes more likely. Later this essay consid-ers some consequences of habitat fragmentation.

Red wolves (Canis rufus) have been reintroduced into the wild by the Nature Conservancy in North Carolina, USA. (Photo by Stephen J. Krasemann/Photo Researchers, Inc. Reproduced by permission.)


ConservationVol. 12: Mammals I

Direct exploitation

Many of the world’s natural resources have been over-exploited. Some resources such as fossil fuels are non-renew-able, and the best we can do is to slow our depletion of theseimportant commodities. Other resources—such as water, tim-ber, and wildlife—are renewable, and, if used wisely, they maylast indefinitely. Unfortunately, people have often been careless about the conservation of renewable resources. Thegigantic Steller’s sea cow (Hydrodamalis gigas) was first en-countered by Europeans in 1741; 27 years later the last indi-vidual was killed. The near-extinction of American buffalo(Bison bison) is an example of over-exploitation known to mostU. S. school children. The last wild European cow (Bos tau-rus) was killed in Poland around 1630, and cattle-breeders stilldecry the loss of important genetic information. Similarly, to-day in Southeast Asia, at least three species of forest “cow” arein peril of extinction, and these are renewable resources thatcould still be preserved. During the early and mid-twentiethcentury, most species of baleen whales were hunted to the edgeof economic extinction. Belated protection has allowed speciessurvival, though recoveries have been slow. Great apes, suchas gorillas, chimpanzees, and bonobos, are being hunted to ex-tinction for commercial bushmeat in the equatorial forests ofwest and central Africa. In 2003, it is projected that some 2,000bushmeat hunters supported by the timber industry infra-

structure will illegally shoot and butcher over 3,000 gorillasand 4,000 chimpanzees.

Introduction of exoticsHumans have accidentally and intentionally introduced

species into new areas. In a sense, agricultural production it-self is a replacement of natural species by domesticatedspecies, under human control. Other examples also abound.Domestic cats (Felis catus) brought by Europeans to Australia,out-competed—or out ate—many small, native marsupials. Asmall, Australian marsupial (Trichosurus vulpecula, the brush-tail possum) was introduced into New Zealand in 1837. Thevarmint prospered beyond all expectations, threatening NewZealand’s fragile domestic wildlife.

Other familiar examples of unfortunate mammalian intro-ductions include rabbits and foxes into Australia; goats andcats into the Galápagos and Hawaii; rats, goats, and cats intoCuba and Hispaniola (pity the poor Solenodon); mongoose intoJamaica; hogs into too many parts of the southeastern UnitedStates; and horses in North America.

Infectious diseaseInfectious disease can spread across people, wildlife popu-

lations, and domesticated animals. Transmission of infectiousagents from domesticated species (e.g., dogs, cattle, water buf-

A small koala clings to the back of a German shepherd dog in a koala park near Brisbane, Australia. (Photo by © Kit Kittle/Corbis. Reproducedby permission.)

falo) to sympatric wildlife can result in a range of potentiallyfatal infectious diseases. Canine distemper virus is believed tohave caused several fatal epidemics among African wild dogs(Lycaon pictus), silverback jackals (Canis mesomelas), and bat-eared foxes (Otocyon megalotis) in the Serengeti. Populationsof African lions (Panthera leo) and cheetah (Acinonyx jubatus)have probably been affected by diseases transmitted from do-mestic cats. Problems of disease transmission from wildlife todomesticated animals and human beings may also be severe,but they are beyond the scope of this essay.

The nature of conservation biologyConservation biology is a multidisciplinary science whose

overall mission is to conserve biological diversity. The disci-pline can be subdivided into three primary areas: document-ing the world’s biodiversity; understanding the nature, causesand consequences of the loss of genetic diversity, populationsand species; and developing solutions for the preservation,restoration, and maintenance of biodiversity.

Three ecological postulates that underlie conservation bi-ology

Modern conservation biologists must often transcend thetraditional boundaries of academic disciplines, for these sci-entists increasingly need to know about politics, economics,philosophy, anthropology, and sociology in order maintain orrestore the health of ecosystems. However, because conser-vation biology is fundamentally concerned with the dynam-ics of wildlife populations, a solid understanding of biologyand ecology is paramount for workers within the discipline.Three ecological principles are fundamental for understand-ing the relationship between population dynamics and con-servation.

MANY ORGANISMS ARE THE PRODUCTS OFCOEVOLUTION

If most species in an ecosystem were generalists, then inthe absence of one generalist species, another generalistspecies would broaden its niche slightly, and the system wouldcontinue to function without important changes. However, ifspecies tend to be specialized, then they are not interchange-able parts in the system; when one is lost, the local ecologi-cal community may be affected. For the conservationbiologist, interdependent specialization is particularly impor-tant, and interdependent specialization often arises throughcoevolution.

Coevolution involves a series of reciprocal adaptive stepsduring which two or more interacting species respond to oneanother evolutionarily. A study of mammalian grazing ecol-ogy offers many classic examples of coevolution. Ruminantartiodactyls have evolved fermentation chambers that shelterlegions of microscopic flora and fauna. These microbial sym-biants extract the energy and nutrients they need from thevegetation consumed by the host-ruminant. In return, thegut-flora ferment cellulose, providing energy and repackag-ing nitrogen for their hosts. Grazing mammals, in turn, struc-ture the vegetative communities of their grassland habitats.Higher-order coevolution has been demonstrated among

species of grazing ungulates, particularly in Africa. Thomson’sgazelles, or “tommies” (Gazella thomsonii), for example, are sosmall that they cannot effectively exploit the tall grass thatgrows rapidly after the first rains of the wet season. So, justas other grazers depart the depleted grasslands surrounding arecovering waterhole, tommies move in to exploit the flushof tender, new grass. Eventually tommies disperse to exploitgrasslands grazed low by other ungulates (particularly zebra,Equus burchellii, and wildebeest, Connochaetes taurinus). Theseasonal ecology, anatomy, and gut flora of G. thomsoniievolved in response to the seasonal ecology of the larger un-gulates; without these other animals, populations of the littletommies would be much smaller indeed.

Some species, called keystone species, are especially im-portant for the interdependent functioning of an ecosystem.Keystone species may comprise only a small proportion of thetotal biomass of a given community and yet have fundamen-tal impacts on the community’s organization and survival. Theloss of such species may have dramatic and far-reaching con-sequences in the broader ecological community. Primates andbats are believed to play key roles in maintaining ecosystemsthrough dispersing seeds (some primates), pollinating plants(bats and some primates) and serving as prey items. The lossof these species from ecosystems would be predicted to havedeep impacts on ecosystem health. For example, throughoutmany areas in Trinidad, large mammalian species such as deer,



At the Animal Welfare and Conservation Organization in Okonjima,Namibia, lions are encouraged to play to help stay fit. (Photo by NigelJ. Dennis/Photo Researchers, Inc. Repoduced by permission.)



paca, agouti, and peccaries have been extirpated—and yet theecosystems still remain functional. On the other hand, withinthese ecosystems, Trinidad’s bat and primate populations maybe fulfilling ecological roles for which few other occupantsremain. Thus the monkeys and bats may now be keystonespecies, whose presence is vital to the now-fragile existenceof the Trinidad ecosystems. Similarly, in pre-European SouthCarolina, cougars (Felis concolor) and a large, social canid (Ca-nis sp.) structured the forest herbivores. Now, in the absenceof these top predators, whitetail deer (Odocoileus virginianus)obliterate populations of several species of forest herb.

IN ECOLOGICAL SYSTEMS SOME CRITICAL VARIABLESHAVE THRESHOLD LEVELS

Changes in one of these variables may make very littledifference in ecosystem operation—until a threshold iscrossed, and then dramatic systems-alterations will occur.The mathematical study of nonlinear “threshold relation-ships” is the province of bifurcation theory, which has beenused to model catastrophic phenomena ranging from do-mestic violence to human heart failure. Many conservationbiologists emphasize a particular corollary of this generalthreshold postulate: some ecological processes may suddenlyfail when the landscape patch in which they operate is re-duced below a threshold size.

Biologist-activist Paul R. Ehrlich has written several bookson ecology and conservation, a recent one is A World ofWounds: Ecologists and the Human Dilemma, Ecology Institute,Oldendorf-Luhe, 1997. He illustrated potential dangers ofecological non-linearities by the following metaphor. Pretendthat the world ecological system is an aircraft and that specieswithin the system are rivets holding the aircraft together. Ifone or two rivets are lost, the aircraft continues to fly as ifnothing had happened. More rivets are lost and the airplanestill flies. But eventually the loss of “just one more rivet” maybring the flight to a sudden, disastrous end.

GENETIC AND DEMOGRAPHIC SYSTEMS HAVETHRESHOLDS

Like ecological systems, genetic and demographic systemscan be nonlinear and have thresholds below which nonadap-tive, random processes begin to displace adaptive, “statisti-cally deterministic” processes.

One example of this is the loss of alleles in small popula-tions because of genetic “drift.” Another is the extinction ofa small population through random binomial processes. Thispoint can be illustrated by an extreme demographic example.Consider a hypothetical species that does not breed duringthe dry season and suffers high dry-season mortality. Morespecifically, assume that each female entering the dry seasonhas a 50% probability of surviving until the end of the dryseason. Now consider the probable fates of two different pop-ulations:

• 10,000 females enter the dry season. The chances areabout 95% that the population at the end of the dryseason will include 4900 to 5100 females. In otherwords, the chances of population extinction are al-most exactly 0%. (These statements can be demon-strated by an approximation of the binomialtheorem.)

• Two females enter the dry season. The chances areabout 25% that the population at the end of the dryseason will include 0 females. In other words, thechances of extinction for this small population areabout 1 in 4.

Conservation biology and three value statementsThe three ecological principles listed above form part of

the biological foundation for the discipline of conservationbiology. In addition, many conservation biologists acceptthree value statements—which by their very nature are notsubject to scientific confirmation or disproof. In other words,conservation biology is inherently a value-laden discipline,and the following assumptions of worth define the ethical po-sitions of many conservation biologists.

DIVERSITY OF ORGANISMS IS ASSUMED TO BE GOOD

Whenever possible conservation biologists defend diver-sity on utilitarian grounds—and make statements like, “Somelittle tropical plant may contain a cure for cancer.” Further-more, evidence exists that biological diversity within anecosystem contributes to the ecosystem’s persistence, stabil-ity, and productivity. Nevertheless, even without utilitariansupport, many conservation biologists would assume that di-

An African wild cat (Felis libyca) in the Kalahari Gemsbok Park, SouthAfrica. Game preserves have been established to provide natural habi-tats for wild animals. (Photo by Animals Animals ©Ingrid Van Den Berg.Reproduced by permission.)

versity is good in itself (an sich, as the German philosophersused to write) and therefore needs no means-toward-an-endjustification. This assumption of intrinsic value is beautifullyexpressed by Archie Carr in his book Ulendo: Travels of a Nat-uralist in and out of Africa.

As a corollary to this value principle, most conservation bi-ologists believe untimely extinctions (in general, defined asextinctions that result from human activities as opposed to ex-tinctions that result from natural processes) should be pre-vented. Most conservation biologists also believe that localbiodiversity is a universal good. Thus if desperately poorMadagascar cannot afford to protect the 50 endangered andvulnerable species living within her borders, then perhapswealthy nations (or individuals) are morally obligated to as-sist with this conservation enterprise. This idea is returned tolater in the present essay.

ECOLOGICAL COMPLEXITY IS ASSUMED TO BE GOOD

Clearly this is related to the first value principle above,but it is not exactly the same thing. Consider, for example,a botanical garden with its specimen trees and its green-houses. Such an installation might contain more differentspecies than a tropical rainforest (and thus would satisfy theprinciple that “diversity of organisms is good”), but it wouldnot manifest the complex web of inter-organism relationshipsthat characterize a tropical rainforest. The conservation bi-ologist would likely prefer the rainforest to the botanical gar-den. Or consider this value principle in the form of aquestion. Some authorities believe that fewer than 1,000species of large mammals can be preserved from extinctiononly in captivity. Will a typical conservation biologist becompletely satisfied if these mammals survive only in zoos?

EVOLUTION IS ASSUMED TO BE GOOD

The diversity of organisms and the ecological complexi-ties of their interrelations are products of evolution. Mostconservation biologists affirm not only the value of the prod-uct but also the value of the process that made it. Let us seehow this value principle might affect the political agenda ofa conservation biologist. What if the wildlife-refuge systemsof the world were sufficiently extensive to preserve every liv-ing species: would the conservation biologist be satisfied ifrefuges were not large and diverse enough to allow contin-ued speciation (evolution)?

What areas are the most important topreserve?

Questions of “conservation triage” are difficult, but theymust be faced in a world of limited support for conservationagendas. Faced with this problem, British ecologist NormanMyers devised the concept of biological “hotspots,” which hedefined as regions particularly rich in endemic species and im-mediately threatened by habitat destruction. Myers is the au-thor of 17 books on the environment, among them Gaia: AnAtlas of Planet Management, 1993. Myers listed 25 particularlyimportant hotspots, which total only 1.4% of the earth’s landsurface, but contain 44% of all plant species and 35% of allterrestrial vertebrate species. The Indo-Burma hotspot covers

approximately 795,000 mi2 (2,060,000 km2) in south andSoutheast Asia, and is home to such threatened species as tigers(Panthera tigris), red-shanked douc langurs (Pygathrix nemaeus),Sumatran and Javan rhinoceros (Dicerorhinus sumatrensis andRhinoceros sondaicus), and Eld’s deer (Cervus eldi). However,only 61,780 mi2 (160,000 km2), or 7.8% of the total area, isprotected. Myers’s favored strategy would be for conservationorganizations to focus their efforts for fundraising and biodi-versity conservation upon these areas, and such organizationsas Conservation International and the MacArthur Foundationnow largely subscribe to the hotspot approach.

However popular it may become, hotspot triage is notwithout its problems and detractors. For example, some read-ers may be surprised to learn that rainforests in the Amazonand Congo Basins do not make the magic Top-25. These ar-eas, of course, are rich in endemic species—but they main-tain over 75% of their forest cover and are in no immediatedanger of complete destruction. Hotspot advocates would ar-gue, “We should spend scarce dollars on species-rich real es-tate that’s about to be destroyed.” Opponents might reply,“I’d rather spend scarce dollars on species-rich Amazoniawhile I can still afford a really big chunk of it.”

Regardless of her or his affection for (or disaffection with)hotspot triage, any mammalogist concerned with long-termconservation should become familiar with the types of habi-tats most important to mammalian diversity and most severelythreatened with destruction. Such habits include tropical rain-forests, tropical deciduous forests, grasslands, mangroves, andaquatic habitats.

During the 1980s and 1990s, tropical rainforests capturedan increasing share of public attention. Rainforests cover lessthan 2% of the earth’s surface, yet they are home to over 40%of all macroscopic life forms on our planet—as many as 30million species of plants and animals. Rainforests are quitesimply the richest, oldest, most productive, and most com-plex ecosystems on Earth. Furthermore, many of them, par-ticularly in Asia and Oceania, are increasingly threatened bydestruction.



An ecotourist sits watching a highly endangered baby mountain gorilla(Gorilla beringei beringei) as it rolls on its back over flattened shrub-bery. (Photo by © Staffan Widstrand/Corbis. Reproduced by permis-sion.)



Because they are more amenable to sedentary agriculture,some tropical deciduous forests are even more severely threat-ened than rainforests. Tropical savannas, with their magnifi-cent relics of the Pleistocene mammalian megafauna, areeasily converted into pasturelands—and unspoiled tropical sa-vannas scarcely exist at all outside of formal National Parks.Mangroves, which shelter a number of important mammalianspecies, such as proboscis monkeys (Nasalis larvatus), arethreatened by pollution, conversion for intensive aquaculture,and destruction for firewood. Lakes, rivers, estuaries, sea-coasts, and other aquatic habitats are also under increasingthreats of multiple dimensions.

A problem faced by most conservation biologists work-ing in the international arena is that countries with the high-est degree of biodiversity (and this is particularly true forthreatened and endangered mammals) are usually the coun-tries least able to afford the conservation of their natural re-sources. For example, in some areas the median per capitaincome is less than $1US per day. People living under theseconditions often consider conservation to be an unafford-able luxury.

Of course conservation biologists have long recognizedthat the futures of tropical peoples and of tropical wildlifeare inextricably mixed. And for more than a decade almost

all conservation action plans have emphasized the fact thatlocal people should have an economic stake in the pro-tection of their wild resources. Zimbabwe’s “Campfire”program provides a classic example of the local benefit phi-losophy in action. Village councils were given authority tomanage wildlife resources. Then, for example, when Eu-ropeans or Americans came to Zimbabwe to kill elephants,the villages could profit from the substantial expendi-tures of the wealthy hunters. Unfortunately, Campfire (andrelated “eco tourism” plans) is selling a high dollar luxuryactivity—which is at the mercy of international marketforces and local interference. International economicdownturns or national instability (both of which have be-set Campfire) can undermine value-added conservationprograms.

Under some circumstances sustained-yield harvest pro-grams that return valued wild products directly to local userscan be successful. Nevertheless, among people who are des-perately poor, the odds against such programs are high. Manyimpoverished people naturally think of wild mammals asmeat—not as an abstract food-resource to be harvested on along-term, sustained-yield basis but as meat, now, for chil-dren who will otherwise be far too hungry before nightfall.The sale of bushmeat is rapidly becoming a substantial sourceof income, as well.

An entangled northern fur seal (Callorhinus ursinus) is held down by an Aleut teen and seal biologist to remove fishnet that would kill the ani-mal. (Photo by YVA Momatiuk & John Eastcott/Photo Reserachers, Inc. Reproduced by permission.)

Because many conservation biologists believe that local bio-diversity is a universal good, some argue that wealthier nations(and individuals) have a moral duty to assist poorer nations inconserving humanity’s general biodiversity heritage. Even ifone subscribes to this idea, it is difficult to determine (partic-ularly on personal, financial levels) the degree of sacrifice thatis morally obligatory. Furthermore, in recognizing that severepoverty threatens conservation, there are two more funda-mental facts:

• First, severe poverty is in part a function of inequal-ity. In 2003 the United States contains about 5% ofthe world’s people—but is responsible for 30% ofthe world’s resource-consumption. It is difficult forAmericans to preach conservation to the rest of theworld until the United States begins to clean up itsown house.

• Second, severe poverty is in part a function of pop-ulation-size. If the economic “pie” is finite in size,then even if the pie were equitably shared, “morepeople” would mean “smaller pieces per capita.” Atsome point, population control becomes a prerequi-site to effective conservation policy.

Conservation biology, habitat fragmentation,and island biogeography

The theory of island biogeography was formulated to ex-plain how rates of colonization and extinction affects speciesdiversity observed on actual islands. Currently, protected ar-eas (such as national parks, to which many threatened mam-malian species are increasingly restricted) are beginning toresemble habitat-islands in vast seas of agricultural or evenurban development. Therefore, island biogeography is in-creasingly considered an intellectual tool with which conser-vation biologists should be familiar.

The basic theory of island biogeography grew out of twoempirical observations: (1) larger islands often have morespecies than small islands, and (2) an island’s distance fromthe nearest continent is inversely related to the island’sspecies diversity. These observations were eventually broughttogether into the equilibrium theory of island species diver-sity. Conservation biologists use insight from this theory inthe management of fragmented landscapes. In particular theyoften ask how small a refuge “island” can be, before thresh-old effects arise and species-extinctions dominate communitydynamics.

Basically, if a habitat-patch is too small to include homeranges for a viable population of a mammalian species, thenthe long-term survival of that species is improbable. Infor-mation about extinction rates of small mammals in habitatfragments is difficult to evaluate, in part because biologistslack comparable data from undisturbed habitats to serve ascontrols. However, two studies on forest fragments providedisturbing evidence that mammalian diversity can declinequickly:

• Short term, Thailand. In Surat Thani Province ap-proximately 100 islands were created in 1986 when

the Saeng River was dammed to create a hydroelec-tric reservoir. Rapid changes occurred in the smallmammal assemblages on these new islands. Withinfive years, two of the 12 species (a murid rodent,Leopoldamys sabanus and an insectivore, Hylomys suil-lus) were lost. Further extinctions are likely.

• Long term, Panama. Early in the twentieth century,several forest hilltops were isolated during thedamming of the Chagras River during the construc-tion of the Panama Canal. After 80 years of isola-tion, only one out of 16 rodents species remained onislands smaller than 42.3 acres (17.1 ha). The rate ofmammalian species-loss from these small island-fragments was approximately one species per 3–11years.

The fate of large mammal communities in small habitat-fragments is even grimmer. Most big mammals must have agreat deal of space. For instance, the home range of a South-east Asian rhinoceros (Rhinoceros sondaicus annamiticus) in CatTien National Park, Vietnam has been estimated at1,480–2,470 acres (600–1,000 ha). Some solitary carnivoresrequire areas an order of magnitude larger. A tiger, for in-stance, might roam across more than 24,700 acres (10,000 ha),and a single wolverine (Gulo gulo) would probably need twicethat much room.

These are area-requirements for individual mammals,while of course, viable populations are comprised of many in-dividuals. These populations need even larger patches of habitat. For example, many species of African grazing artio-dactyls can exhibit their natural social behavior only in largegroups. Large groups require enormous areas, sometimes with widely separated dry-season and wet-season ranges. The



A conservationist with chimpanzees (Pan troglodytes). (Photo by © YannArthus-Bertrand/Corbis. Reproduced by permission.)



annual migration of east African wildebeest (Connochaetes tau-rinus) covers hundreds of miles (kilometers) and crosses na-tional borders. Of course wildebeest can be kept alive inmodest pastures, and tigers can be maintained in zoo-cages.But these conditions are not fully satisfactory and clearly onlythe largest national parks allow viable populations of mostmammals to exist in natural social conditions.

Conserving such large tracts of habitat is often difficult.One approach is to connect habitat fragments by means ofcorridors, or protected habitat-strips that allow animals tomove between patches. In Africa it has been observed thatsome mammals (as well as reptiles and birds) use corridors asinter-patch bridges. However, some conservation biologistsquestion whether this phenomenon is at all general.

It should be clear that as conservationists contemplate theestablishment, enlargement, or maintenance of a refuge, theyshould be aware of the particular needs of those target or-ganisms that the refuge is designed to shelter. Behavioral ecol-ogists, for example, often gather data on a species’ activitypatterns, foraging behavior, group size, home range, and ter-

ritorial behavior. Such information is useful for predictinghow a target species will respond to habitat fragmentation,how edge-effects will impact a given species, or whether thespecies will use habitat corridors.

Genetic concerns about small populationsThe discussion of thresholds bemoaned the fact that small

populations were at risk of extinction by demographic sto-chastic processes. Efforts to maximize intra-specific geneticdiversity are a high priority for conservationists. In general,genetic diversity is correlated with population size. Thuslarger populations should manifest a greater variety of phe-notypes—and should therefore be better able to respond tovariations in environment. However, with habitat loss andfragmentation, populations of many mammalian species aredeclining and are being fractured into small, disconnectedunits. And as populations shrink, genetic variation may be lost.

Loss of genetic variability from a population is primarilya function of three interrelated phenomena: “bottlenecking,”random genetic drift, and inbreeding depression.

Bottlenecks are events that greatly reduce a population’ssize. Such reductions can have many causes, including habi-tat alteration or loss, introduction of competitors or preda-tors, and the spread of epidemic disease. The individuals thatsurvive a bottleneck are the founders for all future genera-tions, and only the genetic variability that is represented inthese founder-individuals (plus subsequent mutations) can bepreserved within the species. The cheetah (Acinonyx jubatus)is the classic example of a bottleneck species. A populationcrash some 10,000 years ago radically reduced genetic vari-ability. Even today all cheetahs remain so similar, genetically,that skin transplants from one animal to another are not re-jected. More significant, cheetahs may lack the genetic vari-ability to respond, evolutionarily, to new diseases confrontingthe species. But a large population size can usually overcomeproblems of low genetic variation, as is the case with the cur-rent populations of elephant seals, for example.

In evaluating a bottleneck, conservation biologists are es-pecially concerned about the effective population size, or Ne,which is (roughly) the number of breeding animals in a pop-ulation. Ne is generally smaller than the number of individ-uals in the population—and if breeding animals are closelyrelated, it can be much smaller indeed. For example, two setsof identical twins do not count as four complete animals, forgenetic purposes. The rate of a population’s heterozygosity-loss, per generation, is largely a function of effective popula-tion size. That is to say, the amount of genetic variabilitypreserved from one generation to the next is approximatelyproportional to (1 � 0.5 Ne). Obviously, when Ne is large,the majority of genetic variability will be maintained, andwhen Ne is small, heterozygosity can be lost very rapidly.

Clearly, even the tightest bottlenecks need not be fatal to apopulation’s survival. Every mammalian species began from aminimal founder-size, and if a bottlenecked population is allowed to increase greatly in numbers, any decay in genetic diversity can be balanced by new variability added through mu-tation. The most serious problems arise when the bottleneck-

Wardens fix water pipes in Khaudum Game Reserve, in Namibia, aselephants in the backround wait for water. (Photo by Rudi van Aarde.Reproduced by permission.)

squeeze is maintained over multiple generations, because inthis case (1) loss of variability by genetic drift vastly exceedsreplacement by mutation, and (2) this process is acceleratedby inbreeding. An example is the lowered allozyme and DNAvariability observed in the brown hares (Lepus europaeus) ofNew Zealand and Britain and attributed to bottlenecks.

Random genetic drift, sometimes called the Sewall Wrighteffect, designates changes in a population’s allele frequenciesdue to chance fluctuations. Random genetic drift becomes im-portant only when populations are small. Cross-generationaltransfer of alleles is then subject to sampling error, and a givenallele can be lost (decline to 0% frequency) or fixed (increaseto 100% frequency). In other words, when small populationsof a species are isolated, out of pure chance the few individ-uals who carry certain relatively rare genes may fail to trans-mit them. The genes can therefore disappear and their lossmay lead to the emergence of new species, although naturalselection has played no part in the process. And the smallera bottleneck, the more rapidly genetic drift can operate. Thelonger a bottleneck persists, the greater the potential cumu-lative effects of genetic drift.

Inbreeding depression can result from matings betweenclose relatives and is more likely to occur in a small popula-tion confined to a small habitat-patch. The deleterious effectsof inbreeding have been repeatedly documented in zoo pop-ulations, before the implementation of genetic managementprograms. For example, inbred calves of Dorcas gazelle(Gazella dorcas) suffered from high juvenile mortality and de-layed sexual maturity of females. Among wild populations, in-breeding depression in Florida panthers (Felis concolor coryi)may have lowered reproductive rates and reduced the species’capacity to respond to disease.

Przewalski’s horse (Equus caballus przewalskii) is the onlysurviving variety of wild horse. This animal is considered ex-tinct in nature (wild individuals were last observed in 1969)and survives only because of captive breeding. The founder-stock for the captive herd was limited in number. Therefore,genetic drift and inbreeding depression have led to a loss ofgenetic diversity in E. c. przewalskii and are reflected by highjuvenile mortality and a reduced lifespan. International man-agement programs aim to retain 95% of the current averageindividual heterozygosity for at least 200 years. And a programis underway to reintroduce these animals into Mongolia.

WildlifeConservation medicine focuses on the changing health-

relationships between people, other animals, and shared ecosys-tems. Of course every variety of mammal has been affected bydiseases and parasites throughout its species-history. And acrossevolutionary time, mammalian species have established ac-commodations with pathogenic organisms: immune and be-havioral defenses evolve in the host; responses (often includingtransmission “improvement” and reduced virulence) co-evolvein the pathogen. However, the present age—with its frag-mented populations of wild mammals and anthropogenic mix-ing of previously separate species—has destabilized these

dynamic equilibria. And the results are of concern to conser-vation biologists.

In recent years several emerging infectious diseases (EIDs)have been identified in wildlife populations. Among immune-naive populations, these EIDs may inflict direct mortality be-yond a species’ evolved capacity for demographic response.In addition, EIDs may affect reproduction, susceptibility topredation, and the competitive fitness of infected hosts. Whenthese detrimental effects extend to the population level, theymay in turn affect community structure by altering the rela-tive abundance of species.

Habitat fragmentation often places wildlife species incloser proximity to domesticated animals because habitatpatches may be adjacent to farms, villages, and even urban ar-eas. Such situations can facilitate cross-species contagion ofdisease. People have transmitted tuberculosis, measles, and in-fluenza to gorillas (Gorilla gorilla), orangutans (Pongo pyg-maeus), ferrets (Mustela putorius furo), and other mammals.The slaughter of primates for bushmeat in Africa was prob-



The Florida panther (Felis concolor coryi) is an endangered species.International efforts are being made to encourage the survival of allidentified endangered species. (Photo by Animals Animals ©John Pon-tier. Reproduced by permission.)



On French Island, Australia, koalas (Phascolarctos cinereus) are cap-tured for conservation measures while they rest in eucalyptus trees.(Photo by Richard T. Nowitz/Photo Researchers, Inc. Reproduced bypermission.)

ably the first exposure of people to the precursor of humanimmunodeficiency virus (HIV). Lions in the Serengeti havebeen affected by diseases of cats and dogs from Tanzanian vil-lages. In 1984 a disease caused by calicivirus was detectedamong rabbits in China. The origin of the disease is not de-finitively known, but the pathogen soon spread westward intoEurope, where it affected perhaps 90% of the rabbit popula-tions. Rabbit calicivirus is now used as the primary means forcontrolling feral rabbits in Australia. (Earlier control reliedmainly in the introduction of myxomatosis virus among Aus-tralian rabbits. In the 1950s, myxomatosis had a kill-efficiencyof about 99%. Over time, however, Australian rabbit popu-lations evolved immunity.) Efforts to re-establish wild popu-lations of black-footed ferrets (Mustela nigripes) in westernNorth America have been hampered by the spread of cat anddog diseases among the ferrets, and because enormous pop-ulations of ferret prey (prairie dogs) had been destroyed bysylvatic plague.

Because human health may be increasingly affected by dis-eases transferred from wildlife, conservation medicine is likely

to become an important area of research for conservation bi-ologists.

Ex situ conservation issues: demand,consumption, and captive breeding

Much of this essay has focused on in situ conservation prob-lems because the most important conservation battles willlikely be fought on the home grounds of the target species.Nevertheless, the importance of ex situ conservation issuesshould not be underrated. Ex situ issues are of two very dif-ferent types.

Issues of demand and consumptionThe impact of economic factors on conservation must be

recognized as well. As mentioned earlier, human poverty un-dercuts conservation programs near many of the world’s biodiversity hotspots, but economic factors can affect conser-vation even from a distance. Research on west Africa’s bush-meat trade shows that if markets for meat are exclusively local,the impact of hunting is relatively limited. However, if bush-meat becomes a commodity in a nation’s general capitalisteconomy (if, for example, a market for bushmeat develops ina large city), then demand for forest animals becomes practi-cally unlimited, and vulnerable species may be hunted to extinction. Similarly (here a non-mammalian example), theperilous condition of Southeast Asia’s hitherto magnificentchelonian fauna is primarily a function of China’s emergenceas the regional economic superpower—and of China’s insa-tiable demand for turtle products. Sometimes economic in-fluences can be somewhat less direct. An analysis of theJapanese whaling industry in the 1950s and 1960s indicatedthat commercial species could be harvested at reasonable prof-its indefinitely, on a sustained-yield basis. However, the rateof whale-replenishment (r in the population growth equa-tions) was slower than the rate of Japan’s economic growth.Therefore, it made good business-sense for commercialwhalers to “liquidate their investments” in whales (i.e., to huntthem out) and reinvest their yen in sectors of the Japaneseeconomy yielding higher rates of “interest.”

It is hoped that many conservation-and-economics dilem-mas may eventually yield to analysis by economically sophis-ticated conservation biologists—or even by “conservationeconomists.” That is, sustainable development programs com-bining people, profits, and wildlife may yet save the day. How-ever, in the long run Wise or Knowing Man must develop anew conservation ethic—of sharing, sacrifice, appreciation,and awe—if an appreciable portion of mammalian biodiver-sity is to be preserved. In other words, why read Phillips andAbercrombie instead of re-reading Aldo Leopold (A SandCounty Almanac first published in 1949) and Archie Carr?

Captive breeding and reintroductionIn recent years ex situ conservation efforts have become

increasingly important. Zoos, botanical gardens, wildlifeparks, and conservation trusts now work in collaboration tomaintain captive assurance colonies of threatened plants andanimals. Studbooks on target species are kept by participat-ing institutions, and breedings are scheduled in consultationwith conservation geneticists.

The proximate mission of ex situ colonies is to maximizegenetic diversity within a captive population of affordable size.Long-term, however, the fundamental conservation goals ofcaptive breeding are release-in-habitat with the skills neces-sary for survival—and eventual reestablishment of viable wildpopulations within target species’ historical ranges. Captivepropagation definitely works, and more threatened species arenow bred in zoos, etc., than ever before. On the other hand,reintroductions (as well as related programs such as translo-cation of wild animals) have enjoyed only mixed success.

The case of the giant panda (Ailuropoda melanoleuca) maybe instructive. Today only about 1,000 of these magnificentanimals survive in the mountain forests of central China. Yearsof environmental degradation, disease, and depredation havetaken their toll on A. melanoleuca. Furthermore, within theanimals’ fragmented habitat, post-flowering bamboo die-offshave added malnutrition to the pandas’ tale of woe. Presently,about 140 giant pandas are maintained in Chinese zoos andin other breeding facilities around the world. However, de-spite the infusion of massive amounts of money, captivebreeding programs have met with only limited success. Of the226 giant pandas born in captivity between 1963 and 1998,only 52% survived for as long as a month, and others diedbefore they reached reproductive maturity. At present thecaptive population is scarcely self-sustaining, and it may notproduce appreciable numbers for release within the foresee-able future.

By contrast, captive propagation and reintroduction havebeen more successful with the golden lion tamarin (Leontop-ithecus rosalia), a small primate endemic to the Atlantic coastalforests of eastern Brazil. Because of over-exploitation and(particularly) habitat destruction, this tamarin had become en-dangered by the late to mid twentieth century. Beginning in1984, scientists from Brazil and the United States began rein-troducing zoo-born golden lion tamarins back into their habi-tat in the wild—primarily onto private lands that could beprotected against the ravages of timber harvest. The com-bined efforts of governments, nongovernmental organizations(NGOs), local communities, zoological parks, and conserva-tion scientists have more than doubled the size of the wildgolden lion tamarin population.

A review of 116 reintroductions (89 involved mammals; allwere carried out between 1980 and 2000) concluded that 26%succeeded and 27% failed. (The remaining 47% were classi-fied as uncertain.) Many factors influence reintroduction suc-cess. These include habitat quality, the number of individualsreleased (there is no magic number, but 100 has become therule of thumb), and the density of predators. Before any rein-troduction is attempted, however, conservationists shouldidentify and eliminate the cause of the target species’ initialdecline. If this can be done, then a reintroduction has a rea-sonable chance of success. Otherwise, a reintroduction mayprovide opportunities for feel-good press releases, but it is un-likely to result in establishment of a viable wild population.

Translocation involves moving wild animals from oneplace to another and therefore is, in a sense, an ex situ activ-ity. Sometimes translocations are attempted without adequatepreparation. For example, in French Guiana, howler monkeys

(Alouatta seniculus) were translocated because their habitat wasto be flooded by the construction of a hydroelectric dam.These individuals were moved to an area where howler num-bers had been reduced by hunters—and where hunting stilloccurred. In other words, the cause of the original popula-tion decline had not been addressed, and the success of thetranslocation is still in doubt.

The translocation of Asian rhinoceroses (Rhinoceros unicor-nis) in Nepal is a happier story. Nepali government biologists,assisted by World Wildlife Fund for Nature (WWF), U.S.Fish and Wildlife Service (USFWS), and the King Mahen-dra Trust, captured rhinos in Royal Chitwan National Parkand transported them 220 mi (350 km) cross-country to RoyalBardia National Park. The receiving park was within the Asianrhino’s historic range. Habitat was excellent (in quality andquantity), and although R. unicornis had been extirpated fromBardia by poachers, the park was well protected by the timethe reintroduction project began. Rhino translocations havecontinued for a decade, and now conservation biologists be-lieve that Nepal has successfully established a second viablepopulation of R. unicornis.

Translocations of wild animals are often attempted for rea-sons unrelated to conservation. While conservationists maynot generally support the movement of wildlife to solve hu-man-animal conflicts, they can sometimes learn valuablelessons from such activities. For example, nuisance brushtailpossums (Trichosuros vulpecula) moved from the city of Mel-bourne into the Australian outback suffered heavy depreda-tion. Similarly, small, endangered mammals, raised in a zoo,might require some sort of predator-avoidance training be-fore they were released into areas with high predator densi-ties. White-tailed deer (Odocoileus virginianus), captured fortranslocation when the Florida Everglades were in flood, gen-erally did not survive the ordeal. From this experience somebiologists learned a great deal about the importance of min-imizing capture-trauma when dealing with mammals alreadyunder severe stress. Translocations of nuisance raccoons (Pro-cyon spp.) and black bears (Ursus americanus), though perhapsunwise, reinforce the lesson that some animals know how toget home—and will walk a very long way to get there.

Evaluating the success of conservationprojects

This essay is not intended to offer instructions on how toconduct a conservation program. Decisions about supportingconservation are important and they should be made consci-entiously on the following basis: “Evaluate with a criticalmind, and then support with an open heart.”

IT IS MOST IMPORTANT TO EVALUATE THE CANDIDATE’SOR ORGANIZATION’S EFFICIENCY AND INTEGRITY

In this day and age, almost every political candidate willclaim to be a great supporter of conservation. Every “Save theWhatever” organization employs experts who design mail-outappeals that are aesthetically elegant and read as sincerely asthe Sermon on the Mount. Most readers of this essay are so-phisticated enough to see beyond political hype. Also, almost





every U. S. state (and many national governments around theworld) has a consumer advocate office that can help evaluatethe non-profit organizations that solicit conservation contri-butions. Typically these consumer advocate offices can pro-vide information on the percentage of contributions that goto support actual conservation activities (as opposed to pay-ing staff personnel, for example). They can almost always warnof organizations that support outright frauds.

IT IS IMPORTANT TO EVALUATE THE PROGRAMADVOCATED BY A CANDIDATE OR CONSERVATIONORGANIZATION

A key to evaluation is to determine whether an organiza-tion’s stated objectives are meaningful and realistic. Here are four hypothetical statements of objectives that should be questioned:

• Elephants are in terrible danger, and your contributionwill save the lives of countless elephants in southern Africa.The organization should offer some idea of how thepromise will be fulfilled. Furthermore, words like“countless” should ring loud alarm bells.

• If I am elected, I will protect lands in such a way as toconserve functioning ecosystems in which living organ-

isms can interact in complex ways. Every living sys-tem—from rice fields to rainforests to urban gar-dens to septic tanks—meets this criterion. This isa meaningless promise, since it will automaticallybe kept.

• The goal of our policy is to preserve appropriate natural,aesthetic values for future generations. Both authors ofthis essay are teachers. Part of our job is evaluation,and we don’t give tests that we cannot grade. Thuswe are wary of claims that cannot be checked. Welike the idea of preserving values—but we wouldn’toffer our votes or our dollars until we learned manymore specifics.

• The objectives of this program are to integrate economicand intrinsic wildlife values in a holistic program thatrecognizes human rights to sustainable development andnational responsibilities for conservation of biodiversity.This statement sounds great. It uses most of the fa-vorite vocabulary words of the conservation com-munity. However, we have no idea what thestatement means—and we wrote it. We would cer-tainly look for specific, measurable objectives beforewe were tempted to support such a program.

ResourcesBooks

Caro, Tim, ed. Behavioral Ecology and Conservation Biology.Oxford: Oxford University Press, 1998.

Carr, Archie. Ulendo: Travels of a Naturalist In and Out ofAfrica. New York: Knopf, 1974.

Ehrlich, Paul. Human Natures: Genes, Cultures, and the HumanProspect. New York: Penguin Books, 2002.

Gosling, L. Morris, and William J. Sutherland, eds. Behaviourand Conservation. Cambridge: Cambridge University Press,2000.

Hunter, M. L., and A. Sulzer. Fundamentals of ConservationBiology. Oxford, UK: Blackwell Science, Inc., 2001.

Kleiman, Devra G., and Anthony B. Rylands, eds. LionTamarins: Biology and Conservation. Washington, DC:Smithsonian Institution Press, 2002.

Leopold, Aldo. A Sand County Almanac. Reissue ed., NewYork: Ballantine Books, 1990.

Meffe, G. K., and C. R. Carroll. Principles of ConservationBiology. Sunderland, MA: Sinauer Associates, Inc., 1997.

Primack, Richard B. Essentials of Conservation Biology. 3rd ed.Sunderland, Massachusetts: Sinauer Associates, 2002.

Wilson, Edward O. The Diversity of Life. Cambridge, MA:Harvard University Press, 1992.

PeriodicalsDaszak, P., et al. “Anthropogenic Environmental Change and

the Emergence of Infectious Diseases in Wildlife.” ActaTropica 78 (2001): 103–116.

Fischer, J., and D. B. Lindemayer. “An Assessment of thePublished Results of Animal Relocations.” BiologicalConservation 96 (2000): 1–11.

Lindburg, D. G., et al. “Hormonal and BehavioralRelationships During Estrus in the Giant Panda.” ZooBiology 20 (2001): 537–543.

McShane, Thomas O. “The Devil in the Detail of BiodiversityConservation.” Conservation Biology 17 (2003): 1–3.

Myers, N., et al. “Biodiversity Hotspots for ConservationPriorities.” Nature 403 (2000): 853.

Peng, Jianjun, et al. “Status and Conservation of the GiantPanda (Ailuropoda melanoleuca): A Review.” Folia Zoologica 50(2001): 81–88.

Rosser, Alison M., and Sue A. Mainka. “Overexploitation andSpecies Extinction.” Conservation Biology 16 (2002): 584–586.

OrganizationsConservation International. 1919 M Street NW, Ste. 600,

Washington, DC 20036. Phone: (202) 912-1000. Web site:<http://www.conservation.org>.

IUCN—The World Conservation Union. Rue Mauverney 28,Gland, 1196 Switzerland. Phone: ++41(22) 999-0000. Fax:++41(22) 999-0002. E-mail: [email protected] Web site:<http://www.iucn.org/>.

Wildlife Conservation Society. 2300 Southern Blvd., Bronx,NY 10460. Phone: (718) 220-5100. Web site:<http://wcs.org>.

World Wildlife Fund. 1250 24th Street N.W., Washington,DC 20037-1193 USA. Phone: (202) 293-4800. Fax: (202)293-9211. Web site: <http://www.panda.org/>.

Kimberley A. Phillips, PhDClarence L. Abercrombie, PhD

IntroductionThe three living species of monotreme have always been

regarded as zoological enigmas, so much so that when thefirst specimen of a duck-billed platypus (a single skin) wasshipped back to Europe from Australia at the close of the eigh-teenth century, it was widely believed to be a hoax, and anunconvincing one at that. It would not have been the firsttime a ship arrived from the East Indies with a cleverly faked“marvel.” Previous hoaxes had included supposed mermaids(half fish, half monkey) and wildly exotic birds of paradise, sothe scientific community at the time can be forgiven for be-ing skeptical. However, the duck-billed platypus is one ofthose cases where fact is at least as strange as fiction. It is anunlikely looking amalgam of parts taken from other animals,including a stout, cylindrical body covered in fur, hugewebbed feet, a flat paddle-shaped tail, and a unique rubberybill. The English naturalist George Shaw examined the skin,and was initially dubious as to the validity of the specimen.After examining it carefully and failing to find any evidenceof forgery, he formally described it in 1799. He named itPlatypus anantinus, which literally translated means “flat-footed duck-like.” The name was changed to Ornithorhynchusanatinus when it later transpired that the genus name, Platy-pus, had already been used to describe a species of flat-footedbeetle. The platypus was not the first known monotreme. Theshort-beaked echidna (Tachyglossus aculeatus) had been de-scribed seven years earlier, also by Shaw, but had caused muchless of a stir, presumably because its superficial similarity tothe European hedgehog made it easier to accept. It was notuntil 1802 that an entire preserved specimen of the platypus

arrived in Europe, providing unequivocal proof that it was agenuine animal. But this was just the first in a long series ofzoological conundrums presented by this highly distinctivegroup. Closer examination of platypuses and echidnas hasshowed that these are far from regular mammals. The sug-gestion that they reproduced by laying eggs instead of givingbirth to live young left most Victorian zoologists incredulous,and it was almost 100 years before this could be proved. Theseand many other disconcerting new discoveries have earnedthe monotremes an enigmatic reputation among mammals,and they are still far from being fully understood.

Evolution and systematicsThe first reaction of many taxonomists on examining the

monotremes was to classify them as an unusual group of fur-bearing reptiles. It took almost 200 years for monotremes tobe declared unequivocally as mammals—indeed, some peopleremain unconvinced. The characteristics that qualify them asmammalian include a single bone in the lower jaw, three smallbones in the middle ear, a high metabolic rate and warmblood, a body covering or hair, and the ability of females toproduce milk to feed their young. This last feature is the mostimportant. Milk is secreted by mammary glands; hence, theclass name, Mammalia.

In order to emphasize the differences between monotremesand other mammals, the order is often placed in its own sub-class, the Prototheria. The name, meaning “first beasts,” isunfortunate, since it implies that monotremes are in some way


●

Monotremata(Monotremes)

Class Mammalia

Order Monotremata

Number of genera, species 3 genera; 3 species

Photo: A short-beaked echidna (Tachyglossus ac-uleatus), pair in Queensland, Australia. (Photo byJ & D Bartlett. Bruce Coleman, Inc. Reproducedby permission.)

ancestral to other mammals. This is a common misconcep-tion. Many people still insist on describing monotremes asprimitive, or inferior. This is demonstrably not the case. How-ever, the Monotremata are certainly an ancient group—theysplit from the main branch of the mammalian phylogenetictree sometime during the Cretaceous period, probably about125–130 million years ago. This was before the divergence ofmarsupials and placental mammals, but at least 80 millionyears after the split between reptiles and mammals.Monotremes are no less advanced than any other living mam-mal group. Far from being ancestors of other mammals, theyare cousins that have simply evolved in a different direction.They have retained many characteristics attributed to mam-mal ancestors, but they have also developed sophisticatedadaptations lacking in other mammals. For example, they pos-sess a remarkable “sixth sense” that enables them to sense theminute electric fields generated by other animals.

Seemingly, the monotremes have never been a particularlylarge or predominant group. The fossils identified to date in-clude just eight extinct species, most of which have been foundin Australia. However, these are quite diverse, including twospecies representing extinct families, the Kollokodontidae andSteropodontidae. There are also three extinct species ofechidna and three long-dead species of platypus. The earliestknown monotreme is also the earliest known mammal in Aus-tralia, a fossil known as Stenopodon galmani. It was discoveredin rocks about 110 million years old during the excavations ofan opal mine at Lightning Ridge in New South Wales. Onlya fragment of jaw and a few teeth have been recovered, butthis is enough to show that monotremes were as much a fea-ture of Cretaceous Australian landscape as dinosaurs. Anotherimportant fossil find includes a 62-million-year-old platypustooth from Patagonia. This fossil, known as Monotrematum su-damericanum, the South American monotreme, is significant

because it suggests that the ancestors of modern monotremesmay once have been widespread on the prehistoric southernlandmass of Gondwana.

The most informative monotreme fossil discovered to datecomes from the extraordinarily rich fossil beds of Riversleighin Queensland, Australia. Estimated at 13 million years old,the specimen is an almost perfectly preserved skull that closelyresembles that of a modern platypus, except that the jaw isfull of developed teeth. The modern platypus only has babyteeth (milk teeth), which are, in the adult, replaced by flathorny pads that are used like millstones to crush and grindfood before swallowing. The long-extinct relatives of theduck-billed platypus probably had a broad insectivorous dietmuch like that of modern-day hedgehogs and shrews. TheRiversleigh platypus was given the generic name Obdurodon,meaning “enduring tooth.” It is considered one of the mam-malian fossil finds of the century, and is one reason River-sleigh has been designated a World Heritage Site.

Physical characteristicsMonotremes have retained a number of skeletal charac-

teristics possessed by reptilian ancestors, most importantly thestructure of the shoulder girdle and some features of the skull.The skull has a fairly large, rounded braincase and an elon-gated muzzle. Adults of the living monotremes have no teeth.Vestigial teeth are present in the jaws of juvenile platypuses,but they never erupt from the gums. The fact that they arepresent at all is an example of what evolutionary and devel-opmental biologists call ontogeny-recapitulating phylogeny,which means the embryonic development of a young platy-pus follows a similar pattern to evolutionary development ofthe species. The same phenomenon is seen in frogs develop-


Vol. 12: Mammals IOrder: Monotremata

The platypus (Ornithorhynchus anatinus) is one of only three egg-lay-ing mammals. (Photo by J. & D. Bartlett. Bruce Coleman, Inc. Repro-duced by permission.)

A short-beaked echidna (Tachyglossus aculeatus) forages for food.(Photo by Ann & Steve Toon Wildlife Photography. Reproduced by per-mission.)

ing from fish-like tadpoles, or land-dwelling crabs starting lifeas aquatic shrimp-like larvae. This theory is supported by thediscovery of several fossil monotremes with fully developeddentition.

Living monotremes lack sensory whiskers. They havesmall, beady eyes and no external ears. Internally, however,the ears are much like those of conventional mammals, withthree tiny ear bones—the incus, malleus, and stapes. Thesethree bones, which help transmit vibrations from the eardrumto the inner ear, evolved in mammal ancestors from part ofthe jaw after the split from other reptiles.

The lack of development in certain sense organs such asears and whiskers is more than amply compensated by thepresence of another sense, which is unique to this order. Inall living monotremes, the snout is covered in soft, rubberyskin, and pitted with tiny pores. These are lined with thou-sands of highly sensitive receptors that detect and transmitsensory information directly to the animal’s brain. The shapeof the snout varies considerably and is clearly adaptive. Thesnouts of the two echidna species are narrow and cylindri-cal, ideal for probing among leaf litter or into anthills. Thebill of the platypus is flat and shovel-shaped for sweepingthrough the top layer of sediment on lake and river beds. Itresembles that of a duck in shape alone; in living specimens,

it is soft and moist, more like a dog’s nose than a bird’s hardbeak.

All monotremes are hairy. The platypus has a particularlywell-developed pelt of fine, dense hairs. The coat is an adap-tation to the animal’s semi-aquatic lifestyle, and serves to keepit warm by trapping a layer of air close to the skin. In theechidnas, as in placental hedgehogs, porcupines, and some in-sectivores, the body hairs are interspersed with spines. In fact,the spines are themselves enlarged hairs. They are made ofthe protein keratin and grow from follicles in the skin.

All montremes have short, powerful legs. Those of theplatypus are adapted for swimming. Each of their large feethas five long toes, connected by a leathery webbing. The legsand feet of echidnas are adapted for digging and breakingopen anthills and rotten logs in search of food. Both echidnaspecies possess very well-developed claws. Male monotremesalso have characteristic horny spurs on their ankles. In adultmale platypuses, these are large and sharp with longitudinalgrooves connected to ducts from glands in the thigh that se-crete a highly potent venom. The spurs of male echidnas aresmaller and less well developed.

Unlike most of the world’s mammals, the digestive, ex-cretory, and reproductive tracts of monotremes, in both males


Order: MonotremataVol. 12: Mammals I

A duck-billed platypus (Ornithorhynchus anatinus) swims underwater. (Photo by Dave Watts/Naturepl.com. Reproduced by permission.)

and females, all exit the body via a single opening, called thecloaca. Females have mammary glands but no teats as such;the mammary ducts open in pores on the female’s furry ab-domen. Male platypuses and echidnas do have a penis—it isforked like that of some marsupials, but is used only for de-livering sperm and not for urination. In male and femalemonotremes, urine from the bladder passes via the cloaca.

Monotremes are warm-blooded, but they maintain theirbody temperature at a slightly lower level than placental mam-mals—usually somewhere between 86°F and 91.4°F(30–33°C). The blood is pumped by a four-chambered heart,which differs from that of other mammals in having an in-complete separation between the right atrium and ventricle.

DistributionModern monotremes, and all but one of the fossil species

so far described, are confined to the continent of Australiaand the island of New Guinea. The short-beaked echidna isthe most common and widespread of the three living species.It occurs throughout Australia and Tasmania and in centraland southern New Guinea. The platypus is more restricted—it occurs only in eastern Australia in the states of Queensland,New South Wales, Victoria, and Tasmania. There is an in-troduced population on Kangaroo Island off the coast ofSouth Australia. The long-beaked echidna (Zaglossus spp.) isendemic to New Guinea and is increasingly restricted to re-mote areas that remain inaccessible to humans.

HabitatFor a small group of specialized animals, monotremes oc-

cupy a surprisingly wide range of habitats. The duck-billedplatypus is semi-aquatic and is dependent on permanent riversor freshwater pools. Thus, it is restricted to parts of Australia

with a relatively high rainfall. Both males and females con-struct simple burrows on the banks of rivers or pools and catchmost of their food underwater. Polluted waterways and thosethat have undergone severe bankside development or canal-ization are generally not suitable. However, platypuses are increasingly common in suburban settings, due to legal pro-tection and environmental restoration projects.

Short-beaked echidnas are among the most ubiquitousAustralian mammals. They have no specialist habitat re-quirements other than an adequate supply of ants for food,and live everywhere from tropical rainforest to suburban gar-dens and city parks. There is enough moisture in their dietto sustain them even in the arid central desert of Australia,although there they are much more sparsely distributed. Thelong-beaked echidna occupies a more restricted range of habi-tats, mainly montane forests and damp alpine meadows in thehigher parts of New Guinea. It is much less tolerant of dryconditions than its short-beaked cousin.

BehaviorAs general rule, monotremes are nocturnal or crepuscular,

and the best time to watch them is around dusk and dawn.They are active by night in order to avoid the heat of the day.However, daily activity is dictated to some extent by climateand the degree of disturbance. The two species whose rangeextends into temperate parts of Australia, the duck-billedplatypus and the short-beaked echidna, are often active byday, especially in winter when the nights can be quite cold.

Cold weather and food shortages can induce the short-beaked echidna to enter short periods of torpor—a deep sleep,during which metabolic processes slow down and energy isconserved. The species is also the only monotreme capableof full hibernation. In most parts of the species’ range, this isnever necessary, but in the Snowy Mountains of New SouthWales, winters can be sufficiently long and harsh so thatechidnas spend up to four months asleep. They may wake pe-riodically to investigate their surroundings, and even move toanother den before going back to sleep. During hibernation,the echidna’s body temperature may drop as low as 39.2°F(4°C), much lower than during shallow summer torpor. A hi-bernating animal uses very little energy, but even so, a longwinter can take a serious toll on an individual’s reserves of fat,and it may emerge in spring some 10–20% lighter than whenit first began hibernating.

Detailed studies of the duck-billed platypus and the long-beaked echidna are hampered by the fact that these are rathershy and elusive animals. The same cannot be said of the short-beaked echidna, which is bold by comparison and especiallytolerant of humans. In fact, Australian echidnas have few en-emies and little to fear from any predator. They are too bigto be threatened by cats or even foxes, and their sharp spinesare usually sufficient to deter large dogs such as the dingo orbirds of prey. If a large animal approaches too close for com-fort, the echidna curls its body into a tight ball and raises itsspines for protection. Should evasive maneuvers be necessary,the echidna can burrow extremely quickly, literally sinkinginto the ground until all that remains are a few protruding



A short-beaked echidna (Tachyglossus aculeatus) in a defensive ball.(Photo by C. B. & D. W. Frith. Bruce Coleman, Inc. Reproduced by per-mission.)

spines. Despite their lack of spines, adult platypuses are largeenough to have few natural predators.

The platypus spends much of its time hidden away in wa-terside burrows, and emerges to feed only in the quiet hoursafter dusk and just before dawn. It tends not to travel far fromhome and usually slips straight into the water. When movingon land, the platypus uses a brisk but relatively inefficient wad-dle, but it is a superb swimmer and spends much of its timebeneath the surface. Its perfectly streamlined body is pro-pelled swiftly and silently through the water with the largewebbed front feet. The back feet act as rudders and brakes,and the animal is able to twist and turn with a speed and agilitycomparable to that of a bird in flight. The platypus returnsto the surface every minute or so to take a breath, but it doesso silently and without a splash. At the start of each dive, itrolls forward in the water, its sleek form barely breaking thesurface. Echidnas can swim, too—their spines help make themsurprisingly buoyant and they can make rapid progress in wa-ter using a steady doggy paddle.

The monotremes are for the most part solitary animals,except for mothers with young. Single animals occupy a homerange that may overlap with those of several others, but theyare not territorial and show very little interest in each otherexcept during the breeding season.

Less is known of the New Guinean long-beaked echidnathan its two Australian cousins. It too is nocturnal and gen-erally lives alone.

Feeding ecology and dietMonotremes are highly specialized feeders on invertebrate

prey, but the diets and foraging behaviors of the living speciesare all very different. The short-beaked echidna specializes infeeding on ants, an abundant food resource exploited by rel-atively few other Australian animals, which is another reasonfor the species’ great success. The echidna’s long narrow snoutor “beak” is thought to be equipped with an additional sensethat enables the animal to detect electrical activity, but prob-ably the most important sense when it comes to feeding issmell. The echidna shoves its snout into ant nests and rottenlogs. If ants are detected, the animal uses its claws to rip openthe nest and begins lapping up the insects with its long, stickytongue. Mouthfuls of ants are mashed between the tongueand the hard palette of the echidna’s mouth before being swal-lowed.

Like the short-beaked echidna, the duck-billed platypusfaces very little competition for food. The platypus hunts un-derwater in the dark, but the gloomy conditions are no hand-icap. The platypus has reasonable eyesight and hearing, butit closes both its eyes and ears when underwater and relieswholly on the information transmitted to its brain by nervesserving the snout. Not only is the snout sensitive to touch, italso contains about 850,000 tiny receptors, able to detect theminute electrical fields generated by the bodies of other liv-ing animals, even very small ones such as those of insect lar-vae. It is difficult to imagine how this extra sense works—itis similar to the lateral line sense of fish, but more finely tuned.Larger prey animals are snapped up and crushed against the

hard palate, while smaller ones are strained out of the wateror sediment. The food is then pushed into large cheekpouches and stored while the platypus searches for more. Theplatypus returns to the surface periodically to process and eatits catch. Food is crushed and ground between horny platesthat line each jaw, and swallowed. It may take several min-utes to finish such a meal, during which time the platypusdrifts at the surface with its feet spread wide.

The third species, the long-beaked echidna of NewGuinea, is though to feed mainly on earthworms, which it un-earths in humid forests. Its extra long nose is used to probedeep into the humus layer or into the topsoil, and once de-tected, prey is quickly excavated with the front feet, collectedwith the aid of a long, mobile tongue that is armed with hook-like spines in a central groove. The worms are lightly mashedin the mouth, then swallowed.

Reproductive biologyOne of the most remarkable montreme features, and the

one that initially seemed to be the biggest obstacle to theirinclusion in the class Mammalia, is the fact that females layeggs instead of giving birth to live young. The eggs are sub-sequently brooded and hatched outside the mother’s body, asin reptiles and birds.

Monotremes typically breed slowly. It takes a motherplatypus about six months to raise a small litter of one or twoyoung to independence, seven months in the case of the short-beaked echidna, which typically has only one baby at a time.Long-beaked echidnas have larger litters of four to six young,but still only breed once a year. By investing a large amountof parental care in a few young, the young have a high rate



A duck-billed platypus (Ornithorhynchus anatinus) in the wild. (Photoby Dave Watts/Naturepl.com. Reproduced by permission.)

of survival. They are also surprisingly long lived. Wild platy-puses usually survive into their early teens, whereas long-beaked and short-beaked echidnas may live well into the 20s,while captives have lived 30 and 50 years, respectively.

By early spring, courtship and rivalry among platypuses iswell underway and males become very aggressive. They willfight for dominance and the right to mate with the femalesliving within their range. They have no teeth and their clawsare blunt, but the sharp spurs on the ankles are deadly. Nor-mally, they are kept folded away to avoid snagging, but dur-ing battle they are raised. Fights occur in the water, wherethe animals are most agile, and combatants swim in tight cir-cles, each attempting to spike the other and inject a debili-tating dose of venom. The venom is toxic enough to kill adog and cause agonizing pain and prolonged paralysis in hu-mans. The male duck-billed platypus is the world’s only ven-omous mammal. The spurs in male echidnas are small andsharp, but lack the deadly venom. Having seen off his rivals,the victorious male woos the female with a courtship involv-ing a slow circular dance, during which he holds her tail inhis bill. Both courtship and mating take place in the water.

Rivalry among male echidnas is equally intense, thoughnot quite as violent. At the start of the breeding season, maleechidnas begin following females around. After two or threeweeks, some females have attracted a following of six or sevensuitors, that follow her every move in a line known somewhat

whimsically as a “love train.” As the female comes into breed-ing condition, the males begin circling her, creating a circu-lar trench from which each male attempts to evict his rivals.The last male left in attendance claims the right to mate.

Beyond courtship and mating, male monotremes havenothing more to do with the rearing of their young. The fe-males, on the other hand, are diligent parents. After mating,females are busy preparing their nests, which are built in deepburrows. The echidnas excavate burrows for nesting or takeadvantage of natural dens such as rock crevices or hollow logs.Platypus burrows are simple oval tunnels with a sleepingchamber at the end. Breeding females also build more exten-sive nesting burrows. These may extend as far as 65 ft (20 m)into the bank, with branching tunnels that twist and turn,some leading to living chambers, others to dead ends. Unlikemost other mammals, which do their best to keep nesting ar-eas snug and dry, the atmosphere inside a platypus nest is veryhumid. The nest is made of damp leaves and other vegeta-tion collected from the water or the banks and carried to theburrow clasped under the body by the tail. The breeding tun-nel is blocked every few feet with loose earth, which the fe-male shifts and replaces every time she comes and goes.

As in marsupials, most development takes place outside themother’s body and pregnancy itself is very short—just twoweeks in both the platypus and the short-beaked echidna. The



The world’s first platypus (Ornithorhynchus anatinus) twin puggles born in captivity are shown together for the first time during a full health checkat Taronga Zoo’s veterinary clinic in Sydney, Australia, March 28, 2003. (Photo by AFP PHOTO/Torsten BLACKWOOD. Reproduced by permission.)

eggshells are rubbery, not brittle, and surround each embryowhile it develops in the uterus. Each egg contains a very largeyolk to sustain the embryo until it has developed sufficientlyto hatch out and sustain itself on milk. The eggs are smalland almost spherical. Those of the short-beaked echidna arelaid directly into a temporary fold of skin, like a marsupialpouch, and can be carried with the mother. The platypus hasno pouch and, once she has laid her eggs, she stays with themin the nest, her body curled around them, never leaving themfor more than a minute or two, for fear they become chilled.The eggs are flexible and slightly sticky, so once laid they tendnot to roll around.

The young of both species hatch after an incubation pe-riod lasting about 10 days. They cut their way out of the eggusing a special milk tooth to pierce and tear the leathery shell.For the echidnas, this single tooth is the only one they willever possess. In the platypus, baby teeth do develop, but theynever become functional.

Newly hatched monotremes are barely 1 in (2.5 cm) long.The body is pink, naked, and almost transparent. Their skinis so delicate that they would shrivel and die in minutes if ex-posed to the sun. But in the humid environment of themother’s pouch or the nest, young echidnas and platypusesare safe from desiccation as long as they can find milk. As forall mammal babies, the first urgent task for a newly hatchedmonotreme is to reach the mammary ducts on the mother’sabdomen, when they start leaking milk about 10 days afterbirth. The development of lactation in mammals is one evo-lutionary mystery on which the monotremes have been ableto shed some light. Mammary glands are thought to haveevolved from sweat glands. In the ancestors of mammals, theyoung of animals that laid eggs like monotremes must havebenefited from the secretion of a sweat-like substance fromcutaneous glands on their mother’s brood pouch. To beginwith, they may have simply absorbed extra salts or moisture,but once this small nutritional advantage was established, nat-ural selection favored lineages in which the glands becamemore and more active. Lactation in mammals was obviouslywell established by the time the monotremes diverged fromthe placental and marsupial lineages, but the former appar-ently never developed specialized structures for the deliveryof milk to the offspring, namely teats. In marsupials and pla-cental mammals, the release of milk is triggered by givingbirth and is sustained by the stimulus of young sucking on ateat. The situation in monotremes is different, since milk isnot needed until 10 days after giving birth and there are noteats for the young to latch on to. Instead, the milk seeps intothe mother’s fur. Young platypuses lap up the milk as it ac-cumulates in the fur, while baby short-beaked echidnas suckvigorously at the mammary pores.

A young echidna may ride in its mother’s makeshift pouchfor up to three months, but not surprisingly it is evicted assoon as its spines begin to grow. Then it will be left in thenest while its mother goes out to feed. Likewise, as youngplatypuses become able to maintain their own body heat, theirmother can leave for longer periods. The young are well pro-tected, even when left home alone—each time she leaves, the

mother carefully replaces a plug of earth as a deterrent topredators and to prevent her offspring from getting out.

Young platypuses are weaned at three or four months.Young short-beaked echidnas first venture outside the pouchat about the same age, but are not capable of feeding them-selves for a further three months.

ConservationThe long-beaked echidna is listed as Endangered by the

IUCN. Never as widespread or abundant as its two Australianrelatives, Zaglossus is now threatened by habitat loss and se-vere over-hunting for meat. The logging industry in NewGuinea is not only responsible for the destruction of huge ar-eas of forest, it also leaves the remaining habitat much moreaccessible to hunters. The latest estimates put the total pop-ulation at about a quarter of a million.

In contrast, the short-beaked echidna is apparently thriv-ing. It is one of few native Australian mammals for which thearrival of European settlers and introduced wildlife has notresulted in a serious decline. It is not hunted for meat, andits spines are ample protection from most animal predators.Its diet of ants means it can survive in a wide variety of habi-tats and is not adversely affected by many forms of develop-ment. Both echidnas and their prey can even survive bushfires, by burrowing underground and waiting for the flamesto pass above.

The duck-billed platypus is something of a conservationsuccess story. It was hunted extensively for its fur, which isthick and silky like that of an otter. The platypus also suf-fered indirectly from the actions of humans, as rivers werepolluted by industrial and mining effluent and waterways were



modified around human settlement. Concrete banks are notgood for burrowing, and human-made structures such asweirs, drain guards, and dams are all potential platypus deathtraps. Many thousands have been drowned in fishing nets.However, the story has a happy ending. Unlike many otherthreatened mammals, the decline of the duck-billed platypusdid not go unnoticed and, since the 1960s, it has been a well-protected species. Many waterways have been restored specif-ically to meet platypus needs and it is an increasingly commonspecies, even in some towns.

Significance to humansEchidnas and platypuses are charismatic animals, which do

no harm to human interests. They are also of considerablenovelty value. “Platypus-spotting” is one of the many wildlifeencounters offered by the highly lucrative Australian eco-tourism industry. Sightings are rarely guaranteed, but formany people, a glimpse of one of these enigmatic creaturesslipping silently into view and disappearing once more willremain a treasured highlight of a visit down under.



ResourcesBooks

Macdonald, D. The New Encyclopedia of Mammals. Oxford:Oxford University Press, 2001.

Nowak, R. “Order Monotremata.” In Walker’s Mammals of theWorld, Vol I, 6th edition. Baltimore and London: JohnsHopkins University Press, 1999.

Quirk, S., and M. Archer. Prehistoric Animals of Australia.Sydney: Australian Museum, 1983.

Strahan, R. The Mammals of Australia. Carlton, Australia: ReedNew Holland, 1995.

PeriodicalsFlannery, T. F., M. Archer, T. H. Rich, and R. Jones. “A New

Family of Monotremes from the Cretaceous of Australia.”Nature 377 (1995): 418–420.

Amy-Jane Beer, PhD

Evolution and systematicsFossil records for echidnas are scarce. The first tachy-

glosssid fossil, a long-beaked echidna (Zaglossus robusta =Megalibgwilia), found in a gold mine at Gulgong, New SouthWales in 1895 was about 15 million years old. Tachyglossus re-mains have been found in Pleistocene sediment (about100,000 years old) at Mammoth Cave, Western Australia andin the Naracoorte Caves of South Australia. Fossil recordsshow that long-beaked echidnas became extinct on mainlandAustralia in the late Pleistocene.

The divergence of present day echidnas and their rela-tionship to other fossil monotremes from the Cretaceous (120million years ago), are unknown.

The family Tachyglossidae is divided into two genera.Tachyglossus, the short-beaked echidna, consists of onespecies, T. aculeatus, and five subspecies. Zaglossus, the long-beaked echidna, has three species, with four subspecies ofZ. bartoni. Zaglossus taxonomy is based on world museumcollections.

Physical characteristicsTogether with the platypus, echidnas are the world’s only

monotremes, or egg-laying mammals. They are sometimesreferred to as “spiny anteaters” because they look like thehedgehog and the porcupine in that they are covered by sharpspines.

Echidnas have a domed shaped back with short stubby tail,no obvious neck, and a flat belly. Back and sides are coveredwith spines (modified hairs) of varying sizes and lengths. Fineto course hair covers the legs and belly and surrounds thespines. The panniculus carnosus, a muscle located under theskin and around the body allows echidnas to assume contor-tionist shapes from very round to nearly flat. This muscle alsopermits movement of individual spines and helps form thepouch in reproductively active females.

Short and long-beaked echidnas are easily distinguishedby differences in size, body mass, and length of the beak.Appearance of ears and eyes are also different. Adult Za-glossus range 24–40 in (60–100 cm) in length, weigh


▲

Echidnas(Tachyglossidae)

Class Mammalia

Order Monotremata

Family Tachyglossidae

Thumbnail descriptionSmall to medium, terrestrial, invertebrate-feeding, egg-laying mammal, characterized by ahead with large brain and narrow beak-like snoutcovered with leathery skin, minute mouthopening under the tip of the beak, no teeth,worm-like tongue, small external eyes, large earslits, stocky, rounded body covered with spinesand fur, powerful front digging limbs, andbackwards rotated hind limbs

Size16–40 in (40–100 cm); 5.5–35.2 lb (2.5–16 kg)

Number of genera, species2 genera; 4 species

HabitatForests, grasslands, heath, shrublands, andwoodlands

Conservation statusEndangered: 3 species; Lower Risk/NearThreatened: 1 species

DistributionAustralia and New Guinea

13.2–35.2 lb (6–16 kg), and have a 4.2 in (10.5 cm) beak, of-ten displaying a downward curve. Adult Tachyglossus are12–20 in (30–50 cm) long, weigh 5.5–15.4 lb (2.5–7 kg), andhave a 2.1 in (5.5 cm) straight beak. Whereas Zaglossus of-ten have small distinct pinna, Tachyglossus generally have noexternal ear. Eyes of Tachyglossus are nearly obscured byhairs, but surrounded by bare wrinkled skin in Zaglossus.Contrary to lore, echidnas see well and can learn using vi-sual cues.

The thick, woolly hair and short spines of Zaglossus aremost like the Tasmanian subspecies of Tachyglossus, T. a. se-tosus. Pelage density, color, and spine length differ betweensubspecies. The arid dwelling T. a. acanthion tend to havelonger, thinner spines and less hair than the other mainlandsubspecies T. a. aculeatus. Pelage of Kangaroo Island, T. a.multiaculeatus, and Tasmania, T. a. setosus, subspecies variesfrom light straw-colored to very dark whereas mainland sub-species are uniformly dark. Albinism has been reported inmost subspecies.

Front and back limbs have five toes, with one to threegrooming claws on each hind foot. Articulation of the rotatedhind limbs in the pelvic girdle gives echidnas extreme dex-terity to scratch between spines on any part of the body.Arrangement of the muscles in relation to the short, stout

limbs gives echidnas enormous strength for digging andclimbing. The limbs of Zaglossus are twice as long as those ofTachyglossus.

Echidna body temperature is low compared to othermammals, 87.8–91.4°F (31–33°C) and individuals use tor-por (lowering of body temperature and metabolic rate) atany time of the year. There is only one opening, the cloaca,for excretion of urinary, fecal, and reproductive productsout of the body. It is not possible to tell the gender of anechidna by external features. All genitalia are located inter-nally. Both males and females may retain a spur on the in-side of the hind foot and both can contract abdominalmuscles to form a pseudo-pouch. Echidnas can live in ex-cess of 50 years.

DistributionShort-beaked echidnas are found throughout Australia and

in some parts of New Guinea. Long-beaked echidnas occuronly in New Guinea and Salawati. They once inhabited partsof Australia, but died out about 20,000 years ago.


Vol. 12: Mammals IFamily: Echidnas

A short-beaked echidna (Tachyglossus aculeatus) forages. (Photo byAnimals Animals ©Roger W. Archibald. Reproduced by permission.)

A short-beaked echidna (Tachyglossus aculeatus) feeds on termites.(Photo by Animals Animals ©K. Atkinson, OSF. Reproduced by per-mission.)


Family: EchidnasVol. 12: Mammals I

HabitatShort-beaked echidnas are found in all types of native and

exotic Australian habitats from sea level to alpine and fromarid through tropical. Little is known about the distributionof T. a. lawesi in New Guinea; most records are from the southand southwest of the country. Long-beaked echidnas havebeen found from sea level to 12,500 ft (4,150 m), primarilyin areas of higher rainfall.

BehaviorEchidnas are solitary living, extremely mobile and have

home ranges up to 494 acres (200 ha). Home ranges of sev-eral animals overlap and are not defended as territories. In-dividuals do not interact, forage communally, or use the sameshelter sites. Short-beaked echidnas are active both day andnight, depending on time of year and locality. They avoid theheat of the day because they do not sweat or pant. Long-beaked echidnas are thought to be totally nocturnal, but lit-tle is known about their natural history.

Echidnas rarely vocalize. Apart from audible snuffingsounds, there are a few reports of soft “cooing” or “purring.”

Feeding ecology and dietWhereas short-beaked echidnas feed on all types of inver-

tebrate species found in the soil or rotting wood; long-beaked

echidnas feed primarily on earthworms. The tongue of thelong-beaked echidna is grooved and has three rows of back-ward directed keratinous spines at the tip, that help extractworms from the ground. The tongue of the short-beakedechidna is lubricated with a sticky secretion, extends up to 7in (18 cm) beyond the tip of the beak, and has an agile tip fordrawing insects into the mouth. Echidnas have no teeth, butgrind their food between a set of tiny keratinized spines lo-cated on the base of the tongue and the roof of the mouth.Echidnas find their prey using acute senses of smell and hear-ing. They also sense vibrations with their beak.

Reproductive biologyShort-beaked echidnas are sexually mature at five to seven

years of age. Courtship and breeding occur during the Aus-tralian winter through spring, June to September. At the be-ginning of the courtship period, male echidnas abandon theirsolitary life style in search of a female. A group of males fol-lowing a single female is called an echidna train. Courtshiplasts between one and four weeks, with up to 10 males ac-companying, prodding, and following a female until she isreceptive. Males then compete, by shoving each other headon head, to dig a trench beside the female. When only onemale remains, he completes the mating trench that preventshim from rolling over as he lifts the female and places histail under hers, cloaca on cloaca. Copulation, which lasts be-tween 30 and 120 minutes, is the only time that the penis isoutside the body. A female mates only once during the re-productive season. After mating, males and females return toa solitary life style.

During the 22-day gestation the mammary glands of thefemale begin to swell and form a longitudinal pouch on thebelly. In a sitting position, the female extends her cloaca andlays a single egg directly into the pouch. The 0.6 in (15 mm)

Long-beaked echidnas (Zaglossus bruijni) are believed to be solitaryanimals. (Photo by Tom McHugh/Photo Researchers, Inc. Reproducedby permission.)

An echidna burrowing for protection. (Photo by Bill Bachman/Photo Re-searchers, Inc. Reproduced by permission.)



The short-beaked echidna (Tachyglossus aculeatus) curls up into a pro-tective ball when threatened. (Photo by Laura Riley. Bruce Coleman,Inc. Reproduced by permission.)

The long-beaked echidna (Zaglossus bruijni) has tooth-like projectionson its tongue. (Photo by Pavel German. Reproduced by permission.)

egg, about the diameter of 10-cent coin, has a soft, leatheryshell. After 10.5 days of incubation, the young echidna, calleda “puggle” hatches. Weighing only 0.0105 oz (300 mg), ittakes 10 puggles to weigh as much as a 10-cent coin. Thereare no teats or nipples for the puggle to attach to. It clings tothe hairs on the mother’s belly with minuscule but well de-veloped front limbs. Milk is suckled from the milk patches,areolae with specialized hairs, located anteriorly and on ei-ther side of the pouch. The puggle remains in the pouch forabout 50 days and increases its body mass 85,000%. Whentoo large to carry, the female leaves the young in a securenursery burrow and returns for two hours every five days tosuckle it. At weaning, seven months of age, the young weigh1.7–3.3 lb (800–1,500g), depending on the size of the mother.There is no mother/offspring relationship after weaning.Young leave the natal area at about one year of age and travelup to 25 mi (40 km) to establish a home range. Most sexuallymature females produce only one young every three to fiveyears.

There have been no observations on the reproductive ecol-ogy of long-beaked echidnas. Their urogenital systems areidentical to Tachyglossus and their reproductive biology is be-lieved to be similar. No one has ever seen a pouch or burrowyoung Zaglossus in the wild and there are no specimens ofyoung in world museum collections.

Conservation statusAlthough T. aculeatus have a wide distribution, popula-

tions are not large. Throughout Australia numbers have de-clined due to loss of habitat, predation by feral foxes, cats,dogs, and pigs, as well as roads, electric fences, and herbi-cide/pesticide use. IUCN lists this species as LowerRisk/Near Threatened. Zaglossus spp. are listed as Endan-gered throughout their range. Populations have disappearedprimarily due to hunting which increased with human den-sities and a breakdown in traditional taboos.

Significance to humansSome aboriginal groups hunted and ate short-beaked echid-

nas while other groups revered them as a totem. Early Euro-peans used echidna fat as a harness dressing or lubricant. Todayshort-beaked echidnas are an Australian icon used by manygrass roots organizations to represent their down-to-earth, get-on-with-it work ethics. In 2000 the echidna was an Olympicmascot. Long-beaked echidnas are hunted for food in some ar-eas of New Guinea. As a member of the oldest surviving groupof mammals echidnas are symbolic of species sustainability.



1

2

1. Long-beaked echidna (Zaglossus sp.); 2. Short-beaked echidna (Tachyglossus aculeatus). (Illustration by Barbara Duperron)



Common name /Scientific name/

Other common namesPhysical

characteristicsHabitat and

behavior Distribution FoodConservation

status

Short-beaked echidnaTachyglossus aculeatus

Stocky, rounded body coveredwith spines and fur. 12–20 in (30–50 cm) long; weight 5.5–15.4 lb (2.5–7 kg); has a 2.1 in (5.5 cm) straight beak. Generally have noexternal ear and eyes are nearly obscured by hairs.

Found in all types of Australian habitats—sea level to alpine, and arid to tropical. Solitary; active both day and night.

Throughout Australia and in some parts of New Guinea.

All types of invertebrate species found in soil or rotting wood.

Lower Risk/Near Threatened

Long-beaked echidnaZaglossus spp.

Stocky, rounded body covered with spines and fur. 24–40 in (60–100 cm) long; weight 13.2–35.2 lb (6–16 kg); has a 4.2 in (10.5 cm) beak, often displaying a downward curve. Often have small distinct external ears, and eyes surrounded by bare wrinkled skin.

Found from sea level to 12,500 ft (4,150 m), primarily in areas of higher rainfall. Solitary; thought to be totally nocturnal.

New Guinea and Salawati.

Primarily earthworms. Endangered

The short-beaked echidna (Tachyglossus aculeatus) uses its flat claws for digging. (Photo by C. B. & D. W. Frith. Bruce Coleman, Inc. Reproducedby permission.)

ResourcesBooksAugee, M. L., ed. Monotreme Biology. Mosman: Royal

Zoological Society of New South Wales, 1978.

Augee, M. L., ed. Platypus and echidnas. Mosman: RoyalZoological Society of New South Wales, 1992.

Augee, M. L., and B. Gooden. Echidnas of Australia and NewGuinea. Kensington: New South Wales University Press, 1993.

Baille, J., and B. Groombridge, eds. IUCN Red List ofThreatened Animals. Gland, Switzerland: InternationalUnion of Conservation for Nature, 1996.



ResourcesFlannery, T. F. Mammals of New Guinea. Sydney: Reed Books,

1995.

Griffiths, M. Echidnas. Oxford and New York: Pergamon Press,1968.

Griffiths, M. The Biology of the Monotremes. New York: AcademicPress, 1978.

Nicol, S. C., and N. A. Andersen. “Patterns of hibernation ofechidnas in Tasnamia.” In Life in the Cold: Tenth InternationalHibernation Symposium, edited by G. Heldmaier and M.Klingenspor. Berlin: Springer, 2000.

Rismiller, P. D. The Echidna, Australia’s Enigma. Southport,Connecticut: Hugh Lauter Levin Associates, 1999.

Rismiller, P. D., and M. W. McKelvey. “Sex, torpor andactivity in temperate climate echidnas.” In Adaptations to theCold, edited by F. Geiser, A. J. Hulbert, and S. C. Nicol.Armidale: University of New England Press, 1996.

Wells R. T. and Pledge, N. S. “Vertebrate Fossils.” In NaturalHistory of the South East, edited by M. J. Tyler, C. R.Twidale, J. K. Ling and J. W. Holmes. Adelaide: RoyalSociety of South Australia, 1983.

PeriodicalsAbensperg-Traun, M. “A study of home range, movements and

shelter use in adult and juvenile echidnas Tachyglossusaculeatus (Monotremata: Tachyglossidae) in WesternAustralian wheatbelt reserves.” Australian Mammalogy 14(1991): 13–21.

Dulhunty, J. A. “Potassium-Argon basalt dates and theirsignificance in the Ilford-Mudgee-Gulgong region.”Proceedings of the Royal Society of New South Wales 104(1971): 9–44.

Flannery, T. F., and C. P. Groves. “A revision of the genusZaglossus (Monotremata, Tachyglossidae) with description ofnew species and subspecies.” Mammalia 62, no. 3 (1998):367–396.

Gates, G. A. “Vision in the monotreme anteater (Tachyglossusaculeatus).” Australian Zoologist 20 (1978): 147–169.

Grigg, G. C., L. A. Beard, and M. L. Augee. “Hibernation in amonotreme, the echidna Tachyglossus aculeatus.” ComparativeBiochemistry and Physiology A 92 (1989): 609–612.

Murray, P. F. “Late Cenozoic monotreme anteaters.”Australian Zoologist 20 (1978): 29–55.

Pledge, N. S. “Giant echidnas in South Australia.” SouthAustralian Naturalist 2 (1980): 27–30.

Rismiller, P. D., and M. W. McKelvey. “Frequency ofbreeding and recruitment in the short-beaked echidna,Tachyglossus aculeatus.” Journal of Mammalogy 81, no. 1(2000): 1–17.

OtherEchidna the Survivor. Documentary videotape. Australian

Broadcasting Corporation, 1995.

Peggy Rismiller, PhD

Evolution and systematicsThe family Ornithorhynchidae includes just one modern

species, the duck-billed platypus. No subspecies or races areknown to occur. Several extinct ornithorhynchid species havebeen described, mainly from fossils found in Australia. At leastone type of ancient platypus is also known to have lived in thePatagonian region of South America some 61–63 million yearsago (mya), when South America was still physically joined toAustralia as part of the giant southern supercontinent, Gond-wana. The nearest living relatives are the echidnas (familyTachyglossidae). Based on genetic evidence, it is believed thatthe platypus and echidna lines have been evolving separatelysince the late Cretaceous or early Tertiary periods, 63–78 mya.

The taxonomy of this species is Ornithorynchus anatinus(Shaw, 1799), New Holland (Sydney), New South Wales,Australia.

Physical characteristicsThe platypus has a flattened, streamlined head and body,

well suited to its aquatic lifestyle. The animal’s color patternensures that the platypus blends in with its watery environ-

ment when viewed from either above or below. The fur is darkbrown above (apart from a small light-colored spot just in frontof each eye) while the chest and belly are silvery cream, some-times marked with a tawny or reddish streak running alongthe animal’s midline. Interestingly, the platypus relies almostexclusively on its front limbs to propel itself through the wa-ter. The end of each front foot is equipped with a broad ex-panse of webbing, forming a highly effective paddle when theanimal swims and dives. In contrast, the back feet are onlymoderately webbed and mainly used for grooming the fur.

Its most striking feature is undoubtedly its bill. Thisstructure is superficially duck-like—so much so that GeorgeShaw, the first professional zoologist to examine a platypus(a dried skin arrived in England in 1799), felt compelled toprobe at the line where the bill joins the rest of the head tosee if the specimen had been forged by a clever taxidermist.While the animal’s bill may look like a duck’s beak, it is ac-tually more like a human thumb in terms of its physical at-tributes and the way it is used. Like a thumb, the platypus’sbill is fleshy and covered by soft, sensitive skin, and is usedby the animal to provide essential information about the sur-rounding environment as well as grab and hold objects.


▲

Duck-billed platypus(Ornithorhynchidae)

Class Mammalia

Order Monotremata

Family Ornithorhynchidae

Thumbnail descriptionAmphibious predator in freshwater habitats,characterized by a broad tail, flat head andbody, short limbs adapted to digging andswimming, and conspicuous duck-like bill

Size16–24 in (0.4–0.6 m); 1.5–6.6 lb (0.7–3 kg)

Number of genera, species1 genus; 1 species

HabitatRivers, lakes, and streams

Conservation statusNot threatened

DistributionEastern Australia, including Tasmania


Duck-billed platypus (Ornithorhynchus anatinus). (Illustration by JosephE. Trumpey)

Vol. 12: MammalsFamily: Duck-billed platypus

The platypus is one of only a few mammals known to be poisonous.Males inject venom with their spurs. (Illustration by Katie Nealis)

The platypus is also remarkable in being one of the fewmammals known to be poisonous. From a gland (the cruralgland) located in the upper thigh, adult males secretevenom, which runs through a duct to a hollow, pointed spur(measuring 0.5–0.8 in [1.2–2 cm] in length) located on theankle of each hind leg. Platypus venom is produced mostabundantly just before and during the annual breeding sea-son, suggesting that it has mainly evolved to help adultmales compete for mates. While platypus venom is not con-sidered to be life-threatening to humans, it can cause ex-cruciating pain for a number of days after a person isspurred.

The platypus is a relatively small animal; males are typi-cally 15–20% longer and weigh 60–90% more than femalesat any given locality. The largest animals measure about 24in (0.6 m) in total length and weigh 6.6 lb (3 kg). To help re-duce its rate of heat loss in the water, a healthy platypus main-tains its body temperature at around 89–90°F (32°C), whichis about 9°F (5°C) cooler than that of humans. Additionally,there are two layers of fur: a dense, wooly undercoat coveredby longer, coarser, waterproof guard hairs. The undercoattraps a layer of air next to the body when a platypus is in thewater, helping to keep the animal warm even in freezing win-ter conditions.

DistributionThe platypus inhabits waterways along the eastern and

southeastern coast of mainland Australia (to about as farnorth as Cooktown, Queensland), and on Tasmania andKing Island. An introduced population is also found on Kan-garoo Island in South Australia, where 19 individuals werereleased in Flinders Chase National Park in the years be-

tween 1928 and 1946. The absence of platypus populationsin central and western Australia reflects the rarity of per-manent lakes or rivers in these areas, while predation bycrocodiles may plausibly limit its distribution at the north-ern end of its range.

HabitatThe platypus occupies a wide range of freshwater habitats,

including ponds, lakes, rivers, and streams at all elevations.The animals are not adapted to feed on dry land, and so aremost commonly found in permanent water bodies. Thespecies will also use humanmade reservoirs as long as the wa-ter is not too deep, mainly feeding at a depth of less than 16.5ft (5 m). The platypus is known to occur in both urban andagricultural areas. The animals are also occasionally seen inriver estuaries, though there is no evidence that they occupysaltwater habitats on a permanent basis.

BehaviorDirect observational studies of platypus behavior are ex-

ceedingly difficult to undertake: the animals are active mainlyat night, and spend most of their time either feeding under-water or resting in underground burrows. Accordingly, muchof what is known about the species’ movements, habits, and ac-tivity patterns has been gained through radio-tracking studies.By fitting animals with special miniature radio-transmitter tags, their location and behavior can be monitored in a con-sistent manner both during the day and at night.

The platypus is essentially solitary in its habits, thoughthree or four animals may occasionally be found foragingwithin a few dozen yards (meters) of each other at a spot wherefood is abundant. Animals residing along a stream or rivertypically have a home range comprising 0.5–6 mi (1–10 km)of channel. Home-range size varies with an individual’s sex

(males have bigger home ranges than females) and habitatproductivity. Home-range size shrinks as waterways supportmore of the small organisms eaten by the platypus, presum-ably because the animals do not have to travel as far to findenough food.

When a platypus is not feeding, it spends up to 17 hoursa day resting in a dry, snug burrow located in a bank at theedge of the water. The animals’ front toes are tipped withstout claws, and observations made in captivity have shownthat a platypus is capable of digging a new burrow at the rateof around 1.5 ft (0.5 m) per hour. An adult without depen-dent offspring normally occupies several different burrows (upto about a dozen) within a period of a few weeks. By havingnumerous burrows scattered along the length of its homerange, a platypus is always reasonably close to a safe refugewhile feeding.

The platypus rarely vocalizes but, when feeling threatened,the animal can produce a high-pitched growl.

Feeding ecology and dietThe platypus is a predator, mainly feeding on bottom-

dwelling aquatic insects such as caddis-fly and mayfly larvae.The platypus is also partial to worms, snails, freshwatershrimps and crayfish, and pea-shell mussels. The size of itsprey is limited by the fact that platypus teeth are lost quiteearly in development and replaced by flat, molar-like grind-ing pads at the back of the mouth. Unlike most mammalianteeth, these pads grow constantly to compensate for surfacewear.

A platypus may find food by digging under banks or snap-ping up morsels floating on the water surface, as well assearching along the bottom sediments. Small prey is storedtemporarily in cheek pouches while an animal is submerged.A foraging platypus typically remains underwater for 10–60

seconds before returning to the surface to breathe and chewits meal with a side-to-side motion of the jaws.

Its eyes and ears are located within shallow, musculargrooves on the sides of the head that automatically pinch shutwhen an animal dives. The platypus mainly relies on its billto find food underwater. The surface of this remarkable or-gan is densely packed with tens of thousands of specializedsensory receptors, sensitive to either touch and vibration(push rods) or electrical currents (mucous sensory glands). Ithas been shown experimentally that the platypus is capable ofregistering the tiny amount of electricity generated in the wa-ter by the tail flick of a shrimp at a distance of around 2 in (5


Family: Duck-billed platypusVol. 12: Mammals I

A single platypus may have several underground burrows, includingone where it incubates its eggs. (Illustration by Katie Nealis)

A duck-billed platypus (Ornithorhynchus anatinus) swimming underwa-ter in Tasmania. (Photo by Erwin & Peggy Bauer. Bruce Coleman, Inc.Reproduced by permission.)

cm). In turn, this information presumably is used to detect aswell as track down the location of prey.

Reproductive biologyTogether with the echidnas, the platypus is distinguished

as a monotreme, or egg-laying mammal. Males and femaleshave a single physical opening (the cloaca) that is used bothfor reproduction and excretion. To help maintain a stream-lined shape, the male’s penis and testes are carried inside thebody; mating occurs in the water. In the female platypus, theright ovary is small and nonfunctional. At the time of ovula-tion, the platypus egg is about 0.16 in (4 mm) in diameter.After being fertilized, the first of three shell layers is formedin the fallopian tube before the egg moves into the uterus.There, the egg is supplied with additional nutrients and twomore shell layers are secreted, so the egg is about 0.6 in (15mm) in diameter when it is laid. Though the time requiredfor gestation has never been determined precisely, it is be-lieved that it takes around three weeks.

Platypus eggs are produced in late winter and spring (Au-gust–November), with some evidence that breeding occurslater in southern populations as compared to those found inQueensland. The eggs are laid in a burrow typically measur-ing 10–20 ft (3–6 m) in length, though sometimes muchlonger. Throughout incubation and juvenile development, thefemale keeps the burrow’s entry tunnel blocked by severalplugs of soil. Besides discouraging access by predators suchas snakes and Australian water rats (Hydromys chrysogaster), theplugs reduce the likelihood that juveniles drown in the eventof a flood. A few days before laying her clutch of one to threeeggs, a female drags a large quantity of wet leaves and othervegetation into the rounded burrow chamber to make a nest.It is believed that the female incubates the leathery-shelledeggs for about 10 days, clasping them between her curled-uptail and belly as she lies on her back or side. When they hatch,the young are less than 0.5 in (9 mm) long. Their emergencefrom the egg is assisted by the presence of a prominent bump(caruncle) at the tip of the snout, an inward-curving egg tooth,and forelimbs armed with tiny claws. When they hatch, theyoung are less than 0.8 in (20 mm) long.

Juveniles develop in the nursery burrow for about fourmonths before entering the water for the first time. Through-

out this period, they are nourished solely on milk. The fe-male does not have nipples. Instead, milk is secreted directlyonto the mother’s fur from two circular patches of skin lo-cated about halfway along her abdomen. An orphaned platy-pus will drink milk from a human hand by sucking up theliquid while sweeping its short bill rhythmically back and forthagainst the palm. In the wild, such sweeping movements mayhelp to stimulate the flow of milk.

Both males and females are physically mature at the age oftwo years, though some females may delay having offspringuntil they are four years old or more. Courtship involves twoindividuals swimming alongside or circling each other, some-times accompanied by nuzzling or rubbing. One animal mayuse its bill to grasp the tip of the other’s tail and be towed orswim behind. Little is known about the platypus breeding sys-tem, apart from the fact that the animals do not appear to formlong-term pair bonds. Instead, it is believed that males tendto move about widely during the breeding season, trying tomate with as many females as possible. By the same token,adult females appear to rear the young without any help fromtheir mates.

Conservation statusThe platypus is a difficult animal to census or survey: bur-

row entrances are generally well hidden and the animals rarelyleave evidence of their activities in the forms of tracks, scats,or food scraps. Live-trapping nets are time consuming to setand must be monitored closely through the night. Accord-ingly, knowledge of how the species is faring is sketchy inmany parts of its range. In broad terms, it is known that theplatypus remains fairly common along some waterways, but


Vol. 12: Mammals IFamily: Duck-billed platypus

A duck-billed platypus (Ornithorhynchus anatinus) walking in the grassin Australia. Usually platypuses are active after dusk and before dawn.(Photo by J & D Bartlett. Bruce Coleman, Inc. Reproduced by permis-sion.)

The bill of a duck-billed platypus (Ornithorhynchus anatinus) is fleshyand covered by soft, sensitive skin. (Photo by © Peter Marsack/LochmanTransparencies. Reproduced by permission.)

has declined or vanished from others. The species is fully pro-tected by law throughout its range.

In most areas, the key factor limiting platypus numbers islikely to be the quality of habitat. Waterways supporting largeplatypus populations generally have plenty of trees andsmaller plants growing on the banks; a varied array of pools,shallow riffles, rocks, and woody materials in the channel; andreliably flowing fresh water throughout the year. All of theseattributes favor the small aquatic invertebrates that in turnfeed the platypus. Conversely, factors implicated in the de-cline of platypus populations include erosion, overgrazing by rabbits and livestock, altered water flow regimes, over-clearing of native vegetation, and the systematic removal oflogs and large branches from the channel.

Besides habitat degradation, the platypus is vulnerableto drowning in nets and traps set illegally for fish and cray-fish. Many individuals also die each year after becoming

entangled in garbage such as abandoned loops of nylonfishing line.

Significance to humansThe platypus was hunted in the nineteenth and early twen-

tieth centuries for its soft fur, which (due to the thickness ofthe skin) was mainly used to make slippers, blankets, and rugs.Today, the animals have no direct economic value apart fromtheir role in attracting tourists to Australia. People living inAustralia generally regard the species with great interest andaffection. Hence, the platypus also has an important role toplay in encouraging landholders and the general communityto protect freshwater environments.


Family: Duck-billed platypusVol. 12: Mammals I

A duck-billed platypus (Ornithorhynchus anatinus) exits the water. (Photoby Mitsuaki Iwago/Minden Pictures. Reproduced by permission.)

The duck-billed platypus (Ornithorhynchus anatinus) lives in a fresh-water habitat, but also forages on land. (Photo by Dr. Lloyd Glenn In-gles © California Academy of Sciences. Reproduced by permission.)

ResourcesBooksAugee, Michael L., ed. Platypus and Echidnas. Mosman, New

South Wales: The Royal Zoological Society of New SouthWales, 1992.

Grant, Tom. The Platypus: A Unique Mammal. Sydney:University of New South Wales Press, 1995.

Moyal, Ann. Platypus: The Extraordinary Story of How a CuriousCreature Baffled the World. Crows Nest, New South Wales:Allen & Unwin, 2001.

PeriodicalsEvans, B. K., D. R. Jones, J. Baldwin, and G. R. J. Gabbott.

“Diving Ability of the Platypus.” Australian Journal ofZoology 42 (1994): 17–27.

Fenner, P. J., J. A. Williamson, and D. Myers. “PlatypusEnvenomation—A Painful Learning Experience.” TheMedical Journal of Australia 157 (1992): 829–832.


Vol. 12: Mammals IFamily: Duck-billed platypus

ResourcesMusser, A. M. “Evolution, Biogeography and Palaeocology of

the Ornithorhynchidae.” Australian Mammalogy 20 (1998):147–162.

Proske, U., J. E. Gregory, and A. Iggo. “Sensory Receptors inMonotremes.” Royal Siety of London Philosophical Transactions353 (1998): 1187–1198.

Serena, M. “Use of Time and Space by Platypus(Ornithorhynchus anatinus: Monotremata) along a VictorianStream.” Journal of Zoology, London 232 (1994): 117–131.

——— “Duck-billed Platypus: Australia’s Urban Oddity.”National Geographic 197, no. 4 (April 2000): 118–129.

Serena, M., and G. Williams. “Rubber and Plastic Rubbish: ASummary of the Hazard Posed to Platypus Ornithorhynchusanatinusin Suburban Habitats.” The Victorian Naturalist 115(1998): 47–49.

Serena, M., M. Worley, M. Swinnerton, and G. A. Williams.“Effect of Food Availability and Habitat on the Distributionof Platypus (Ornithorhynchus anatinus) Foraging Activity.”Australian Journal of Zoology 49 (2001): 263–277.

Temple-Smith, P., and T. Grant. “Uncertain Breeding: AShort History of Reproduction in Monotremes.”Reproduction, Fertility and Development 13 (2001): 487–497.

OrganizationsAustralian Platypus Conservancy. P.O. Box 84, Whittlesea,

Victoria 3757 Australia. Phone: 613 9716 1626. Fax: 6139716 1664. E-mail: [email protected] Web site:<http://www.platypus.asn.au>.

OtherThe Complete Platypus. 2000 [2003]. <http://www.platypus

.org.uk>.

Melody Serena, PhD

Evolution and systematicsThis group of mammals was traditionally included in the

marsupials until 1993 when it was placed in its own order,Didelphimorphia, together with two other New Worldopossum-like families, the Microbiotheriidae (one species)and the Caenolestidae (five species). Here Didelphidae istreated in its own order, Didelphimorphia, and Microbio-theriidae and Caenoletidae are each covered in an order aswell. The fossil record suggests that didelphids are relativelyprimitive, unspecialized mammals that emerged some75–100 million years ago (mya) in North America. Theirevolutionary and biogeographical history is complex; theycolonized Europe, Asia, and Africa some 60 mya, but disap-peared from those continents some 20 million years later,presumably due to competition and predation with the ap-pearance of placental mammals. Twenty mya they were re-stricted to South America, where they underwent animpressive radiation in the absence of other ecologically sim-ilar or predatory placental mammals. It was not until theIsthmus of Panama rose and North and South Americajoined, some three million years ago at the beginning of the

Pleistocene, that the didelphids again entered North Amer-ica. Throughout this time they retained a remarkably stablemorphology. The connection between North and SouthAmerica also allowed the entrance of other placental mam-mals into South America. For the first time in 20 millionyears, marsupials again faced the faster, larger-brained pla-cental competitors and predators. Groups like theBorhyaenids (wolf- or hyena-like marsupials) and Thylacos-milids (marsupial saber-toothed cats) disappeared and gaveway to true canids and felids. Some factors that may havecontributed to their disappearance are the smaller en-cephalization quotient, lower metabolic rate and overallspeed, and lower cursorial abilities of the marsupials com-pared to their placental counterparts. Didelphids have rela-tively low evolutionary rates and a strong stabilizingselection that prevents greater morphological diversificationin the group.

The family Didelphidae is arranged into two subfamilies,Caluromyinae and Didelphinae. As of 2002, 15 genera arerecognized: woolly opossums (Caluromys), black-shouldered


●▲

DidelphimorphiaNew World opossums

(Didelphidae)Class Mammalia

Order Didelphimorphia

Family Didelphidae

Number of families 1

Thumbnail descriptionSmall- to medium-sized terrestrial mammal withlong, naked tail, opposable thumbs both in thehands and feet, long, pointed snout, naked earsthat range from small to large, and medium tolarge eyes; color varies from nearly pure whiteto blackish; some species are unicolored,whereas others have distinct light and darkblotches and bands

Size3–22 in (8–55 cm); 0.9 oz–11 lb (25–5,000 g)


HabitatDry and moist tropical forests, temperate forest,woodland, grasslands, scrub, and mangroves

Conservation statusCritically Endangered: 3 species; Endangered: 3species; Vulnerable: 15 species; NearThreatened: 18 species; Data Deficient: 2species

DistributionNorth America from southern Canada and New England to southern Mexico, CentralAmerica, and South America to southern Argentina and Chile

opossums (Caluromysiops), water opossums (Chironectes), com-mon opossums (Didelphis), bushy-tailed opossums (Glironia),gracile opossums (Gracilinanus), Patagonian opossums(Lestodelphys), lutrine opossums (Lutreolina), mouse opossums(Marmosa), slender mouse opossums (Marmosops), brown four-eyed opossums (Metachirus), woolly mouse opossums (Mi-coureus), short-tailed opossums (Monodelphis), gray four-eyedopossums (Philander), and fat-tailed mouse opossums (Thy-lamys). In 1993, Gardner recognized a total of 61 species, butthere have been at least three additional species describedsince then.

Physical characteristicsNew World opossums are small- to medium-sized mam-

mals. The tail can be almost completely covered with hair oralmost naked, depending on the species, and frequently is bi-colored with the distant half whitish and the base dark. Whenthe tail is naked, it is covered with scales. Tail length is aslong as or longer than the head and body in all genera exceptMonodelphis, in which it is about 50% of the head and bodylength. In most genera, the tail is at least partially prehensile.Ears are always medium to large, rounded and naked, exceptin the genera Lutreolina and Lestodelphys, in which ears areshort. The snout is long and pointed, and eyes are large, some-times bulging, and black or brown. The mouth is large andcan open to a remarkably wide gape. Tooth and skull mor-phology is notably consistent, indicating the relatively lowlevel of specialization in this group. The dental formula isI5/4 C1/1 PM3/3 M4/4 � 2 � 50. The thumbs are oppos-able in the hind feet, giving extremities their characteristicgrasping ability, although the water opossum has webbed feetto aid in swimming action and its thumbs are only slightlyopposable. Arms and legs vary with the genus. Some genera,

like Metachirus, have relatively long legs, whereas others likeMonodelphis and Lestodelphys have relatively short legs. Exceptfor a few species such as Monodelphis dimidiata, there is no sex-ual dimorphism.

Coloration varies widely. Some species are uniformly black-ish, while others are almost completely whitish; other speciesare rusty reddish, gray, brown, tan, or yellowish brown. Un-derparts are nearly always paler than the dorsum. The venterof the water opossum is silvery white. Two genera have dis-tinct dark blotches above the eyes; they are called four-eyedopossums. Some genera have characteristic dark and pale pat-terns, sometimes broad, dark saddle-like bands across the back,sometimes a longitudinal stripe along the dorsal spine and con-tinuing along the top of the snout and to the tip of the nose.The hair can be short or long depending on the species, butit is always dense. In females of some genera, there is a dis-tinct ventral pouch where young are kept in the developmen-tal stages. The pouch opens circularly and can be almostcompletely closed. Mammae number 12 to 18 and are arrangedin a circle with one in the center. One species, the water opos-sum, has a pouch that seals hermetically with an oily substanceso that females can dive under the water surface withoutdrowning the young that are attached to the nipples. Likewise,males of this species have a pouch, which protects the scro-tum and testicles from contact with the water.

DistributionIndividuals belonging to this family inhabit only the New

World, from Patagonian Argentina and Chile north to


Vol. 12: Mammals IMonotypic order: Didelphimorphia

The bare-tailed woolly opossum (Caluromys philander) is a marsupial.(Photo by Jany Sauvanet/Photo Researchers, Inc. Reproduced by per-mission.)

A Virginia opossum (Didelphis virginiana) peers out from tree trunknest. (Photo by Animals Animals ©Carson Baldwin, Jr. Reproduced bypermission.)

southern Canada and the northeastern United States. Theyare much more diverse in the tropical and subtropical re-gions between Mexico and Argentina, while only a singlespecies, the Virginia opossum (Didelphis virginiana), extendsinto the United States and Canada. Because of their longperiod of evolutionary isolation in South America, manygenera and species can only be found in that subcontinent.The genera Thylamys, Lestodelphys, one species of Didelphis(D. aurita), three of the six species of Gracilinanus (G. ace-ramarcae, G. agilis, and G. microtarsus), two species of Mar-mosops (M. dorothea and M. incanus), one of Micoureus (M.constantiae), and 10 species of Monodelphis (M. americana, M.dimidiata, M. domestica, M. iheringi, M. kunsi, M. osgoodi, M.rubida, M. scallops, M. sorex, and M. unistriata) are restrictedto South America south of the Amazon river. Several speciesof Marmosa, Marmosops, and Thylamys are known only fromthe type localities, and several genera such as Caluromysiopsand Glironia and species such as Gracilinanus emiliae, Mar-mosa rubra, and Monodelphis americana are restricted to theAmazon basin.

The Virginia opossum is one of the most widespreadspecies in the family, and the only one with a distribution ex-tending well beyond that of any other species. Virtually allother species coexist with one or more additional species ofdidelphids, but in all of the United States and southernCanada, the Virginia opossum is the only species present.Most species inhabit tropical habitats, but a few species, re-markably in the genera Thylamys and Lestodelphys, are adaptedto temperate ecosystems, and inhabit only the southern lati-tudes of Chile and Argentina.

HabitatThe family Didelphidae can be found in a wide variety of

habitats, from moist and dry tropical forests to cloud forests,mangrove swamps, grasslands, scrub, and even into temper-ate forests. One species, the lutrine opossum or thick-tailedopossum (Lutreolina crassicaudata) is considered to be stronglyadapted to life in the South American grasslands or pampas,

and readily enters lakes and streams where it swims remark-ably well. Another species, the water opossum (Chironectesminimus), has as a primary habitat of streams and lakes inmoist forests, making its dens in the banks.

Many species are able tree climbers and also move aroundon the ground; some individuals have been found high in trop-ical moist forest canopy trees. Other species are predomi-nantly terrestrial, such as the members of the generaMonodelphis and Metachirus, and appear clumsy if placed intrees, even low to the ground.

Because of their long period of evolutionary isolation inSouth America, opossums were able to invade virtually everyhabitat available at every latitude and from sea level to almost13,100 ft (4,000 m) above sea level. Most species, however,have a relatively restricted habitat and geographic range. Onlyspecies such as Didelphis virginiana and D. marsupialis can befound in several varying habitats, from temperate forests totropical moist and dry forests to mangrove swamps.

Some species are able to exist in human-modified habitatsand a few may even benefit from these, by invading banana,coffee, and citrus plantations, corn fields, and other agroe-cosystems. Other species seem particularly adept at using for-est edges and secondary vegetation. Finally, many otherspecies depend on undisturbed habitats and do not toleratedisturbance or deforestation.

BehaviorNearly all species in the family are nocturnal, although oc-

casionally diurnal sightings of mouse opossums and water opos-sums have been reported, and some species of Monodelphis arereportedly primarily diurnal. Many scansorial species take tothe trees when threatened, whereas terrestrial species run witha characteristic gait. No species is particularly fast during es-cape behavior. One species, the Virginia opossum, feigns deathwhen threatened by a predator, lying on its side, gaping itsmouth spasmodically, and emitting a strong musky smell. Otherdefense behaviors found in the family include gaping and snap-ping at intruders while hissing loudly and secreting musk from


Monotypic order: DidelphimorphiaVol. 12: Mammals I

A Virginia opossum (Didelphis virginiana) feeds on wild muscadinegrapes. (Photo by Animals Animals ©Fred Whitehead. Reproduced bypermission.)

A southern opossum (Didelphis marsupialis) wards off a dog. (Photoby Joe McDonald. Bruce Coleman, Inc. Reproduced by permission.)

the anal region. The water opossum dives under the surfaceand then propels itself with strong strokes from the hind legs.

All opossums are primarily solitary, avoiding contact witheach other. After dispersal, juveniles do not keep contact.Males and females come in contact only during the female es-trus for a short period of time. Individuals generally remainin a home range, but this is almost never defended. Instead,when two animals coincide in space and time, they avoid eachother. At least in the bare-tailed woolly opossum, Caluromysphilander, social dominance is clearly established on the basisof age and body mass. Older, heavier males dominate younger,lighter ones, and agonistic behavior is exacerbated by the pres-ence of females. Interspecific aggression may occur only as aresult of the generalized opportunistic behavior to procurefood; one Didelphis reportedly attacked, killed, and partiallyconsumed a Philander opossum after an encounter.

Opossums are silent animals the vast majority of the time;sounds are produced only when they are threatened and theseare only hisses and explosive gasps. Foraging behavior is ex-ploratory and continuous. Opossums use primarily their senseof smell to locate food. Stalking is seldom used to capture an-imal prey, but sight and hearing are continually used in the

search for food. Young opossums, particularly mouse opos-sums, emit a loud chirping cry when detached from the fe-male’s nipple. This induces the female to approach and graspthe young, and push it under the venter, where it reattachesitself to the nipple.

Predators of opossums include a variety of snakes, foxes,owls, ocelot (Leopardis pardalis), puma (Puma cencolor), andjaguar (Panthera onca). Indigenous human groups in theNeotropical region often include the larger species of opos-sums in their diet. Didelphis albiventris has been shown to havean antibothropic biochemical factor in its blood and milk thatneutralizes the venom of poisonous snakes.

Longevity records in the wild rarely reach two years, withmany species barely surpassing one year. In captivity,longevity is extended with reports of three to five years forspecies such as Marmosa robinsoni, Caluromys philander, andChironectes minimus. The record is seven years for a captiveCaluromysiops irrupta.



A red mouse opossum (Marmosa rubra) shows aggressive behavior.(Photo by Art Wolfe/Photo Researchers, Inc. Reproduced by permission.)

A murine mouse opossum (Marmosa murina) eats fruit after dark ona branch 15 ft (4.6 m) above ground in the lowland Amazon rainfor-est of northeast Peru. (Photo by Gregory G. Dimijian/Photo Re-searchers, Inc. Reproduced by permission.)

Feeding ecology and dietNew World opossums are generalist omnivores. Food

items include insects, insect larvae, worms and other inverte-brates, bird’s eggs and nestlings, fruit, carrion, reptiles, am-phibians, birds, and small mammals. Almost all species areomnivorous with varying degrees of frugivorous or carnivo-rous tendencies. Species in the genera Caluromys andCaluromysiops are considered primarily frugivorous, althoughthey do include animal matter in their diet. Smaller speciessuch as those in the genera Marmosa, Marmosops, Gracilinanus,etc., tend to be primarily insectivorous with some eggs, fruit,and meat also included. Mouse opossums kept in captivity willnot hesitate to attack large moths or grasshoppers, graspingthem with their hands and quickly administering killing bitesall over the body of the insect. They normally discard thewings and legs, and other chitinous, undigestible pieces.Caterpillars are rapidly rolled and rubbed against substratesto remove stinging hairs. Fruit can be plucked off treebranches directly or can be eaten after the fruit has fallen tothe ground. Sweet, juicy fruits are preferred, such as zapotes,blackberries, guavas, chirimoyas, etc., although other drierfruits such as wild figs and wild cacao, as well as introduced,human-grown varieties like bananas, figs, citrus fruits, apples,and cherries, are also consumed. Common and four-eyedopossums take large amounts of fruit from secondary forestspecies such as Cecropia. Common opossums (Didelphis) seemto be better seed dispersers and to invest more in seeking fruitsof Cecropia than gray four-eyed opossums (Philander).

The water opossum (Chironectes minimus) is particularly in-teresting in that it seems to be the only New World opossumspecies that is completely carnivorous. This species feedsmainly on fish, crustaceans, mollusks, and frogs. Its long fin-gers and bulbous fingertips are held outstretched while theanimal swims. Under water, their hands are used to feel un-der rocks and logs for potential prey. They coexist and over-lap locally with the common Neotropical otter (Lontralongicaudis). In the Old World, in Africa and Asia, commonotters coexist with clawless or small-clawed otters (generaAonyx and Amblonyx), which have similar habits and handmorphology to the water opossum. This allows them to co-exist by partitioning food resources. The water opossum andthe otter may be in the same situation, with the otter feedingprimarily on fish and less on crustaceans and mollusks,whereas the opossum probably takes more invertebrates thanfish.

In Mediterranean habitats of South America, Thylamys el-egans has been shown to regulate the frequency of torpor pe-riods, and therefore energy expenditure, by the availability offood. When food is plentiful, animals never enter torpor, andfrequency of torpor periods increases with decreasing foodavailability.

Reproductive biologyInformation on reproduction is available for only a few

species. Some species show one defined reproductive eventduring the year that coincides with the greatest seasonal abun-dance of food. Other species, particularly those inhabiting

more tropical climates, may have two reproductive periodsevery year or even have an indistinct pattern in which repro-ductive females can be found in every month of the year.

New World opossums are polygamous. Like other marsu-pials, have a very short gestation period, followed by a longdevelopmental period. After a gestation between 12 and 15days, the embryo-like newborn, naked, with eyes and earsclosed but strong arms and well-developed claws, crawls alonga path between the cloaca and the marsupium (or mammaryregion in those species with no marsupium) that has beenlicked by the female. Once in the mammary region, each in-dividual attaches to a nipple, where it will remain for four toeight weeks, depending on the species. Offspring can then de-tach from the nipples for the first time. When they are toolarge to fit in the female’s pouch, they crawl on her back orare simply dragged behind her, while still attached to themammae. Young remain dependent on their mothers untilthey are two to four months old, after which they are weanedand proceed to disperse.

Litter size varies greatly in different genera. Five to 12 andup to 16 offspring are born in Monodelphis, two to five inCaluromys, four to 12 in Marmosa, two to five in Chironectes,six to 15 in Didelphis, and one to nine in Philander. Likely,many more young are born than those found by scientists at-tached to the mammae, but they die before they can attachthemselves to a nipple.

Sexual maturity is attained at three to nine months in dif-ferent genera. Many species construct nests inside rotten treesboth standing and fallen, while others have nests on theground or, in the case of the water opossum, in tunnels ex-cavated in stream banks. Some species of mouse opossum uti-lize hummingbird nests as their own resting places. NewWorld opossums use primarily plant matter to construct thespherical nests. These materials are transported in the par-tially rolled-up tail while the animal moves to the nest.

Many species are semelparous with males dying shortly af-ter mating and females after weaning their first and only lit-



A southern opossum (Didelphis marsupialis) with its young. (Photo byLaura Riley. Bruce Coleman, Inc. Reproduced by permission.)

ter produced. Females of some species, however, can breedtwice in the same year with only a few months apart betweenbirths, and individuals of a few species can have two years ofreproductive activity.

Conservation statusOf the species recognized by Gardner in 1993, three (Gra-

cilinanus aceramarcae, Marmosa andersoni, and Marmosops han-dleyi) are considered Critically Endangered by the IUCN, andthree other species (Marmosa xerophila, Marmosops cracens, andMonodelphis kunsi) are considered Endangered. All three Crit-

ically Endangered species have extremely restricted distribu-tions, limited to one or two localities in Bolivia or Colombia.Although none of these species face direct threats from hu-mans, all are facing rampant habitat destruction that hasstrong negative conservation implications. The three Endan-gered species face the same threats of habitat destruction andrestricted distributions in Colombia, Venezuela, Bolivia, andBrazil, albeit slightly larger than the Critically Endangeredspecies. Fifteen additional species are considered Vulnerable,18 more are under the category of Lower Risk/Least Con-cern, and two are Data Deficient. There are 20 species thathave not been ranked by the IUCN. Undoubtedly otherspecies are facing conservation threats, especially those withrestricted distributions and found in habitats affected by highrates of deforestation, but much more information is neces-sary to correctly assess their status.

In Mexico, two species, the water opossum and the woollyopossum, are included in the list of species at risk as endan-gered. These two species are considered sensitive to habitatdisruption and their populations have been severely decreasedas a result of deforestation and water pollution by dischargeof fertilizers and pesticides.

Significance to humansSpecies such as the common opossums and even some four-

eyed and mouse opossums frequently benefit from human-induced habitat changes. Some humans find opossum speciesattractive as pets, and their tanned pelts used to have somevalue in the fur market, especially at the end of the nineteenthcentury. In the tropics, mouse opossums and short-tailedopossums are valued for controlling of cockroaches, scorpi-ons, and other unwanted animals, especially in rural settle-ments. Virginia, common, and four-eyed opossums aresometimes used as food by indigenous and other human pop-ulations. Colonies of some species, notably Monodelphis, arekept for developmental and biomedical research.

Opossums are sometimes considered pests because of theirraids on commercially valuable fruits in orchards and agri-cultural fields, as well as on poultry farms. The southern opos-sum, Didelphis marsupialis, has been identified as one of thekey hosts of the parasitic protozoan Trypanosoma cruzi, whichcauses Chagas’ disease. Chagas’ disease is transmitted to hu-mans when an infected kissing, or assassin, bug (Hemiptera:Reduviidae; genus Triatoma) bites a human to feed on theblood and then defecates on the skin. The person thenscratches the bite and transports the protozoans through anopen wound into the body. Sixteen to 18 million people areinfected, and 50,000 of these die annually. Other species ofmammals have also been identified as hosts.



A Virginia opossum (Didelphis virginiana) uses its tail as an aid inclimbing down. (Photo by Animals Animals ©Ted Levin. Reproduced bypermission.)


1 2

3

4

5

6

1. Bare-tailed woolly opossum (Caluromys philander); 2. Bushy-tailed opossum (Glironia venusta); 3. Water opossum (Chironectes minimus); 4.Patagonian opossum (Lestodelphys halli); 5. Virginia opossum (Didelphis virginiana); 6. Thick-tailed opossum (Lutreolina crassicaudata). (Illus-tration by Jonathan Higgins)


1

2

3

4

56

1. Alston’s woolly mouse opossum (Micoureus alstoni); 2. Pygmy short-tailed opossum (Monodelphis kunsi); 3. Gray slender mouse opossum(Marmosops incanus); 4. Mexican mouse opossum (Marmosa mexicana); 5. Red-legged short-tailed opossum (Monodelphis brevicaudata); 6. Grayfour-eyed opossum (Philander opossum). (Illustration by Jonathan Higgins)

Bare-tailed woolly opossumCaluromys philander

SUBFAMILYCaluromyinae

TAXONOMYDidelphis philander (Linnaeus, 1758), America, restricted toSurinam; Ghana.

OTHER COMMON NAMESFrench: Opossum laineux; German: Gelbe Wollbeutelratte;Spanish: Tlacuache lanudo, comadreja lanuda, cuica lanuda.

PHYSICAL CHARACTERISTICSLength 7–10 in (18–28 cm); weight 6.0–15 oz (180–450 g).The back is nearly uniform cinnamon brown and the face isgray with brown bulging eyes, with a black fine line betweenthe eyes. Ears are large, naked, pink, and membranous. Morethan half of the tail is furry.

DISTRIBUTIONVenezuela, Trinidad and Tobago, Guyana, Suriname, FrenchGuiana, and Brazil.

HABITATPrimary and secondary tropical lowland moist forest in bothswampy and well-drained areas, from sea level up to about2,000 ft (600 m). Rarely, it has also been found in plantationsand other agroecosystems. Often found high in the canopy butalso rarely seen on the ground or close to it.

BEHAVIORThis is a solitary species. The only groups reported are thosecomposed of a female and her suckling young attached to themammae. Primarily arboreal and rarely abandons the shelter ofthe high and medium canopy. They are primarily nocturnaland crepuscular, decreasing their activity in periods of highlevels of lunar illumination.

FEEDING ECOLOGY AND DIETFeeds primarily on fruits but also takes some leaves, insects,bird eggs, and nestlings.

REPRODUCTIVE BIOLOGYPolygamous. Females construct nests with plant matter insidehollow trees. After a brief gestation of less than 15 days, one tosix young are born blind, naked, and with closed ears. Theyoung crawl to the nipple area, where each attaches to one.There is no well-developed pouch, only lateral folds of skin.Reproduction may occur throughout the year but most fre-quently at the start of the rainy season.

CONSERVATION STATUSSeems to be dependent on undisturbed tropical moist forest,although it has sometimes been found in secondary vegetation.Destruction of its habitat is the most serious threat. TheIUCN lists the species as Lower Risk/Near Threatened.

SIGNIFICANCE TO HUMANSIt is sometimes kept as a pet, and otherwise the species is con-sidered harmful to banana and citrus plantations. ◆

Water opossumChironectes minimus

SUBFAMILYDidelphinae

TAXONOMYLatra minima (Zimmerman, 1780), Cayenne, French Guiana.

OTHER COMMON NAMESFrench: Opossum aquatique; German: Schwimmbeutler; Span-ish: Tlacuache de agua, cuica de agua, yapok, zorro de agua,comadreja de agua.

PHYSICAL CHARACTERISTICSLength 10.6–15.7 in (27–40 cm); weight 21.2–28 oz (600–790g). Dense and silky hair with four to five broad dark brownbands across the back joined along the dorsal spine. Venter issilvery white and tail is almost naked and scaly. The eyes arelarge and black, and the face has another dark band across theeyes. The tail is slightly flattened laterally and bicolored, withthe distant half whitish. The toes are clearly webbed to aid inswimming.


Species accounts


Caluromys philander

Didelphis virginiana

DISTRIBUTIONSouthern Mexico, through Central America, Colombia,Venezuela, Guyana, Suriname, French Guiana, Ecuador, Peru,Brazil, Bolivia, Paraguay, and Argentina.

HABITATRivers and streams in primary lowland tropical moist forest,generally from sea level up to about 3,300 ft (1,000 m), al-though it has been found at 6,230 ft (1,900 m).

BEHAVIORA solitary species that swims under water to avoid danger. It isprimarily nocturnal, secretive, and silent.

FEEDING ECOLOGY AND DIETFeeds mainly on fish, crustaceans, and mollusks. This is themost carnivorous of the New World opossums.

REPRODUCTIVE BIOLOGYPolygamous. The female constructs a den on the bank of ariver or stream where she builds a nest with vegetation. Theyoung are born very undeveloped after a short gestation. Thefemale keeps the young in a well-developed pouch that closeshermetically when she swims. The male also has a marsupiumto protect the testicles.

CONSERVATION STATUSConsidered Lower Risk/Near Threatened by the IUCN, butthe water opossum has disappeared from many areas in its his-torical distribution. Deforestation and water pollution are twofactors that determine their local extinction.

SIGNIFICANCE TO HUMANSNone known. ◆

Virginia opossumDidelphis virginiana


TAXONOMYDidelphis virginiana Kerr, 1792, Virginia, United States.

OTHER COMMON NAMESFrench: Opossum de Virginie; German: Nordopossum; Span-ish: Tlacuache común, tlacuache norteño.

PHYSICAL CHARACTERISTICSLength 14–21.6 in (35–55 cm); weight 28–176 oz (800–5,000g). Long hair and dense underfur; colors vary from uniformwhitish to blackish brown. Ears are black and naked, andcheeks are white. Tail nearly naked, scaly, and bicolored: thebasal half is black and the distal half whitish. The feet have op-posable thumbs that render their footprints unmistakable.

DISTRIBUTIONExtreme southwestern Canada, the west coast and the easternhalf of the United States, tropical and subtropical Mexico, andCentral America south to Costa Rica.

HABITATTropical and temperate forests, in wet and subhumid ecosys-tems. Found in a wide variety of human-disturbed habitatsfrom logged and secondary forests to agricultural lands andeven landfills and urban areas.

BEHAVIORSolitary and nocturnal. Roosts in hollow trees and branches, inleaf litter, crevices and caves under rocks, and in the soil.Feigns death when threatened, gaping its mouth wide and ly-ing on its side while emitting an offensive musky odor.

FEEDING ECOLOGY AND DIETOmnivorous. Eats fruit, insects, eggs, small vertebrates, spoiledfruit, carrion, and even trash. Forages at night opportunisticallyand avoids other medium and large-sized mammals such asraccoons and skunks. It is not a good hunter but rather eatsitems that are easily available.

REPRODUCTIVE BIOLOGYPolygamous. The female builds a nest with leaf litter and vege-tation that she transports with the help of the tail. The repro-ductive season extends from January through July and twobirth peaks are reported. After a gestation of about 13 days, asmany as 21 young are born undeveloped. Only the first tomake it to the pouch are able to survive, as the female has only13 teats and rarely are all occupied by a young one.

CONSERVATION STATUSNot threatened. Inhabits both pristine and modified ecosys-tems. They have colonized towns and cities and they are notrare in New York City, Miami, or other large cities. Thespecies does not face any immediate threats of extinction.

SIGNIFICANCE TO HUMANSSometimes consumed for food by indigenous or mixed humangroups. The species has been pointed out as an agriculturalpest or a disease reservoir. ◆



Lestodelphys halli

Chironectes minimus

Bushy-tailed opossumGlironia venusta


TAXONOMYGlironia venusta Thomas, 1912, Huánuco, Peru.

OTHER COMMON NAMESGerman: Buschschwanzbeutelratten; Spanish: Comadreja decola peluda, zarigüeya de cola peluda.

PHYSICAL CHARACTERISTICSLength 6.3–8.3 in (16–21 cm). The hair on the back is denseand soft, uniformly cinnamon brown. The venter is grayish tobrownish white. The tail is long and completely furred withonly part of the ventral surface naked, which gives this speciesits common name. There are two large blackish patches sur-rounding the eyes, separated by a brown stripe along the top ofthe snout.

DISTRIBUTIONEastern Amazonia in western Brazil, Ecuador, Peru, and Bo-livia.

HABITATIt has been found only in intact lowland tropical moist forest,up to an altitude of 2,600 ft (800 m).

BEHAVIORNot much is known about this species. Considered arboreal onthe basis of the specimens found in trees and the morphologyof the hand with well-developed grasping abilities.

FEEDING ECOLOGY AND DIETPrimarily a insectivorous species, but likely it also feeds onfruit, eggs, and small vertebrates.

REPRODUCTIVE BIOLOGYPolygamous, but nothing else is known.

CONSERVATION STATUSConsidered Vulnerable by the IUCN. Habitat destruction isthe primary threat. There is no information on effects of habi-tat loss.


Patagonian opossumLestodelphys halli


TAXONOMYNotodelphys halli (Thomas, 1921), Santa Cruz, Argentina.

OTHER COMMON NAMESFrench: Opossum de Patagonie; German: Patagonien-Beutelratten; Spanish: Comadrejita patagónica.

PHYSICAL CHARACTERISTICSLength 5–6 in (13–15 cm). The dorsal hair is dense and soft,dark grayish brown with paler sides. Males have an orangepatch on the throat. The face is paler than the rest of thebody. There are dark patches on shoulders and hips, and theunderparts, hands, and feet are white. The tail is clearlyshorter than the head and body, and seasonally it appears thickfrom fat reserves. Tail furry only at the base and covered withfine hairs the rest of its length. Canine teeth are relativelylong.

DISTRIBUTIONOccurs in a relatively small region of southern Argentina in theprovinces of Río Negro, Neuquén, Santa Cruz, La Pampa,Mendoza, and Chubut.

HABITATIt has been reported from the South American steppe grass-lands (pampas), and also from shrublands; often associated withstreams and other water bodies.

BEHAVIORSeems to be a primarily terrestrial species. It is solitary and ac-tive at night.

FEEDING ECOLOGY AND DIETA specimen was captured in a trap baited with a dead bird.This species is considered a carnivore but more likely it is in-sectivorous. Its diet may also include fruit, eggs, and small ver-tebrates.


CONSERVATION STATUSThe distribution is restricted to a small region of southern Ar-gentina. Classified as Vulnerable. Some portions of its habitathave been modified.




Glironia venusta

Marmosops incanus

Thick-tailed opossumLutreolina crassicaudata


TAXONOMYDidelphis crassicaudata (Desmarest, 1804), Asunción, Paraguay.

OTHER COMMON NAMESEnglish: Little water opossum; French: Opossum á queuegrasse; German: Dickschwanzbeutelratte; Spanish: Comadrejacolorada, coligrueso.

PHYSICAL CHARACTERISTICSLength 10–16 in (25–40 cm); weight 7–19 oz (200–540 g). Thedense, soft, and relatively short hair is uniformly light cinna-mon to dark brown and paler below. The legs are relativelyshort and the body is elongated with a long neck; the ears areshort; the tail is long and almost completely furred, except forthe ventral surface. There is a well-developed pouch.

DISTRIBUTIONAs understood in 2002, the distribution is disjunct, with onepopulation occurring in eastern Colombia, southern Venezuela,and Guyana, and another in eastern Bolivia, northeastern Ar-gentina, southern Brazil, Paraguay, and Uruguay, from an alti-tude of 1,970–6,560 ft (600–2,000 m).

HABITATFound in lowland and mid-elevation tropical moist forests,grasslands, and shrublands, as well as in forest edges. Alwaysassociated with streams and rivers.

BEHAVIORRoosts in hollows in trees, dens of other animals, and nestsconstructed among the vegetation. An excellent swimmer and

also a good climber, this is a nocturnal species. It is apparentlythe only species of didelphid that can be accommodated incaptivity in small groups, with a weak social structure that per-mits coexistence of two to three animals.

FEEDING ECOLOGY AND DIETPrimarily carnivorous, feeding on small vertebrates on land andin the water, as well as crustaceans, insects, and other small an-imals. An antibothropic biochemical factor has been isolatedfrom its blood, indicating some level of immunity to thevenom of snakes.

REPRODUCTIVE BIOLOGYPolygamous. Gestation lasts about two weeks. Females givebirth to the young in a very undeveloped state. These crawlinto the pouch where they attach themselves to a nipple. Birthsoccur twice during the year.

CONSERVATION STATUSNot listed by the IUCN. It seems to be adaptable to a certaindegree of disturbance and can be locally common in some areas.

SIGNIFICANCE TO HUMANSSometimes considered a nuisance because of its occasionalraids on henhouses. ◆

Mexican mouse opossumMarmosa mexicana


TAXONOMYMarmosa murina mexicana Merriam, 1897, Oaxaca, Mexico.

OTHER COMMON NAMESSpanish: Ratón tlacuache, tacuazín.

PHYSICAL CHARACTERISTICSLength 4.7–6.7 in (12–17 cm); weight 0.9–3.2 oz (26–92 g).The back is uniformly reddish brown to grayish brown. Thetail, which is prehensile, is about as long as the head and bodyand 90% of its length is naked. The feet and undersides arepaler, sometimes white. There are two large black patches sur-rounding the large, black eyes. The ears are large, rounded,and naked.

DISTRIBUTIONFrom eastern and southern Mexico south through centralAmerica to western Panama, from sea level up to about 5,900ft (1,800 m).

HABITATThe main habitat is tropical moist forest, but it can also befound in dry tropical forest, secondary forests and disturbedvegetation, and mangrove forests.

BEHAVIORA nocturnal species that is primarily arboreal, although it canalso be found on the ground. The mouse opossum readily eatsin captivity, quickly attacking and consuming any large insects,eggs, or small vertebrates. It has been found resting insideabandoned hummingbird nests.

FEEDING ECOLOGY AND DIETPrimarily insectivorous but also eats some fruit, bird eggs, andnestlings, and other prey similar in size.



Marmosa mexicana

Lutreolina crassicaudata

REPRODUCTIVE BIOLOGYPolygamous. Gestation is about 14 days long. The females donot have a marsupium, so the newborn crawl to the mammaeand attach themselves to the nipples, which may number from11 to 15. As they grow larger, the young begin traveling on themother’s back, sometimes curling their tails around hers. Re-productive season extends at least from March through August.

CONSERVATION STATUSThe species is not listed by the IUCN. Since it is found inboth undisturbed and modified habitats, it probably is not fac-ing major conservation problems.

SIGNIFICANCE TO HUMANSSometimes these opossums are kept as pets in rural communi-ties. Some individuals have been found as stowaways in bananashipments to New York City. ◆

Gray slender mouse opossumMarmosops incanus


TAXONOMYDidelphis incana (Lund, 1840), Minas Gerais, Brazil.

OTHER COMMON NAMESNone known.

PHYSICAL CHARACTERISTICSLength 4.7–7.9 in (12–20 cm); weight 1–1.9 oz (30–55 g). Dor-sal fur is grayish brown to brown and underparts paler. Thesnout is long and pointed and the ears are large, naked, andpink to brown. There is a patch of black hair around each eye.The tail is long and naked.

DISTRIBUTIONEndemic to eastern Brazil from the state of Bahia to Parana.

HABITATFound in the Atlantic forest of the southeastern coast of Brazil,below 2,640 ft (800 m), in tropical moist forest and deeper in-land in somewhat drier forest.

BEHAVIORNocturnal and crepuscular. Solitary.

FEEDING ECOLOGY AND DIETFeeds on insects, eggs, fruit, and small vertebrates.

REPRODUCTIVE BIOLOGYPolygamous. A semelparous species in which individuals investall their effort on a single reproductive event in their lives.Typically, the births occur in a single three-month periodaround the onset of the rainy season.

CONSERVATION STATUSConsidered Lower Risk/Near Threatened by the IUCN. TheAtlantic forest of Brazil is one of the most endangered biomesof South America and, if deforestation trends continue, thisand other species will face very serious extinction risks.


Alston’s woolly mouse opossumMicoureus alstoni


TAXONOMYCaluromys alstoni ( J. A. Allen, 1900), Cartago, Costa Rica.

OTHER COMMON NAMESFrench: Souris-opossum laineuse d’Alston; Spanish: Zorricí.

PHYSICAL CHARACTERISTICSLength 6.7–7.9 in (17–20 cm); weight 2–5.3 oz (60–150 g).One of the largest mouse opossums. The dorsal hair is yellow-ish brown to reddish; underparts are paler. Distinct black maskover each eye. The tail is long, slender, and naked. There is nomarsupium. The feet have strongly opposable thumbs.

DISTRIBUTIONCaribbean coast of Central America from Belize to Panamaand into Colombia, and also in some Caribbean coastal islands.

HABITATInhabits lowland tropical moist forest and cloud forest below5,250 ft (1,600 m), and also areas of secondary forest.

BEHAVIORNocturnal and solitary. Primarily moves in tree canopies andfrom branch to branch, but can also be found occasionally onthe ground.

FEEDING ECOLOGY AND DIETPolygamous. Feeds on insects, eggs, fruit, and small verte-brates. Attacks its prey by grasping it with its hands and apply-



Micoureus alstoni

Philander opossum

ing a series of quick bites all over the body of the prey. Thenit is consumed from the head down. Legs and wings of insectsare discarded.

REPRODUCTIVE BIOLOGYPolygamous. Females build spherical nests with vegetation anddebris. After a short gestation of less than two weeks, theyoung are born in a very undeveloped state. Births have beenreported almost in every month of the year. Litter size variesfrom two to about 14 young.

CONSERVATION STATUSThe IUCN classified this species as Lower Risk/Near Threat-ened. Severe deforestation in Central America is likely having astrong negative impact on this and other species of the region,although it has been found in some protected areas in CostaRica.


Red-legged short-tailed opossumMonodelphis brevicaudata


TAXONOMYDidelphis brevicaudata (Erxleben, 1777), Surinam.

OTHER COMMON NAMESGerman: Kurzschwanz-Spitzmausbeutelratte; Spanish: Colicortode patas rojas.

PHYSICAL CHARACTERISTICSLength 4.7–7 in (12–18 cm); weight 1.6–3.5 oz (45–100 g).Legs are relatively short as is the tail. Hair is relatively rigid,short, and dense. Color pattern is variable. The back can bedark gray, grizzled with pale hair tips. The sides are rich deepreddish and the change between the gray and red is a verysharp line. Underparts vary from pale, almost white, to lightbrown. Some individuals are reddish all over the back. Thesnout is conical, and the ears are rounded, dark, and naked.The tail is relatively short and hairy only at the base and dorsalsurface of the basal one-third.

DISTRIBUTIONVenezuela, Guyana, Suriname, French Guiana, and Brazilnorth of the Amazon river. This species seems restricted to thenorthern half of the Amazon river basin.

HABITATTropical moist forest in pristine and modified conditions. Canalso be found in orchards and other agroecosystems, but usu-ally upland and away from rivers and streams. It has beenfound only below 2,620 ft (800 m).

BEHAVIORThis is among the few diurnal species in the family. It is alsoone of the least adapted to climbing and moving in trees; themajority of reports describe it as a terrestrial or strictly terres-trial species.

FEEDING ECOLOGY AND DIETFeeds primarily on insects, rodents, birds, eggs, and some fruit.It hunts opportunistically, running and searching through theforest floor under the litter, under logs, and in hollow treesand fallen logs.

REPRODUCTIVE BIOLOGYPolygamous. Breeding has been reported almost in everymonth of the year. Nests are built with plant matter inside orunder fallen or hollow logs. The young are born after a gesta-tion of about 15 days. Litters number between five and 12young. As there is no marsupium, the young are attached tothe female’s nipples and are dragged under her. As they grow,they begin to travel clinging to their mother’s back or sides.

CONSERVATION STATUSThis species is not listed by the IUCN. Although it has beenfound mainly in undisturbed forest, it seems able to survivealso in modified forests and agroecosystems.


Pygmy short-tailed opossumMonodelphis kunsi


TAXONOMYMonodelphis kunsi Pine, 1975, Beni, Bolivia.

OTHER COMMON NAMESFrench: Opossum á queue courte de Kuns; German: Kuns-Spitzmausbeutelratte; Spanish: Colicorto pigmeo.



Monodelphis kunsi

Monodelphis brevicaudata

PHYSICAL CHARACTERISTICSLength 2.4–3.1 in (6–8 cm); weight 0.6–1.2 oz (18–35 g). Theback is uniform yellowish brown with paler underparts. The furis short and dense. There is a gular gland in males, partially ob-scured by fur. The tail is short, slender, and almost completelycovered with fine, sparse hair, except for its tip. The rostrum isconical and the eyes black. The ears are medium and naked.This is the smallest species in the genus Monodelphis.

DISTRIBUTIONKnown only from a few localities in western Brazil and westernBolivia, apparently endemic to the upper Amazon river basin,below 2,100 ft (640 m).

HABITATTropical moist forest, and maybe also some secondary vegetation.

BEHAVIORProbably solitary. It may also be nocturnal, but almost nothingis known about this species.

FEEDING ECOLOGY AND DIETPresumably feeds on insects and other small animals.


CONSERVATION STATUSClassified by the IUCN as Endangered. Since this is a rela-tively rare species in nature, and western Amazonia is subjectto major deforestation, the species faces serious extinctionthreats.


Gray four-eyed opossumPhilander opossum


TAXONOMYDidelphis opossum (Linnaeus, 1758), Paramaribo, Surinam.

OTHER COMMON NAMESFrench: Opossum á quatre yeux; German: Vieraugenbeutel-ratte; Spanish: Tlacuache cuatro ojos, zorro cuatro ojos, co-madreja cuatro ojos.

PHYSICAL CHARACTERISTICSLength 8–13 in (20–33 cm); weight 7–24.7 oz (200–700 g).This relatively large opossum has dense and relatively shorthair that varies from pale gray to dark gray dorsally and yel-lowish white ventrally. The cheeks and chin are also yellowishwhite, as are two conspicuous spots just above the eyes, whichgive this species its common name. The ears are large and

naked, blackish with pink bases. There is a marsupial pouchthat stains orange if the female has had young. The tail inmost individuals is bicolored with the base dark and the finalthird to half white, naked, and scaly except the basal 0.8 in (2cm), which are furred.

DISTRIBUTIONFrom eastern and southern Mexico south through CentralAmerica and into South America to Bolivia, Paraguay, north-eastern Argentina, and southeastern Brazil.

HABITATInhabits dense tropical moist forests, secondary areas, orchards,and other agricultural and modified ecosystems. It has beenrecorded from sea level up to about 5,400 ft (1,650 m). It ismost abundant near streams, rivers, and other water bodies.

BEHAVIORWhen threatened, it hisses and gasps, snapping at the intruder.This is a mostly nocturnal species but sometimes may be activeby day. Although most of the time it stays on the ground, itmay also climb into trees. Like other didelphids, gray four-eyed opossums are solitary. When it is asleep, it rolls into aball and the eyes are not visible, but the bright spots above theeyes give the appearance of an awake and alert opossum.

FEEDING ECOLOGY AND DIETThe four-eyed opossum is omnivorous. It feeds on manyspecies of tropical and introduced fruits, corn, palm fruits,flower nectar, frogs, birds, rodents, and other small vertebrates,snails, insects, crustaceans, and carrion. Insects are most fre-quently eaten in the dry season. They tend to take fruits thatare larger than 2 in (5 cm) in diameter and that are fleshy,juicy, with high contents of sugars or lipids, and low levels ofnitrogen.

REPRODUCTIVE BIOLOGYPolygamous. Breeds throughout the year or seasonally, de-pending on the region. Females have seven mammae. Althoughthere may be more babies born than this number, a maximumof seven can be found in the pouch. Females may have morethan one birth per year. They construct a nest of litter andother vegetation in tree limbs, in hollows in standing or fallentrees, or in dens underground. The nest is spherical and about11.8 in (30 cm) in diameter. Litters of one to seven with an av-erage of about five are reported. Females are sexually receptivewhen they are seven months old. Maximum longevity is about2.5 years in the wild and 3.5 years in captivity.

CONSERVATION STATUSThis is generally an abundant species that can live in both pris-tine and disturbed conditions. It can also live in houses in ruralareas. The IUCN has not listed it, and it does not seem to bethreatened.

SIGNIFICANCE TO HUMANSSometimes considered a nuisance because it may raid hen-houses. This species and other didelphids are reservoirs of Try-panosoma cruzi, the protozoan that causes Chagas’ disease.








behavior Distribution DietConservation

status

Black-shouldered opossumCaluromysiops irruptaFrench: Opossum àépaules noires; German: Bindenwollbeutelratten; Spanish: Cuica de hombros negros

Pearl gray dorsal fur with black patches extending from the shoulders down to each forefoot. From the shoulder patches, two parallel black lines run down the back to the rump. Tail is sparsely covered with hair and grayish black except for the final few inches (centimeters) which are white.

Nocturnal and solitary. Primarily arboreal species. Lives in undisturbed tropical moist forests.

Southeastern Peru and extreme western Brazil in the upper Amazon River basin.

Fruit, insects, eggs, and small vertebrates.

Vulnerable

Brown four-eyed opossumMetachirus nudicaudatusFrench: Brun opossum àyeux; German: Nacktschwanzbeutelratte; Spanish: Tlacuache cuatro ojos café, zorricí, cuica; Portuguese: Jupati

Uniform brown dorsum. Pale spots just above the eyes that give the appearance of a second set of eyes. Long, thin, tapered tail, which is naked and virtually unicolored. Length 8.3–11.8 in (21–30 cm).

Solitary and nocturnal. Mostlyfound in tropical moist forests.Rarely goes into trees, generally running along the forest floor. Sea level to bout 3,900 ft (1,200 m).

Extreme southern Mexicothrough Central America south to southern Brazil, Paraguay, and northern Argentina.

Arthropods, bird eggs, nestlings and other small vertebrates, fruit.

Not listed by IUCN

Southern opossumDidelphis marsupialisEnglish: Common opossum; German: Nordopossum; Spanish: Tlacuache común, cuica, zorro; Portuguese: Gambá, saruê

Dark gray or blackish to pale gray with long, dense fur. The tail is long and naked, bicolor with the basal half black and the rest whitish. Length 12.6–19.7 in (32–50 cm).

Solitary and nocturnal. Terrestrial and arboreal. Movement in trees is aided by a prehensile tail. Females carry young in their pouch. Found in moist and dry tropical forests, cloud forests, semidesertic habitats, secondary vegetation, agricultural lands, and edges of towns and cities. Important as a reservoir of Trypanosoma cruzi whichcauses Chagas disease.

Central and eastern Mexico south to eastern Peru, northern Bolivia, and Brazil.

Omnivorous; feeds on fruit, insects and other invertebrates, small vertebrates, and carrion.

Not threatened

Northern gracile mouse opossumGracilinanus maricaSpanish: Chuchita costeña

Uniform reddish brown pelage on the back. Underparts paler. One large black patch over each eye. There is no pouch.

Solitary and nocturnal. Primarily arboreal. Lives in tropical and subtropical moistand dry forests and even in savannas, at an altitude of 4,920–8,530 ft (1,500–2,600 m).

Northern Colombia and western Venezuela.

Insects and other arthropods, eggs, andfruit.


Grayish mouse opossumMarmosa canescensFrench: Souris-opossum grisâtre; Spanish: Tlacuatzin; ratón tlacuache

Small opossum with grayish brown dorsal hair and a long, slender, tapered, prehensile, and naked tail. Two large black patches surround the eyes.Length 2.4–4.3 in (6–11 cm).

Solitary and nocturnal, mainlyarboreal species. Makes spherical nests with vegetationamong tree branches or in hollow trees, but has been found roosting inside hummingbird nests. Feeds primarily on insects but also on fruit, eggs, and small vertebrates. Found in tropical dry forest from sea level up to about 5,250 ft (1,600 m).

Endemic to western Mexico.

Fruit, arthropods, bird eggs and nestlings; also small animals such as snakes, bats, and lizards.

Data Deficient

Elegant fat-tailed opossumThylamys elegansEnglish: Chilean mouse opossum; French: Opossum àqueue adipeuse elegant; German: Elegantes Fettschwanzopossum; Spanish: Yaca, llaca

The hair is thick and dense, pale brown on the sides with a wide dark stripe along the back and paler underparts. The rostrum is short and conical and the ears medium sized and naked. The tail is almost completely naked and seasonally it is used to store fat reserves. Dark and rust-brown with white-tipped tail. Length 4.7–5.5 in (12–14 cm).

Solitary, semiarboreal, and nocturnal. This species lives in cloud forest, temperate southern rainforest, and scrub associated with forest edges. They build nests with plant matter and hairs among tree or shrub branches, or underground.

Southwestern coastal Peru and western Chile.

90% of their diet is composed of insects but they also eat fruit, eggs, and small vertebrates.

Not listed by IUCN

[continued]


Monotypic order: DidelphimorphiaVol. 7: Reptiles





status

Small fat-tailed opossumThylamys pusillaEnglish: White-bellied fat-tailedmouse opossum; French: Petit opossum à queue adipeuse; German: Kleines Fettschwanzopossum; Spanish: Comadrejita,marmosa común

Gray to brown on the back and white underparts. Short and conical rostrum. Tail relatively long, almost naked. It can store reserves and appear fatter seasonally. Length 4–5.5 in (10–14 cm).

Solitary, semiarboreal, andnocturnal. Found in the Andean piedmont and furtherabove, from desert areas to submontane habitats.

Southern Brazil and Bolivia, Paraguay, and northern and central Argentina.

Mostly insects and otherarthropods, but also fruit, eggs, and small vertebrates.

Not listed by IUCN

Slaty slender mouse opossumMarmosops invictusEnglish: Slaty mouse opossum; French: Opossum schisteux de souris; Spanish: Marmosa de montaña

Dorsal hairs reddish brown to dark brownand paler underparts. Tail uniformly dark brown. Black patches on eyes. Length4.7–5.9 in (12–15 cm).

Solitary, semiarboreal, nocturnal species. Found in rainforest at intermediate altitudes.

Eastern Panama, Colombia, and Venezuela.

Mostly insectivorous but also eats fruit, eggs, and small vertebrates.


Southern short-tailed opossumMonodelphis dimidiataEnglish: Yellow-sided opossum, eastern short-tailed opossum; Spanish: Colicorto pampeano

Unicolored gray-brown on the back, with a short tail that is nearly naked. The snout is elongated and conical, and the ears are relatively short. Length 4.3–7.9 in (11–20 cm).

Solitary, terrestrial, diurnal. Found in pampas grasslands, induced grasslands, and wetlands. Males and females reproduce only once in their lifetime.

Southern Brazil, Uruguay, and Argentina.

Mostly insectivorous and not too carnivorous. Probably feeds also on fruit and eggs.

Lower Risk/NearThreatened

Black four-eyed opossumPhilander andersoniSpanish: Comadreja cuatro ojos negra

Grayish black sides and a black stripe down the center of the dorsum. Two bright pale spots above the eyes that resemble a second pair of eyes. Tail as long as the head and body, naked, and bicolor: basal half dark, the rest white. Length 9–11 in (23–28 cm).

Solitary and nocturnal. Primarily terrestrial but also climbs trees. Lives in lowland tropical moist forest. Females have a pouch to protect young.

Northern and western Amazon basin, from Venezuela and eastern Colombia south through western Brazil, Ecuador, and Peru.

Omnivorous; feeds on insects, small vertebrates, eggs, and fruit.

Not listed by IUCN

Orange mouse opossumMarmosa xerophilaEnglish: Dryland mouse opossum; French: Souris-opossum orange; Spanish: Marmosa del desierto, comadrejita de los desiertos

The dorsum and flanks are orange-yellow and underparts white. Large, naked ears. Black patches on the eyes. Long, naked, semiprehensile tail. 3.5–5.5 in (9–14 cm).

Solitary and nocturnal. Mostly arboreal but readily takes to the ground. Inhabits desert and semidesert areas.

Northeastern Colombia and northwestern Venezuela.

Primarily insectivorous. Also feeds on birds' eggs and fruit.

Endangered

ResourcesBooksBenton, M. J. The Rise of the Mammals. New York: Crescent

Books, 1991.Collins, L. Monotremes and Marsupials. Washington, DC:

Smithsonian Institution Press, 1973.Eisenberg, J. F. Mammals of the Neotropics. Vol.1, The Northern

Neotropics. Chicago: University of Chicago Press, 1990.Eisenberg, J. F., and K. H. Redford. Mammals of the Neotropics.

Vol. 3, The Central Neotropics. Chicago: University ofChicago Press, 1999.

Hunsaker II, D. The Biology of Marsupials. New York: AcademicPress, 1977.

Nowak, R. M. Walker’s Mammals of the World. 6th ed., Vol. 1,Baltimore: John Hopkins University Press, 1999.

Redford, K. H., and J. F. Eisenberg. Mammals of the Neotropics.Vol. 2, The Southern Cone. Chicago: University of ChicagoPress, 1992.

Wilson, D. E., and D. M. Reeder. Mammal Species of the World.Washington: Smithsonian Institution Press, 1993.

PeriodicalsAlonso-Mejía, A., and R. A. Medellín. “Marmosa mexicana.”

Mammalian Species 421 (1992): 1–4.

Caceres, N. C. “Food Habits and Seed Dispersal by theWhite-eared Opossum, Didelphis albiventris, in SouthernBrazil.” Studies on Neotropical Fauna and Environment 37(2002): 97–104.

Castro, I., H. Zarza, and R. A. Medellín. “Philander opossum.”Mammalian Species 638 (2000): 1–8.

Lemos, B., G. Marroig, and R. Cerqueira. “Evolutionary Ratesand Stabilizing Selection in Large-bodied Opossum Skulls(Didelphimorphia: Didelphidae).” Journal of Zoology 255(2001): 181–189.

Marshall, L. G. “Chironectes minimus.” Mammalian Species 109(1978): 1–6.

———. “Glironia venusta.” Mammalian Species 107 (1978): 1–3.

———. “Lestodelphys halli.” Mammalian Species 81 (1977): 1–3.

McManus, J. J. “Didelphis virginiana.” Mammalian Species 40(1974): 1–6.

Medellín, R. A. “Seed Dispersal of Cecropia obtusifolia by TwoSpecies of Opossums.” Biotropica 26 (1994): 400–407.

Rodrigo A. Medellín, PhD

Evolution and systematicsThe order Paucituberculata is represented by just a single

living family, the Caenolestidae, with just two genera. Thehandful of living species is all that remains of what appears tohave been a once-abundant marsupial dynasty during theOligocene epoch, approximately 25 million years ago. Thereare seven extinct families, some of which were described fromfossils before the living caenolestids were discovered, includ-ing the Groberiidae. Some of the earliest fossils, members ofthe family Polydolopidae, date back to the Palaeocene, morethan 60 million years ago.

The decline of the paucituberculates began in theOligocene, and it gathered pace in the Miocene, when the con-tinents of North and South America were briefly joined. Therewas an influx of placental mammals from the north into whathad been for many millions of years a bastion of marsupial di-versity. The newcomers included rodents and primates whosedescendants have since thrived at the expense of many oustedmarsupials.

A number of similarities with other American marsupialshas led some authorities to consider the shrew opossums tobe no more than a subgroup of the order Didelphimorphia.However, molecular evidence supports the classification usedhere—it may be that at one time the Paucituberculata wereas diverse as the extant Australian order Diprotodontia.

Until recently, there were thought to be three livingcaenolestid genera. The third, Lestoros, contained the species,L. inca, and is now considered part of the larger genus,Caenolestes.

Physical characteristicsShrew opossums are all rather similar looking. The largest

specimens (usually males) are no more than 10 in (25 cm)long, half of which is tail, except in the Chilean shrew opos-sum, whose tail is relatively short. The face is long and ta-pering, with a pointed snout, long whiskers, and very smalleyes. The ears are quite large and project well beyond the an-


●▲

PaucituberculataShrew opossums

(Caenolestidae)

Class Mammalia

Order Paucituberculata

Family Caenolestidae


Thumbnail descriptionSmall, shrewlike animals with small eyes,shaggy fur, and a long tail; females lack apouch

SizeHead-body 3.5–5 in (9–13 cm); tail 2.5–5 in(6.5–13 cm); weight 0.7–1.5 oz (20–40 g)


HabitatTemperate rainforest and alpine scrub borderinghigh altitude paramo meadow

Conservation statusVulnerable: 1 species

DistributionWestern South America, including parts of Ecuador, Colombia, Venezuela, Peru,Chile, and Argentina

imal’s fur. The overall appearance is comparable to a rat orovergrown shrew.

DistributionThe living shrew opossum species all derive from western

South America, from the coast to the high Andes.

HabitatThe preferred habit of most shrew opossums is densely

vegetated and humid–temperate rainforest, montane wood-land, or the lush high altitude meadows of the Andeanparamo. Such habitats offer cover and an abundance of suit-able nest sites. They also support a rich invertebrate faunaand thus present good feeding opportunities.

BehaviorThe shrew opossums’ small size and the remote nature of

their habitats mean they have little contact with humans; con-sequently, details of their ecology and behavior are not wellknown. They are all largely nocturnal or crepuscular, andspend the day resting in hollow logs or holes around the rootsof trees. They appear to live alone, and travel around the homerange on regular runways. They are not territorial, and morethan one individual use the paths. They are proficientclimbers, and will scramble into the branches of shrubs, us-ing the tail as a prop and a counterbalance, but not for grasp-ing.

Feeding ecology and dietThe diet is predominantly insects and other invertebrates

such as earthworms, which the shrew opossums find by rum-maging in the surface litter and investigating likely nooks andcrannies along their regular runways. Like placental shrews,they hunt mainly by smell; they also have sharp hearing, buttheir eyesight is relatively poor. Various species have also been

reported feeding opportunistically on fruit, scavenging theflesh of dead animals, and killing and eating the young ofother mammals such as rats found in nests.

No torpid or hibernating specimens have been recorded,but there is good evidence that shrew opossums can becometorpid in times of food shortage. The Chilean shrew opos-sum builds up reserves of fat in its tail in late summer, whichhelp it survive the cold Andean winter.

Reproductive biologyVery little is known about caenolestid reproduction, in-

cluding mating system. Normal litter sizes can be guessed atfrom the number of teats—four in members of the genus,Caenolestes, five or seven in the Rhyncholestes species. Femalesdo not have a pouch, so nursing young must latch on firmlyto the mother’s teat in order to survive. Once milk is flow-ing, the teat swells in the infant’s mouth so that it cannot eas-ily become detached. When the young become too big to becarried beneath the mother’s body, she presumably leavesthem in a nest while she goes out to feed, returning period-ically to suckle them.

Conservation statusThe Chilean shrew opossum (Rhyncholestes raphanurus) is

listed as Vulnerable by the IUCN. Information regardingshrew opossum population density is very limited, since fewspecimens have ever been collected and field sightings are notwell known. However, the temperate rainforest in which theChilean shrew opossum lives is shrinking quickly, and otherspecies in the same habitat have undergone a significant de-cline. Caenolestes shrew opossums are probably more secure.

Significance to humansNone known.


Vol. 12: Mammals IMonotypic order: Paucituberculata


1

2

1. Silky shrew opossum (Caenolestes fuliginosus); 2. Chilean shrew opossum (Rhyncholestes raphanurus). (Illustration by Brian Cressman)


Silky shrew opossumCaenolestes fuliginosus

TAXONOMYHyracodon fuliginosus (Tomes, 1863), Ecuador.

OTHER COMMON NAMESEnglish: Ecuador shrew opossum; French: Caenolestidé d’E-cuador; German: Ekuador-Opossumaus; Spanish: Ratónmusarana de los Andes.

PHYSICAL CHARACTERISTICSHead and body 3.5–5.5 in (9–13 cm) long; tail 3.5–5.5 in (9–13cm) long; fur brown, soft, and shaggy, toes bear small sharpclaws.

DISTRIBUTIONAlpine regions of northern Colombia, Ecuador, and westernVenezuela.

HABITATCool, humid thickets in alpine forests and meadows.

BEHAVIORNocturnal, terrestrial, fast-moving; an excellent climber.

FEEDING ECOLOGY AND DIETMostly insect larvae, will also take young vertebrate prey andcarrion.

REPRODUCTIVE BIOLOGYNot well known, but young are probably born between Juneand September in litters of two to four.

CONSERVATION STATUSNot listed by the IUCN.


Chilean shrew opossumRhyncholestes raphanurus

TAXONOMYRhyncholestes raphanurus Osgood, 1924, Chiloe Island, Biobio,Chile.

OTHER COMMON NAMESFrench: Caenolestidé du Chili; German: Chile-Opossumaus;Spanish: Comadrejita trompuda.

PHYSICAL CHARACTERISTICSHead and body 4–5 in (10–13 cm) long; tail 2.5–3.5 in (6–9cm); may fatten prior to onset of winter. Female has five orseven teats.

DISTRIBUTIONSouth central Chile and Chiloe Island.

HABITATTemperate rainforest.

BEHAVIORNocturnal, terrestrial, burrows through surface litter; may en-ter torpor in winter.

FEEDING ECOLOGY AND DIETInsects, worms, and other invertebrates caught by rummagingin topsoil and leaf litter.

REPRODUCTIVE BIOLOGYNot well understood, but females are apparently capable ofbreeding at any time of year.

CONSERVATION STATUSListed as Vulnerable by IUCN.

SIGNIFICANCE TO HUMANSNone known.

Species accounts

Vol. 12: Mammals IMonotypic order: Paucituberculata

Caenolestes fuliginosus

Rhyncholestes raphanurus


Monotypic order: PaucituberculataVol. 12: Mammals I

ResourcesBooksAplin, K. P., and M. Archer. “Recent Advances in Marsupial

Systematics with a New Syncretic Classification.” In Possumsand Opossums: Studies in Evolution. Sydney, Australia: SurreyBeatty and Sons & Royal Zoological Society of New SouthWales, 1987.

Feldhamer, G. A., L. C. Drickamer, S. H. Vessey, and J. F.Merritt. Mammalogy: Adaptation, Diversity, and Ecology.Boston: WCB McGraw-Hill, 1999.

Macdonald, D. The New Encyclopedia of Mammals. OxfordUniversity Press, 2001.

Nowak, R. “Order Paucituberculata.” In Walker’s Mammals ofthe World. Vol. I, 6th ed. Baltimore and London: JohnsHopkins University Press, 1999.

Amy-Jane Beer, PhD

Evolution and systematicsThe mouse-like monito del monte is a small, inconspicu-

ous species of marsupial from South America. Its unprepos-sessing appearance belies its huge zoological importance. Thisdrab little mammal is a relic of a bygone era—all that remainsof a once-prominent group that may have given rise to theentire diverse marsupial fauna that now lives on the other sideof the world in Australia. The Microbiotheridae are thereforeconsidered part of the otherwise exclusively Australian groupknown as the cohort Australidelphia.

Of the seven species of microbiothere that have been de-scribed, six members of the genus Microbiotherium are longextinct and are known only from fossil remains. This orderof marsupials has only one living family, the Microbiotheri-idae, with a single representative, Dromiciops gliroides, thediminutive monito del monte, also known in its native Chileas the colocolo. Dromiciops has several very primitive traits andis only distantly related to other South American marsupials(opossums). In fact, it has more in common with some Aus-tralian marsupials, in particular the carnivorous dasyurids,

from which it must have been separated for at least 40 mil-lion years. The monito del monte is thus thought to be theonly surviving member of an early offshoot of the marsupiallineage that lived on the ancient supercontinent of Gond-wana, to which Australia, Antarctica, and South America wereonce joined. A microbiotherian marsupial could have beenthe ancestor of the diverse marsupial fauna seen in Australiatoday. While the descendants of ancient micorbiotheres weredoing well in Australia, the initially successful marsupial ra-diation in South America came to an end when placentalmammals arrived from the north. Like most other SouthAmerican marsupial orders, the little microbiotheres weremostly edged out—all but Dromiciops, which alone survivesto this day.

The taxonomy of this species is Dromiciops gliroides(Thomas, 1894), Biobio, Chile, “Huite, NE Chiloe Island.”

Physical characteristicsThe monito del monte is small (head and body less than

5 in [13 cm] long) and superficially mouse-like, with a pointed


●▲

MicrobiotheriaMonitos del monte

(Microbiotheriidae)Class Mammalia

Order Microbiotheria

Family Microbiotheriidae


Thumbnail descriptionSmall, mouse-like, South American nocturnalmarsupials

SizeHead and body length 3–5 in (8–13 cm); taillength 3.5–5.2 in (9–13 cm); weight 16–42g(0.5–1.4 oz)


HabitatOccupies dense, humid forest

Conservation statusVulnerable

DistributionChile and Argentina

face, small rounded ears, and large eyes. Its furry tail is prehensile, up to 5 in (16 cm) long and sometimes very thick, especially around the base where fat accumulates prior to hi-bernation. There is a patch of naked skin on the undersideof the tail tip, which helps improves traction when the tail isused to grasp branches. The paws are similar to those of opos-sums, each having opposable toes adapted for gripping. Theface is short and pointed, with very large eyes ringed withdark fur. The ears are oval and erect. The body is coveredin soft brownish gray fur, which fades to buff-white on thebelly and sometimes shows a pattern of swirls on the shoul-ders and back.

DistributionThe monito del monte is found only in the southern An-

des mountains between the latitudes of 36° and 43°S in Chile,and just over the border into southwestern Argentina. Thisvery limited distribution makes the Microbiotheria the leastwidespread of all living mammalian orders.

HabitatThis small, nimble marsupial lives for the most part off the

ground, in trees and shrubs and especially in thickets ofChilean Chusquea bamboo. These grow best in the cool, hu-mid forests of the Andes foothills. The species’ common namemeans “mouse of the mountain.”

BehaviorMonitos del monte are nocturnal and active most of the

year in milder parts of their range. However, prolonged peri-ods of cold winter weather or food shortage induce hiberna-tion during which the animals survive on reserves of fat storedin the base of the tail. They spend most of their life above-ground, climbing with great skill using hands, feet, and tail tograsp branches and stems. They build intricate but sturdy nestsof twigs and bamboo leaves woven into a ball. Preferred nestsites are tree holes or dense thickets, but rocky crevices andhollow fallen logs are also used, and nests are sometimes builtsuspended aboveground in trailing liana vines. The bambooleaves with which the nests are made are waterproof, so thelining material of soft moss and grass remains dry and snug.Mosses are also sometime used to adorn the outside of the nestas well, helping to make it less conspicuous.

Individuals typically live in pairs or in small groups thatusually comprise a mother and up to four young of the cur-rent year. Neighbors and family members communicate bysound; the most distinctive call is a long, trilling sound end-ing in a soft, hoarse cough.

Feeding ecology and dietMonitos mainly eat insect grubs and pupae, also flies and

small lizards that they collect from leaves and from cracks andcrevices in tree bark. They grab prey with their nimble hands.They will also eat fruits, especially when preparing to hiber-nate in the fall.

Reproductive biologyThe breeding season is in spring, and males and females

mate in October soon after emerging from hibernation. Thefirst litters appear in November, but continue to be born un-til January. Litters of between one and four young are nor-mal; there are some records of five but, since the female onlyhas four teats, the chances are the fifth will not survive. Theyoung spend the first few weeks of life in their mother’s pouch,attached to a teat. As soon as they are old enough to main-tain their own body heat, the female leaves them in the nestwhile she goes out to feed. A little later, the young family ac-companies the mother, at first riding on her back, and thenlearning to climb and feed themselves. Once independent,they often remain close to their mother for the rest of theyear. They are sexually mature at one year old.

Conservation statusThe monito del monte was once considered a common an-

imal in parts of its range, but it is increasingly under pressurefrom habitat loss due to deforestation and development. Thespecies’ very restricted range means that even small losses canbe significant. Having survived apparently little change for atleast 20 million years, it would be a tragedy if the monito delmonte was to become extinct as a result of human negli-gence—its loss would represent the demise of an entire orderof animals. The species is listed as Vulnerable by the IUCN.


Vol. 12: Mammals IMonotypic order: Microbiotheria

Monito del monte (Dromiciops gliroides). (Illustration by MichelleMeneghini)

Significance to humansThe monito del monte is the subject of some extreme su-

perstitions. Some Andean people regard it as a bearer of illfortune. Being nimble and inquisitive, and interested in storedfood such as fruit, monitos inevitably enter houses from time

to time. They do little real harm, but in some places a “colo-colo” indoors is believed to be such bad luck that the onlyway to avert disaster is to move out and destroy the housecompletely. In actual fact, these animals probably do moregood than harm by feeding on a variety of insect pests.


Monotypic order: MicrobiotheriaVol. 12: Mammals I

ResourcesBooks

Aplin, K. P., and M. Archer. “Recent Advances in MarsupialSystematics with a New Syncretic Classification.” In Possumsand Opossums: Studies in Evolution. Sydney: Surrey Beattyand Sons & Royal Zoological Society of New South Wales,1987.

Feldhamer, G. A., L. C. Drickamer, S. H. Vessey, and J. F.Merritt. Mammalogy: Adaptation, Diversity, and Ecology.Boston: WCB McGraw-Hill, 1999.

Nowak, R. “Order Microbiotheria.” In Walker’s Mammals ofthe World. Vol. I, 6th ed. Baltimore and London: JohnsHopkins University Press, 1999.

Amy-Jane Beer, PhD

Evolution and systematicsThe order Dasyuromorphia includes three families of car-

nivorous marsupials in the superfamily Dasyuroidea: theDasyuridae (dasyures), the Myrmecobiidae (numbat), and theThylacinidae (thylacines). The dasyurids and thylacinids aremore closely related to each other than they are to the num-bat. The Australian marsupial radiation produced a numberof other species of carnivorous marsupials in the otherwiseherbivorous order Diprotodontia. These include two genera(Thylacoleo and Wakaleo) and seven species of large, up to 220lb (100 kg), predatory marsupial lions of the family Thyla-coleonidae, which are most closely related to koalas and wombats (superfamily Vombatoidea), and an omnivorous(partly flesh-eating) giant rat-kangaroo, in the subfamily Pro-pleopinae, family Hypsiprymnodontidae, superfamily Macrop-odoidea.

The earliest known carnivorous marsupial in Australia,Djarthia murgonensis, comes from the early Eocene (55 mil-lion years ago [mya]). The taxonomic affiliation of this andtwo other early carnivorous marsupials is not certain, as keyanatomical features used to clearly identify them to familylevel or even to separate them from the South American mar-supial fauna are lacking in the fossils found to date. The Aus-tralian dasyuromorphian and American marsupial taxa arequite distinct but are allied in the possession of many incisors

(polyprotodonty) which distinguish them from the herbivo-rous Diprotodontia. Dasyuromorphians originated in the lateOligocene. The early radiation comprised the very conserv-ative or “primitive” thylacinids. Ranging in size from smalldog-sized, 70.5–176.4 oz (2–5 kg) to slightly larger than 65lb (30 kg), thylacines dominated the Australian carnivorousmarsupial fauna until the late Miocene, after which theysteadily declined to two species present in the Pleistocene andonly one persisting until historic times. Dasyurids first ap-peared in the fossil record in the early to middle Miocene butwere rare until the late Miocene when they diversified andreplaced the thylacine as the dominant marsupial carnivorefauna. Most of the Pleistocene fossil dasyurids are from still-living taxa, although none of the living groups occur earlierthan the Pliocene. Dasyurids are considered to be highly spe-cialized or “derived” dasyuromorphians in terms of their mor-phology. The numbats are represented by only one livingspecies which appeared in the fossil record as recently as thePleistocene. The numbat is a highly specialised dasyuromor-phian, with features of the skull, teeth, and tongue adaptedfor termite feeding.

Physical characteristicsDasyuromorphians are quadrupedal (move on four legs),

with four toes on the front feet, four or five toes (including


●

Dasyuromorphia(Australasian carnivorous marsupials)

Class Mammalia

Order Dasyuromorphia


Number of genera, species 23 genera; 71species

Photo: The yellow-footed antechinus (Antechinusflavipes) forages in a rockpile in Warwick, Queens-land, Australia. (Photo by B. G. Thomson/PhotoResearchers, Inc. Reproduced by permission.)

a clawless toe called a hallux) on the hind feet, long tails andlong, pointed snouts, and are considerably uniform in bodyshape despite the large size variation, from 0.14 oz (4 g) tomore than 65 lb (30 kg). Extreme exceptions in body forminclude the kultarr, which has elongated hind legs and boundsrather than runs, and the robust form and massive skull, teethand jaw musculature of the specialist scavenger, the Tasman-ian devil. Unlike placental carnivores, the fleshy foot pad ofthylacines and dasyures extends to the heel and wrist joint,which may contact the ground when stationary or movingslowly, although most species are digitigrade (run on the toes)when moving fast. Arboreal (tree-dwelling) species tend tohave broader feet and a better-developed, more dexterous hal-lux. Some dasyurid species store fat in the tail. None are pre-hensile and in some such as the thylacine, the tail is semi-rigid.Tail length is generally shorter than body length, except inthe numbat and in the long-tailed dunnart.

The dentition is polyprotodont, meaning many incisors(four upper, three lower), which distinguishes this group ofmarsupials from the Diprotodontia or herbivorous marsupi-als. Premolars number three in thylacines and numbats, two

in dasyures. All molar teeth (four in thylacines and dasyures;five in numbats) are similar in form, in contrast with the dif-ferentiation of slicing and grinding functions into separateteeth in the placental carnivores. Thylacine and dasyure mo-lars each retain meat-slicing (carnassial) cusps and function,and grinding surfaces. This marsupial feature may be a con-sequence of reproductive mode. Permanent teat-attachmentduring tooth development appears to suppress the eruptionof the deciduous teeth, which remain vestigial, leading toearly eruption of the permanent dentition. Each of thesepermanent molars must, in turn, function as slicing andgrinding/crushing teeth when they first erupt, and then ei-ther specialized slicing or crushing teeth when they achievetheir final position in the mature jaw. Tooth structure rangesfrom simple, cuspless molars in the termite-eating numbat,to the more complex slicing/crushing molars of the othertwo families. The degree of carnassiality (or meat-slicingfunction) grades with diet. Highly carnivorous taxa, such asthylacines and devils, have well-developed carnassial cusps,reduced crushing surfaces, and molar orientation is more antero-posterior. This is particularly the case in the two rearmolars, which are biomechanically positioned in adults formaximal slicing function, in a position halfway along the jawbone comparable to the carnassial tooth in placental carni-vores. As the diet becomes more insectivorous, the crushingsurfaces (the rear part of each molar tooth) become larger


Vol. 12: Mammals IOrder: Dasyuromorphi

A mulgara (Dasycercus cristicauda) searches grass tops for food nearAlice Springs, Northern Territory, Australia. (Photo by Photo Re-searchers, Inc. Reproduced by permission.)

The Tasmanian devil (Sarcophilus laniarius) has teeth capable of crush-ing bone. (Photo by © Erwin & Peggy Bauer. Bruce Coleman, Inc. Re-produced by permission.)

at the expense of the carnassial cusps (sharp, pointy bits) andthe molar teeth become wider and more triangular in shape.A feature at least of the larger dasyuromorphians is contin-ual or over-eruption of the canine teeth throughout life.This may be a consequence, again, of early eruption of thepermanent teeth at an age when the juvenile animal is lessthan half of its adult size. Over-eruption, while probably aresponse to tooth wear and occlusal patterns, has the effectthat the canine teeth continue to get bigger as the individ-ual grows.

Coat color in most species ranges from sandy to reddishto grayish brown, sometimes with a lighter colored under-belly. Black is rare (only devils and one of the two color phasesof the eastern quoll) and only eight taxa have distinct mark-ings: stripes on the back in the thylacine, numbat and threegroups of New Guinean dasyurids, a facial stripe in the num-bat, spots in the quolls and white chest, shoulder and rumpmarkings in the devil. Fur length is mostly short to slightlywispy, although tail fur can vary from short, to a bushy tip,to completely fluffy or bushy.

DistributionThe order Dasyuromorphia comprises the Australian ra-

diation of the polyprotodont marsupials and is restricted toAustralia, New Guinea, Tasmania, and some smaller close-byislands. At times during evolutionary history, including mostrecently the Pleistocene (2 million to 10,000 years ago), landbridges connected Australia and New Guinea, and Australiaand Tasmania, and there was opportunity for interchange be-tween the faunas of these major land masses. This historicalpattern of connectivity between land masses is reflected in thedistributions and genetic relationships of species. Two speciesof dasyurids in the genus Sminthopsis—S. archeri and S. vir-giniae—have ranges that cross Torres Strait from northernAustralia to New Guinea, and one of the New Guinean quolls,the bronze quoll (Dasyurus spartacus), is very closely related tothe chuditch (D. geoffroii) from the Australian mainland. Allof the Tasmanian dasyurid species are currently, historically,or prehistorically (depending on the timing of mainland ex-tinctions) represented in mainland populations (sevenspecies). Where genetic studies have been carried out, main-land and Tasmanian populations represent different evolu-tionary significant units, a consequence of over 10,000 yearsof evolutionary separation. It is notable, however, that thesefaunal interchanges were restricted largely to savanna andwoodland species. The cold, dry conditions that prevailedduring the Pleistocene precluded the development of signif-icant rainforest corridors. Rainforest Antechinus of Cape Yorkand the sister clade Murexia from New Guinea did not makeit across the land bridge, although some small dasyurids ofwet habitats (Antechinus minimus—closed, wet heath, grass orsedgelands; A. swainsonii—wet forest and heath) do occur oneither side of Bass Strait.

HabitatCarnivorous marsupials occupy habitats from deserts to

mountain tops to rainforests and show an accordingly widerange of behavioral, morphological, and physiological adap-


Order: DasyuromorphiVol. 12: Mammals I

A spotted-tailed quoll (Dasyurus maculatus) gets a drink in easternAustralia. (Photo by E. & P. Bauer. Bruce Coleman, Inc. Reproducedby permission.)

An eastern quoll (Dasyurus viverrinus) nest in Australia. (Photo by An-imals Animals ©J. & C. Sohns. Reproduced by permission.)

tations. Australia’s small desert dasyurids are remarkable intheir ability to move very long distances in response to localrainfall and fire events, thereby utilizing different vegetativegrowth stages and short-term flushes in food availability.Planigales live in deep soil cracks and have a suitably flattenedbody shape. Arboreal and scansorial (above-ground) species,including the antechinuses, are more likely to have a well-developed and dexterous clawless hallux on the inside of thehind foot, which assists with grasping branches or rocks. Verycapable climbers such as spotted-tailed quolls (Dasyurus mac-ulatus), also possess fleshy ridges on their foot pads and sharpclaws. Spotted-tailed quolls can climb large, straight trees tokill possum prey in their daytime tree-hollow refuges, movefrom tree to tree through the canopy, and climb head-firstdown trees.

Dasyurids live at extremes of temperature, have a low basalmetabolic rate like other marsupials, experience a fluctuatingfood supply, and most species are small and so lose and gainheat easily. Carnivorous marsupials cannot sweat but resort tolicking, panting, and lying flat out on the substrate to keepcool. Strategies to conserve body heat and reduce energy ex-penditure are diverse. Surface-dwelling desert species such asningaui have a spherical body shape, which maximises heat

conservation. Antechinuses and Tasmanian devils increase furthickness in winter and the fur color of some species (fat-taileddunnart, Sminthopsis crassicaudata) becomes darker towardstemperate regions. Most dasyurids use protected locations inhollow logs and trees, underground burrows, soil crevices,caves, and tussock grasses to rest during the day or betweenforaging bouts. Many species line their nest with insulativedead vegetation which they harvest and carry in their mouth,and some huddle in groups comprising adults, or mother andoffspring. Huddling in communal nests reduces energy ex-penditure in dunnarts by 20%. Torpor, in which the body tem-perature is voluntarily reduced to between 52–82oF (11–28oC)for periods of several hours, is used by half of dasyurids andthe numbat, species ranging from 0.17 oz (5 g) to 35 oz (1,000g) in body size. Torpor is employed as a daily or occasionalstrategy to conserve energy while resting, under the stressesof cold or food restriction. The females of some species evengo into torpor when with young. The slow marsupial devel-opment rate may allow this without adverse effects on the ba-bies. Perhaps as a consequence of their relatively low basalmetabolic rate, common to all marsupials, carnivorous marsu-pials have a pronounced ability to increase metabolic rate whencold that exceeds that of some placental mammals.

Another interesting question to ask is what determines howspecies live together. As most carnivorous marsupials are gen-eralised predators that can take a wide size range of inverte-brate and vertebrate prey, structurally complex habitats thatoffer a variety of different places to forage are an importantcontributor to local species diversity.

Rather counter-intuitively, it is the arid zone habitats, as wellas forest and heath, that are more structurally complex and of-fer the most opportunities for multiple species to partition re-sources. This may explain why there are so many species ofdesert dasyurids. Although the scansorial or above-ground for-aging niche, that is important in forest, is lacking in deserts, awealth of opportunities to segregate are provided by cracks inclay soils, sandy, sand dune and rocky substrates, and struc-turally complex vegetation such as hummock grasslands.

In forests, the arboreal or above-ground foraging nichecontributes to species coexistence. A number of antechinusesare scansorial, meaning that they scramble around both onthe ground and a number of metres up into shrubs and trees,even denning in tree hollows. Among the larger marsupialcarnivores of Tasmania, spotted-tailed quolls separate fromtheir close competitors, eastern quolls (Dasyurus viverrinus)and devils (Sarcophilus laniarus), on their greater arboreal useof habitat.

BehaviorAustralian mammals are almost all nocturnal or crepuscu-

lar and the carnivorous marsupials are no exception. Most arenocturnally active, although some diurnal foraging and bask-ing activity has been recorded in a number of species for whichdetailed field observations are available, including in antech-inuses and thylacines. In some populations, spotted-tailedquolls exploit opportunities to prey upon nocturnal possumprey asleep in tree hollows, and are almost arhythmic in their



The chuditch (Dasyurus geoffroii), also known as a western quoll, isnocturnal. (Photo by Michael Morcombe. Bruce Coleman, Inc. Repro-duced by permission.)

activity. Three species are substantially or completely diur-nal, the numbat, the speckled dasyure from New Guinea, andthe southern dibbler (Parantechinus apicalis) from WesternAustralia.

Well developed auditory and olfactory communicationcould be expected in these primarily nocturnal mammals, al-though carnivorous marsupials use a variety of visual displaysas well. Vocalizations range from hisses, growls, squeaks,barks to screeches in the low (0.1 kHz) to ultrasonic (mostless than 12 kHz) frequency range. Contact calls betweenmother and young start while young are still living in thepouch and consist of squeaks and wheezes which are returnedby the mother at a lower pitch. Aggressive calls range fromhisses, to growls and screeches. The screech of spotted-tailedquolls has been described as a blast from a circular saw andthat of the Tasmanian devil sufficient to “raise the devil,” atrait which may have contributed to its name. Female plani-gales and quolls in estrus emit male-attracting soft cluckingcalls when receptive to mating. Tasmanian devil females, andto a lesser extent males, crouch mouth to open mouth andgive continuous soft barks, each of which ends in a whine.Unwelcome suitors are repelled aggressively.

Scent is an important vehicle for the dissemination of so-cial and reproductive information between individuals, suchas male dominance status and the estrous state of females. Incarnivores, the information-laden metabolic breakdown prod-ucts of reproductive hormones are excreted mainly via the fe-ces, although urine of male antechinus also containssex-specific compounds. Dasyurids have well-developed par-acloacal glands from which a pungent, viscous, yellowish liq-uid is exuded during cloacal dragging form of scent marking.Male Tasmanian devils cloacal drag frequently in the pres-ence of oestrous females, and both sexes mark frequently dur-ing non-breeding social interactions. This behavior is wellestablished even in advanced pouch young before the glandshave begun to produce scent. Sternal skin glands and chestrubbing are widespread primarily among males of the smallerdasyurids (antechinuses, dunnarts, phascogales), an activitywhich increases during the breeding season under the controlof male reproductive hormones (testosterone). Female quollsand devils produce prodigious quantities of reddish oil in thepouch, the quality and quantity of which is an indicator of es-trous state, but which probably also serves to prepare thepouch for occupancy by the young. That this oil also has afunction in communicating reproductive state is suggested bythe intense interest that males show in sniffing the female’spouch compared with her cloaca.

Visual signals include extensive repertoires of postures,which the use of light-amplifying equipment enables humansto observe. Tasmanian devils use in excess of 20 different pos-tures in social interactions. Visual displays that accentuatebody size and weaponry (threat displays) or reproductivereadiness usually prelude potentially dangerous aggressive orreproductive interactions. Open mouthed threat displays thatshow the teeth are common.

Feeding ecology and dietCompetition for food contributes to differences in forag-

ing niche among all size ranges of carnivorous marsupials thatlive together, with the exception of the termite-eating num-bat but including, historically, the thylacine. Competition appears to be more prevalent in mesic forests and heathlandsthan in arid environments, where droughts, floods, and un-predictable food supplies may often reduce populations to lowlevels. Competition from larger antechinus species excludessmaller species from the highest quality habitat, with the re-sult that the smaller species eats smaller prey for which theyprobably have to work harder. In Tasmania, food competitionamong the larger carnivores has resulted in separation betweenspecies on prey size. If species consume different-sized prey,competition for the same prey items is reduced. Competitionhas been sufficiently intense over a long enough time scale todrive evolutionary changes in canine tooth size among thequolls. Canine tooth strength, which determines the size ofprey that can be killed, have become evenly spaced. Even spac-ing in prey size among species minimizes competition.

Reproductive biologyShort life spans, leading in their extreme form to single

breeding followed by death in the first year of life (semel-parity), are a defining feature of carnivorous marsupials.Among mammals, semelparity has arisen only in dasyuridsand didelphids, in which groups it has evolved at least sixtimes, including in medium-sized species over 2.2 lb (1 kg) inbody weight (northern quoll, Dasyurus hallucatus). All carniv-orous marsupials, including thylacines and possibly numbats,



The Tasmanian devil (Sarcophilus laniarius) has an open-mouthedthreat display. (Photo by E. & P. Bauer. Bruce Coleman, Inc. Repro-duced by permission.)

are short-lived, however, compared to similar-sized placentalmammals. This entire taxon seems to be evolutionarily dis-posed towards early senescence.

Semelparity among dasyurids is obligate in most antechi-nuses (Antechinus spp.), in both Phascogale species and in thelittle red kaluta (Dasykaluta rosamondae), but faculatative in thedibbler and the northern quoll. In the larger antechinuses,complete male die-off occurs immediately after mating butfemales may live to breed in a second year. The adaptive ex-planation developed on antechinus to explain die-off postu-lates that as a consequence of small body size, slow growthand the consequent long period of time required to raiseyoung to independence, and tightly seasonal environments inwhich food is limiting, males and females are unlikely to beable to gain sufficient energy to breed and then survive to asecond year. Their best option may be to put all their energyinto one big reproductive effort in the first year, even if it killsthem. In antechinuses, a consequence of the need to weanyoung in a tightly seasonal climate at the time of year whenfood supplies are maximal is that mating occurs in winterwhen food resources are scarce. Males are unable to store suf-ficient fat to see them through the intense mating rut andovercome this energy deficit by using elevated levels of stresshormones to promote the use of protein in muscle tissue asan energy resource. This only becomes possible through com-plete destruction of the ability to produce more sperm beforemating starts (sperm production would interfere with syn-thesis of stress hormones but also removes any possibility ofbreeding in a second year) and the shutdown of a negativefeedback system that prevents sustained levels of damaging

stress hormones in most mammals. Death results from a mul-titudinous cascade of events related to dramatic loss of bodycondition and immunosuppression from prolonged elevationof stress hormone levels. Males become anaemic and supporthuge numbers of ectoparasites, which exacerbates their prob-lems. The proximal cause of death is usually gastrointestinalulcers or an outbreak of a normally benign disease.

This model is supported by the geographic distribution ofsemelparous species, which are generally restricted to tightlyseasonal environments where reproductive opportunities arelimited to a narrow window each year. Iteroparous or multi-ple-breeding species, such as some dunnarts, include mostspecies from unpredictable arid environments where puttingall the eggs in one reproductive basket would be a risky strat-egy indeed. The lack of sustained elevated stress hormone lev-els, and opportunities, that come with larger body size andtail fat stores, for sufficient fat storage to tide over the mat-ing period in the northern quoll suggests that a universalmodel of male die-off remains obscure.

Very small quantities of some of the largest sperm pro-duced by any mammal are other unique features of repro-duction in carnivorous marsupials. Complete failure of spermproduction prior to the mating period in antechinuses andlimited sperm storage leave comparatively small amounts ofsperm available for a very intense, once in a lifetime rut; inthe brown antechinus (Antechinus stuartii ) as few as eight ejac-ulations. Dasyurid sperm have an unusual form of motilitywhich may compensate for this apparent disadvantage.

Copulation in semelparous species is an intense affair withintromission lasting as long as seven to 12 hours. Given thelimited sperm supplies, it must be assumed that sperm is usedcarefully and ejaculation is timed to maximise the chance offertilization. Most of the time and energy devoted to matingprobably serves the dual functions of stimulating the femaleand mate guarding, both of which increase the male’s chanceof siring the young. Physical stimulation provided by thethrusting male during copulation improves sperm transportup the female reproductive tract, and occupying the femalein copulo for a substantial proportion of the limited time inwhich she is in estrus physically prevents other males frommating with her. Antechinus, which mate in communal leks,are able to turn 180° while in copulo and fight off other males.Tasmanian devils indulge in ferocious mate guarding, keep-ing the female a prisoner in the den for days at a time with-out food or water, until her estrus is finished or the female’sdesire to escape reaches such an intensity that she succeedsin fighting off the male. Both male and female are likely tobe injured in this process.

The female is by no means a passive spectator in the mat-ing business. Female Tasmanian devils actively assess differ-ent males and solicit copulations from the male of their choice,avoiding or fighting off the others. Long periods of behav-ioral estrus allow time for females to mate with a number ofmales, resisting mate guarding attempts and fighting each oneoff in turn.

Multiple paternity has been found in all of the small num-ber of species in which mating systems have been investigated



A spotted-tailed quoll (Dasyurus maculatus) displays defensive be-havior. (Photo by © Erwin & Peggy Bauer. Bruce Coleman, Inc. Repro-duced by permission.)

using genetic paternity markers, and suggest high levels ofpromiscuity among females. Four fathers per litter is not un-common in devils (four teats) and up to seven fathers havebeen recorded in the agile antechinus (six to 10 teats), with50% of litters having three or more. Prolonged copulation,larger than average testes size (correlated with greater spermproduction), strong male-biased sexual size dimorphism (maleslarger than females), intense mate guarding, long periods ofbehavioral estrus, prolonged periods of sperm storage withinthe female reproductive tract prior to ovulation, and higherpopulation densities are associated with the likelihood of spermcompetition (between the sperm of different males within thefemale reproductive tract) and possibly the intensity of femalechoice. Semelparous species such as antechinueses exhibit allof the above traits. Iteroparous species from less predictable,arid environments, such as some dunnarts, do not.

Carnivorous marsupials, at least the dasyurids, have onemore trick up their metaphorical sleeves. Together with bats,dasyurids are unique among mammals in having sperm stor-age facilities in the female reproductive tract. (Sperm storageis common in birds and insects.) Ovulation occurs up to 12days after behavioral estrus and the sperm of several males arestored, possibly right next to each other, in tiny crypts in theoviducts. The sperm is reactivated and released at ovulation.This puts quite a different spin on how sperm competitionmight operate.

Parental care in all carnivorous marsupials for which it isknown is restricted to maternal care of the young during per-manent attachment to the teat and lactation. Once young havepermanently vacated the pouch, they are deposited in a veg-etation-lined nest in a den (underground burrow, cave, or hol-low log). Apart from records of chuditch (western quolls)moving young to new dens on their back, there are no otherrecords of females escorting young outside the den. Juvenilechuditch gradually explore further and further from themother’s den as they grow and teach themselves to forage andhunt. As weaning from lactation approaches, both mother andyoung start to spend nights apart in different dens. The fre-quency of these separations increases until the male youngdisperse. Once the males move away from the mother’s homerange they move rapidly over long distances.

Among many mammals, and it appears most carnivorousmarsupials, it is usually the male offspring that disperse fromtheir mother’s home range, females staying close to home forlife. Females thus exact a longer term cost to the mother, al-though the difference in the number of young produced byboth good and poor quality females will not be great. If, how-ever, there are major differences among individual males inreproductive success, it may be advantageous for females toinvest more heavily in male offspring. Strongly male-biasedsex ratios occur in some species of dasyurids, including in ag-ile antechinuses. The mechanism of sperm storage offers pos-sibilities for sex-based sperm selection.

ConservationThe pattern of endangerment among the carnivorous mar-

supials is consistent with that for Australian mammals in gen-

eral. Australia accounts for 50% of the world’s recent mam-malian extinctions, the causes of which are multiple and con-founded. Causes include habitat destruction, fragmentation,and degradation resulting from land clearance, altered fireregimes, and grazing by introduced livestock and rabbits, andvulnerability to predation by introduced foxes. Dasyuridstrack the overall mammalian pattern, in which extinctions anddeclines have been greatest in arid areas and in medium-sizedterrestrial species. An exception to this is the thylacine, whichhas the distinction of being the only large carnivore globallyto become extinct in recent times. The loss of the thylacinerepresents not just a species but also an entire genus and afamily extirpated.

Significance to humansMany species of native marsupials had a place in the dream-

time histories of aboriginal peoples. Aboriginal histories haveindeed revealed ecological information on species that becameextinct prior to European documentation. However, exceptfor the very distinctive animals, aboriginal peoples did notnecessarily distinguish between species of the smaller Aus-tralian mammals. The larger, more distinctive species wereheld in reverence, with dreaming stories, totemic status, andritual treatment that sometimes precluded consumption. Abo-riginal peoples probably hunted and ate all species of carniv-orous marsupials depending on abundance.

Commercial exploitation of carnivorous marsupials for fursor skins has not been recorded, apart from early collecting formuseums, despite the beautiful coat patterns of some of thelarger species. Perhaps the lack of intensely cold climates andwinter pelts contributed to this lack of economic interest.Some species may confer economic benefits in their dietaryproclivity for agricultural and forest insect pests and their abil-ities in dispatching rodents. The diet of eastern quolls livingon farmland is dominated at times of the year by pest pasturegrubs (corbie grubs and wire worms).



The fat-tailed pseudantechinus (Pseudantechinus macdonnellensis) isa carnivorous marsupial. (Photo by B. G. Thomson/Photo Researchers,Inc. Reproduced by permission.)

Economic impacts of carnivorous marsupials are restrictedto the larger species. The predatory abilities of carnivorousmarsupials in tackling large prey (relative to their body size)means that any species larger than 4.8 oz (150 g) can take ondomestic poultry. Inadequately housed poultry may be tar-geted by phascogales, quolls, and devils, particularly at nightand especially by young animals and females feeding young.Lambs in the first 24 hours of life are vulnerable to Tas-

manian devils. Lambs from multiple births and certain breedsof sheep are more vulnerable. Fencing is not difficult (strongmesh wire, no holes, footings 6 in [15 cm] below ground),but education and attitudinal change is a major hindrance.Thylacines would have killed sheep of all sizes. Persecutionon individual properties can have a significant impact on lo-cal populations of devils in particular and certainly did onthylacines.



ResourcesBooksArcher, M., T. Flannery, S. Hand, and J. Long. Prehistoric

Mammals of Australia and New Guinea: One Hundred MillionYears of Evolution. Sydney: UNSW Press, 2002.

Cockburn, A. “Living slow and dying young—senescence inmarsupials.” In Marsupial Biology: Recent Research, NewPerspectives. Sydney: UNSW Press, 1997.

Dickman, R. R. “Distributional ecology of dasyuridmarsupials.” In Predators with Pouches: The Biology ofCarnivorous Marsupials. Melbourne: CSIRO Publishing,2003.

Dixon, J. M. “Thylacinidae.” In Fauna of Australia, Canberra:Australian Government Publishing Service, 1989.

Flannery, T. Mammals of New Guinea. Sydney: Reed Books,1995.

Friend, J. A. “Myrmecobiidae.” In Fauna of Australia, pp. 583-590. Canberra: Australian Government Publishing Service,1989.

Krajewski, C., and M. Westerman. “Molecular systematics ofDasyuromorphia.” In Predators with Pouches: The Biology ofCarnivorous Marsupials. Melbourne: CSIRO Publishing,2003.

Maxwell, S., A. A. Burbidge, and K. Morris. “The Action Planfor Australian Marsupials and Monotremes. IUCN/SSCAustralasian Marsupial and Monotreme Specialist Group,Wildlife Australia, Environment Australia, Canberra ACTAustralia.” In Wildlife Australia, Endangered Species Program,Project Number 500 Report. Canberra: AustralianGovernment Publishing Service, 1996.

Morton, S. R., C. R. Dickman, and T. P. Fletcher.“Dasyuridae.” In Fauna of Australia. Canberra: AustralianGovernment Publishing Service, 1989.

Strahan, R., ed. The Mammals of Australia. Sydney: ReedBooks, 1995.

Taggart, D. A., G. A. Shimmin, C. R. Dickman, and W. G.Breed. “Reproductive Biology of Carnivorous Marsupials:Clues to the Likelihood of Sperm Competition.” InPredators with Pouches: The Biology of Carnivorous Marsupials.Melbourne: CSIRO Publishing, 2003.

Toftegaard, C. L., and A. J. Bradley. “Chemicalcommunication in dasyurid marsupials.” In Predators withPouches: The Biology of Carnivorous Marsupials. Melbourne:CSIRO Publishing, 2003.

Ward, S. J. “Biased sex ratios in litters of carnivorousmarsupials; Why, when & how?” In Predators with Pouches:

The Biology of Carnivorous Marsupials. Melbourne: CSIROPublishing, 2003.

Wilson, B. A., C. R. Dickman, and T. P. Fletcher. “Dasyuriddilemmas: Problems and solutions for conserving Australia’ssmall carnivorous marsupials.” In Predators with Pouches: TheBiology of Carnivorous Marsupials. Melbourne: CSIROPublishing, 2003.

Wroe, S. “Australian marsupial carnivores: an overview ofrecent advances in palaeontology.” In Predators with Pouches:The Biology of Carnivorous Marsupials. Melbourne: CSIROPublishing, 2003.

PeriodicalsDickman, C. R. “An experimental study of competition

between two species of dasyurid marsupials.” EcologicalMonographs 56 (1986): 221–241.

Firestone, K. B., M. S. Elphinstone, W. B. Sherwin, and B. A.Houlden. “Phylogeographical population structure of tigerquolls Dasyurus maculatus (Dasyuridae: Marsupialia), anendangered carnivorous marsupial.” Molecular Ecology 8(1999): 1613–1625.

Fisher, D. O., and C. R. Dickman. “Body size–prey sizerelationships in insectivorous marsupials: tests of threehypotheses.” Ecology 74 (1993): 1871–1883.

Jones, M. E. “Character displacement in Australian dasyuridcarnivores: size relationships and prey size patterns.” Ecology78 (1997): 2569–2587.

Jones, M. E., and L. A. Barmuta. “Diet overlap andabundance of sympatric dasyurid carnivores: a hypothesisof competition?” Journal of Animal Ecology 67 (1998):410–421.

Kraaijeveld-Smit, F. J. L., S. J. Ward, and P. D. Temple-Smith. “Multiple paternity in a field population of a smallcarnivorous marsupial, the agile antechinus, Antechinusagilis.” Behavioral Ecology and Sociobiology 52 (2002): 84–91.

Righetti, J., B. J. Fox, and D. B. Croft. “Behaviouralmechanisms of competition in small dasyurid marsupials.”Australian Journal of Zoology 48 (2000): 561–576.

Soderquist, T. R., and M. Serena. “Juvenile behaviour anddispersal of chuditch (Dasyurus geoffroii) (Marsupialia:Dasyuridae).” Australian Journal of Zoology 48 (2000):551–560.

Taggart, D. A., and P. D. Temple-Smith. “An unusual modeof progressive motility in spermatozoa from the dasyuridmarsupial, Antechinus stuartii.” Reproduction, Fertilization andDevelopment 2 (1990): 107–114.



Resources———. “Transport and storage of spermatozoa in the female

reproductive tract of the brown marsupial mouse, Antechinusstuartii (Dasyuridae).” Journal of Reproduction and Fertility 93(1991): 97–110.

———. “Comparative studies of epididymal morphology andsperm distribution in dasyurid marsupials during thebreeding season.” Journal of Zoology 232 (1994): 365–381.

Menna Jones, PhD

Evolution and systematicsFirst appearing in the fossil record in the early to middle

Miocene, dasyurids were rare (only two species known) un-til the late Miocene, when they increased steadily in diver-sity to replace the thylacinids as the largest group ofAustralian carnivorous marsupials. Dasyurids comprise threeextant subfamilies and one extinct subfamily (the earliestform), which was a sister group to the living subfamilies, andare most closely related to the thylacinids. Molecular data in-dicate that all four radiations of dasyurids took place in thelate mid-Miocene, perhaps in response to climatic drying.Most of the species present in the Pleistocene were of livingtaxa, representatives of which occurred no earlier than thePliocene. It is suggested that the dasyurids are highly spe-cialized among dasyuromorphians in their morphologyrather than primitive. The living fauna currently comprises69 described species in seventeen genera (fifty-three re-stricted to Australia and islands, fourteen in New Guinea andislands). The number of species will almost certainly increasewith taxonomic revisions, particularly with the recognitionof morphologically cryptic but genetically distinct species.There is genetic and morphological differentiation at thesubspecific level in some species.

Physical characteristicsDasyurids are nearly all quadrupedal with long tails, long

pointed snouts, four toes on the front feet, and four to fivetoes on the hind feet. If the fifth toe (inner rear) is present,


▲

Marsupial mice and cats, Tasmanian devil(Dasyuridae)

Class Mammalia

Order Dasyuormorphia

Family Dasyuridae

Thumbnail descriptionA large family of quadrupedal, predatoryinsectivores and carnivores, ranges in size fromminute to medium

Size1.8–25.7 in (46–652 mm); 0.07 oz–28.7 lb (2 g–13 kg)


HabitatOccupy all terrestrial habitats in Australia andPapua New Guinea

Conservation statusEndangered: 6 species; Vulnerable: 9 species;Lower Risk: 4 species; Data Deficient: 9species

DistributionAll of Australia, Tasmania, and Papua New Guinea, including close offshore islands

An eastern quoll (Dasyurus viverrinus) with young. (Photo by TomMcHugh/Photo Researchers, Inc. Reproduced by permission.)

it is a clawless hallux. The footpads, which may be placed onthe ground when standing or moving slowly, extend to theheel and wrist joints. There are four upper and three lowerincisors, two premolars, and four molars, each of which is sim-ilar in form and has distinct cusps with both slicing (carnas-sial) and grinding surfaces (less so in highly carnivorous formssuch as the Tasmanian devil, Sarcophilus laniarius). Across theconsiderable size range (from the 0.14 oz [4 g] Planigale in-grami, the world’s smallest marsupial, to the 28.6 lb [13 kg]devil), body shape is remarkably uniform. Arboreal speciestend to have broader hind feet than terrestrial species, and amore prominent, dexterous hallux. One sandy desert specieshas fine bristles on the footpads. The most extreme variationsin morphology include Antechinomys laniger, which has elon-gated hind legs and a bounding gait, and the heavily built,specialist scavenger, the Tasmanian devil, with massive skull,teeth, and jaw musculature. Coat color is mostly uniformshades of gray, sandy to reddish to dark brown, or black,sometimes with a lighter underbelly. Striking markings arethe province of the larger dasyurids, with white spots on quollsand white markings in the devil, although six New Guineandasyures (three Murexia, one Myoictis, and at least one Phas-colosorex) have dark dorsal stripes, and two diurnal species havespeckled (speckled dasyure, Neophascogale lorentzii) or grizzled(dibbler, Parantechinus spp.) gray fur, all of which may serveas camouflage. Some desert dasyurids have very sparse finetail hair, the smaller quolls have soft, fluffy tails, while othersare finely tufted at the tip, or sport a highly visible black bushybrush that contrasts with the pale body fur. Tail fur may func-tion as flags in communication. Some species, notably the fat-tailed pseudantechinus (Pseudantechinus macdonnellensis), thefat-tailed dunnart (Sminthopsis crassicaudata), and the Tasman-ian devil, store quantities of fat in their tail when environ-mental conditions are good, leading to a distinctly parsnip-shaped tail. The pouch is either well developed (though stillquite shallow compared with diprotodont marsupials) as well

as backwards facing, or it is almost absent (raised lateral ridgesof skin) and downward facing. Teat number varies from fourto 12 and may vary within species. Male Tasmanian devilshave a shallow scrotal pouch.

DistributionDasyurids occur in virtually every terrestrial environment

at all altitudes in mainland Australia and some offshore islands,mainland New Guinea, and some islands between Australiaand New Guinea. In Australia, species diversity of the smallerspecies is higher in arid regions than in the more mesic coastaland sub-coastal areas of the east, southeast, and extreme south-west, while the converse is true for the larger dasyurids (morethan 17 oz [500 g]), quolls, and devils). Species richness ofsmall dasyurids reaches its highest density in the spinifex hum-mock grasslands of arid central Australia (average 5.3, maxi-mum eight species) and is correlated with structural complexityof the habitat that allows niche separation. Population density,on the other hand, reaches highest levels in coastal forest andheath among the smaller species, and is uniformly low in thearid zone. With the disappearance of the chuditch (Dasyurusgeoffroii), there are no larger dasyurids in the arid zone. Theisland of Tasmania supports the largest assemblage of largerdasyurids (three species, historically four) following the his-toric and prehistoric extinction of three of these species frommainland Australia. Dasyurid distribution within New Guineais poorly documented.

HabitatEvery type of terrestrial habitat in Australia and New

Guinea is occupied by dasyurids. Habitat preferences of in-dividual species are strongly associated with food supply, andwith either protection from predators or suitable habitat


Vol. 12: Mammals IFamily: Marsupial mice and cats, Tasmanian devil

A Tasmanian devil (Sarcophilus laniarius) orphaned juvenile beingraised in the Bonorong Wildlife Park in Tasmania, Australia. (Photo byAnimals Animals ©Steven David Miller. Reproduced by permission.)

A Tasmanian devil (Sarcophilus laniarius) feeds in Tasmania. (Photoby Animals Animals ©Don Brown. Reproduced by permission.)

structure for hunting. Even the largest species require densevegetation or crevices as refuge from mammalian and rapto-rial predators. Tasmanian devils cover many miles (kilome-ters) in a night’s foraging and show a preference for habitatswith an open understory or routes through dense vegetation.

BehaviorThe majority of dasyurids for which spacing patterns have

been studied occupies undefended home ranges that overlapwith other individuals of both sexes. The females of twospecies of quolls maintain a core or major part of their homerange exclusive to other females, but overlap with severalmales. The mechanism of territorial defense is not known. Atthe other extreme, among very small arid-zone dasyurids,drifting home ranges, transience, and high mobility are com-mon. Very long-distance movements relative to the diminu-tive size of these animals have been recorded, includingmovements in excess of 0.6 mi (1 km) in 24 hours in the 1.05oz (30 g) white-footed dunnart (Sminthopsis leucopus). Thisstrategy is adaptive in environments where insect prey abun-dance is low and unpredictable.

Feeding ecology and dietThe huge range of body sizes in the Dasyuridae means that

diet encompasses a broad range of invertebrate and vertebrateprey sizes. Prey size increases with body size. Dasyurids thatare less than 5.2 oz (150 g) in body size are mostly insectiv-orous, although they may kill and eat small mammals, lizards,and frogs, and eat carrion of larger species if it is available.Carnivory (consumption of vertebrate prey) gradually re-places insectivory as body size increases. At approximately 2.2lb (1 kg), dasyurids become too large to support themselvesprimarily on invertebrates, and carnivory takes over as the


Family: Marsupial mice and cats, Tasmanian devilVol. 12: Mammals I

A fat-tailed dunnart (Sminthopsis crassicaudata) forages in Australia.(Photo by Animals Animals ©Hans & Judy Beste. Reproduced by per-mission.)

A red-tailed phascogale (Phascogale calura) eats a gecko (Gymnodacty-lus sp.). (Photo by Eric Lindgren/Photo Researchers, Inc. Reproducedby permission.)

principal component of the diet. Only the two largest species,the Tasmanian devil and the spotted-tailed quoll (Dasyurusmaculatus), in which adult females and males exceed 4.4 lb (2kg), are exclusively carnivorous. Tasmanian devils are spe-cialized scavengers as well as being highly effective predators,although all species are likely to eat carrion if it is available.Several species have been recorded eating soft fruit or flow-ers seasonally, including antechinuses and eastern quolls.

Some species, both large and small, are renowned for theirferocity and take prey up to several times their body size. Preyis killed using generalized crushing bites towards the anteriorend. The rear of the skull and the nape are often targeted insmall vertebrates, and devils and spotted-tailed quolls go forthe throat or chest of macropods.

Reproductive biologyThe degree of reproductive synchrony and seasonality in

dasyurids is associated with latitude and climatic predictabil-ity. Reproductive seasonality is known for approximately halfof species with an information bias on a few temperate and

arid zone animals; very little is known of the New Guineanspecies. Most Australian dasyurids are seasonal breeders, andprobably promiscuous. Reproduction is tightly synchronous(three to four weeks) in many temperate species, particularlythe semelparous antechinuses and phascogales, but can extendover a number of months in arid zone animals. New Guineandasyurids from wet tropical forests, for the two species ofMurexia and one species of Phascolosorex, breed year-round.Changes in photoperiod seem to be the most important forcedriving timing of reproduction, which is consistent with asea-sonal breeding in the wet tropical forests. In arid areas, rain-fall events are important in defining the precise timing ofreproduction within the broader seasonal window. This flex-ibility in arid-zone species enables reproduction to be syn-chronized with maximal food supply after rain, as breeding inpredictably seasonal regions is timed so that young emerge inthe late spring food flush.

Conservation statusFourteen (24%) of the 58 smaller (less than 17.6 oz; 500 g)

and two (40%) of the five larger (more than 17.6 oz; 500 g)Australian dasyurids are classified as Vulnerable, Endangered,or Data Deficient (IUCN criteria). This list does not includeanother five small and two larger species that are LowerRisk/Near Threatened. There is insufficient information avail-able to assess the status of the New Guinean dasyurids.

Among the smaller species, larger (3.5–17.6 oz;100–500 g)body size and restricted habitat associations correlate stronglywith endangerment. Habitat loss and fragmentation, alteredfire regimes, and predation are the main threateningprocesses. The larger dasyurids have been more affected byhuman impacts than the smaller species. This is perhaps aconsequence of their lower population densities and greaterneeds for space. They also are more likely to run into directconflict with humans over livestock depredations, and are sus-ceptible to non-target poisoning from fox baits and road mor-tality. The principal factor threatening the smaller quolls hasbeen predation by red foxes, resulting in catastrophic declinesand population extinctions across continental Australia every-where fox populations are abundant. Tasmania has remaineddingo- and fox-free until very recently (2000) and has func-tioned as a refuge for larger dasyurids, supporting healthypopulations of three species.

A recovery plan implemented in 1992 for the chuditch(western quoll) has used captive breeding, reintroduction,and translocation of quolls to suitable areas of habitat withinits former distributional range, as well as intense ongoingfox control through poison-baiting programs. The success



Brush-tailed phascogales (Phascogale tapoatafa) prefer Australia’s eu-calyptus forests for foraging and nesting sites. (Photo by Michael Mor-combe. Bruce Coleman, Inc. Reproduced by permission.)

A slender-tailed dunnart (Sminthopsis murina) scenting the air. (Photoby Animals Animals ©B. & B. Wells, OSF. Reproduced by permission.)

Significance to humansApart from an occasional food source, the smaller species

of daysurids seem not to have had great significance for abo-riginal peoples. The larger, more distinctive species likequolls, were frequently totemic species and had dreaming his-tories and individual names that persisted long after they be-came extinct in a region.



of this plan saw the recovery of this species from Endan-gered to Vulnerable in 1996. Chuditch may soon be re-moved from threatened species lists as well, although it islikely to retain the status of Lower Risk/Conservation De-pendent, referring to the requirement in perpetuity for foxcontrol. No recovery plans have yet been adopted for thesmaller species.


1

2

3

4

5

6

1. Long-tailed planigale (Planigale ingrami); 2. Long-tailed dunnart (Sminthopsis longicaudata); 3. Brush-tailed phascogale (Phascogale tapoatafa);4. Pilbara ningaui (Ningaui timealeyi); 5. Kultarr (Antechinomys laniger). (Illustration by Emily Damstra)


1

2

3

4

5

6

1. Speckled dasyure (Neophascogale lorentzi); 2. Southern dibbler (Parantechinus apicalis); 3. Mulgara (Dasycercus cristicauda); 4. Brown an-techinus (Antechinus stuartii); 5. Tasmanian devil (Sarcophilus laniarius); 6. Chuditch (Dasyurus geoffroii). (Illustration by Emily Damstra)


MulgaraDasycercus cristicauda

SUBFAMILYDasyurinae

TAXONOMYDasycercus cristicauda (Krefft, 1867), South Australia, Australia,probably Lake Alexandrina. Two subspecies described.

OTHER COMMON NAMESEnglish: Crest-tailed marsupial mouse.

PHYSICAL CHARACTERISTICSLength 4.9–8.7 in (125–220 mm). Light brown above, pale be-low with crest of long black fur distal two-thirds of short tail;short, rounded ears; stores fat in the base of the tail.

DISTRIBUTIONInland central and western Australia.

HABITATFound in arid, sandy regions.

BEHAVIORLives solitarily in burrows it digs in flats between or on lowerslopes of sand dunes.

FEEDING ECOLOGY AND DIETGeneralized insectivore, takes small vertebrates.

REPRODUCTIVE BIOLOGYQuite long-lived for a dasyurid. Breed for up to six years andproduce up to eight young. Probably promiscuous.

CONSERVATION STATUSVulnerable. Decline possibly a result of predation by intro-duced foxes and cats, and changes in fire regimes. Susceptibleto decline because of larger body size and restricted habitat.


ChuditchDasyurus geoffroii

SUBFAMILYDasyurinae

TAXONOMYDasyurus geoffroii (Gould, 1841), Liverpool Plains, New SouthWales, Australia.

OTHER COMMON NAMESEnglish: Western quoll.

PHYSICAL CHARACTERISTICSBrown above, light below, with conspicuous white spots onbody, and bushy tail black on distal half.

DISTRIBUTIONFormerly western two-thirds of inland Australia. Now restrictedto nine localities (including reintroduction sites) in the extremesouthwest.

Species accounts

Vol. 12: MammalsFamily: Marsupial mice and cats, Tasmanian devil

Planigale ingrami

Dasycercus cristicauda

Dasyurus geoffroii

Ningaui timealeyi

HABITATOpen, dry eucalypt forests, woodlands, and shrublands. For-merly deserts.

BEHAVIORSolitary. Females maintain an exclusive core range that over-laps with several males.

FEEDING ECOLOGY AND DIETPrimarily insects, also birds, mammals, and reptiles. Can killvertebrate prey larger than body size.

REPRODUCTIVE BIOLOGYUp to six young. Longevity in the wild rarely more than threeyears. Probably promiscuous.

CONSERVATION STATUSVulnerable. Was Endangered until 1996. Introduced red foxesare the primary cause of decline. Current populations requireongoing fox baiting for their survival.

SIGNIFICANCE TO HUMANSA nuisance as a predator of poultry. ◆

Speckled dasyureNeophascogale lorentzi

SUBFAMILYDasyurinae

TAXONOMYNeophascogale lorentzi (Jentink, 1911), Irian Jaya, Indonesia.


PHYSICAL CHARACTERISTICSLength 6.5–8.7 in (166–220 mm). Silvery speckled gray to red-dish coat with long, white-tipped tail; long, pointed snout,small eyes, and very long claws.

DISTRIBUTIONHigh mountain forests of western New Guinea (over 6,500 ft;2,000 m).

HABITATWet montane moss forest.

BEHAVIORDiurnal.

FEEDING ECOLOGY AND DIETLarge insects, probably small vertebrates.

REPRODUCTIVE BIOLOGYNothing is known, but probably promiscuous.

CONSERVATION STATUSData Deficient.


Southern dibblerParantechinus apicalis

SUBFAMILYDasyurinae

TAXONOMYParantechinus apicalis (Gray, 1842), Southwestern Western Aus-tralia, Australia.



Sarcophilus laniarius

Neophascogale lorentzi

Phascogale tapoatafa

Parantechinus apicalis

Sminthopsis longicaudata

OTHER COMMON NAMESEnglish: Freckled antechninus, speckled marsupial mouse.

PHYSICAL CHARACTERISTICSLength 5.5–5.7 in (140–145 mm). Coarse brownish gray fur,speckled with white, and pale below; tapered hairy tail; whitering around eye.

DISTRIBUTIONA few locations in extreme southwestern Western Australia andoffshore islands.

HABITATShrubland.

BEHAVIORNothing is known.

FEEDING ECOLOGY AND DIETLarge insects, small reptiles.

REPRODUCTIVE BIOLOGYFacultatively semelparous; male die-off in some years in islandpopulation but not on mainland. Probably promiscuous.

CONSERVATION STATUSEndangered. Restricted habitat associations may play a role.


Tasmanian devilSarcophilus laniarius

SUBFAMILYDasyurinae

TAXONOMYSarcophilus laniarius (Owen, 1838), Wellington caves (Pleis-tocene), Australia.


PHYSICAL CHARACTERISTICSLength 22.4–25.7 in (570–652 mm). Black all over with coarselong fur on medium-length tail; white markings most commonon chest as well as on shoulders and rump; robust build withmassive head, sloping hindquarters, and very short legs; fatstorage in tail.

DISTRIBUTIONThe island of Tasmania, Australia.

HABITATOpen forests and woodlands.

BEHAVIORSocial, but can be solitary; aggregates at carcasses. Promiscuousmating system.

FEEDING ECOLOGY AND DIETPredator and specialized scavenger. Medium-sized mammalssuch as wallabies and possums.

REPRODUCTIVE BIOLOGYLives up to five or six years in the wild. Up to four youngfrom ages two to six. Probably promiscuous.

CONSERVATION STATUSLower Risk. Common in suitable habitat.

SIGNIFICANCE TO HUMANSPredates poultry and weak lambs. ◆

Brown antechinusAntechinus stuartii

SUBFAMILYDasyurinae

TAXONOMYAntechinus stuartii (Macleay, 1841), Manly, New South Wales,Australia. Two subspecies described.

OTHER COMMON NAMESEnglish: Macleay’s marsupial mouse, Stuart’s antechinus.

PHYSICAL CHARACTERISTICSLength 2.9–5.5 in (74–140 mm). Uniform grayish brown; palerbelow, with thin, hairy tail almost body length; broad headwith pale fur around eye.

DISTRIBUTIONAustralian east coast and hinterland from southeast Queenslandto southern New South Wales.

HABITATWet to dry forests with dense ground cover and numerous logs.

BEHAVIORNocturnal, but may be active during day if food scarce. Terres-trial; partly arboreal if sparse groundcover or larger terrestrialcompetitor present.



Antechinus stuartii

Antechinomys laniger

FEEDING ECOLOGY AND DIETSmall to large insects, beetles, and spiders.

REPRODUCTIVE BIOLOGYTightly synchronized mating season (two weeks). Semelparouswith abrupt male die-off immediately after mating season.Probably promiscuous.

CONSERVATION STATUSLower Risk.


Brush-tailed phascogalePhascogale tapoatafa

SUBFAMILYDasyurinae

TAXONOMYPhascogale tapoatafa (F. Meyer, 1793), Sydney, New SouthWales, Australia.

OTHER COMMON NAMESEnglish: Tuan, common wambenger, black-tailed phascogale.

PHYSICAL CHARACTERISTICSLength 5.8–10.3 in (148–261 mm). Uniform grizzled grayabove, cream to white below, with large, naked ears, and con-spicuous black brush tail with hairs up to 2.1 in (55 mm) long.

DISTRIBUTIONMesic coastal and hinterland areas of southeastern and south-western Australia (P. t. tapoatafa). Monsoonal northern Aus-tralia (P. t. pirata).

HABITATDry eucalypt forest and woodlands with open under-story intemperate and tropical Australia.

BEHAVIOROne of most arboreal of the dasyurids; very agile hunteraboveground. Nesting and mating in tree hollows.

FEEDING ECOLOGY AND DIETNectar, large insects, spiders, and small vertebrates. Forages bytearing away bark and probing into crevices.

REPRODUCTIVE BIOLOGYSemelparous with complete male die-off after a synchronizedthree-week mating season. Probably promiscuous.

CONSERVATION STATUSLower Risk (Least Concern: P. t. tapoatafa and Near Threat-ened: P. t. pirata).

SIGNIFICANCE TO HUMANSOccasionally takes penned poultry. ◆

KultarrAntechinomys laniger

SUBFAMILYSminthopsinae

TAXONOMYAntechinomys laniger (Gould, 1856), interior New South Wales,Australia. Two subspecies described.

OTHER COMMON NAMESEnglish: Jerboa, marsupial mouse.

PHYSICAL CHARACTERISTICSLength 2.8–3.9 in (70–100 mm). Grizzled fawn-gray above,white below, with very large ears, large eyes, and a long tailwith black brushed tip; hind-foot greatly elongated with onlyfour toes.

DISTRIBUTIONBroad band across central and southern arid Australia.

HABITATStony and sandy desert plains and acacia scrubland where smallbushes constitute the principal vegetation.

BEHAVIORBounding gait; terrestrial; shelters beneath tussocks and incracks in the soil, burrows, and logs. Nocturnal.

FEEDING ECOLOGY AND DIETLarge insects and spiders.

REPRODUCTIVE BIOLOGYIteroparous (breeds in multiple years) with long breeding sea-son. Pouch a crescent-like fold over anterior part of mammaryglands. Six or eight teats. Probably promiscuous.

CONSERVATION STATUSData Deficient. Uncommon over most of range. Populationsappear to fluctuate seasonally. Not directly impacted by hu-mans.


Pilbara ningauiNingaui timealeyi


TAXONOMYNingaui timealeyi (Archer, 1975), Western Australia, Australia.

OTHER COMMON NAMESEnglish: Ealey’s ningaui.

PHYSICAL CHARACTERISTICSLength 1.8–2.2 in (46–57 mm). Minute predatory dasyruidwith grizzled gray, bristly fur, and furred, long tail.

DISTRIBUTIONRestricted distribution on Hamersley Plateau, Western Aus-tralia.

HABITATSemi-arid grasslands. Prefers drainage lines where large hum-mocks of spinifex, scattered shrubs, and mallee trees grow.

BEHAVIORMostly nocturnal.

FEEDING ECOLOGY AND DIETDesert centipedes and cockroaches that may be larger than it-self.



REPRODUCTIVE BIOLOGYProbably promiscuous. Potentially long breeding season (sixmonths) to allow for annual rains. Pouch a simple furless de-pression in belly. Semelparous. Four to six young are indepen-dent at 0.07 oz (2 g) body weight.

CONSERVATION STATUSLower Risk. Common. May survive only in moister pockets ofhabitat in dry seasons, repopulating after rains.


Long-tailed dunnartSminthopsis longicaudata


TAXONOMYSminthopsis longicaudata (Spencer, 1909), Western Australia,Australia.

OTHER COMMON NAMESEnglish: Long-tailed marsupial mouse.

PHYSICAL CHARACTERISTICSLength 3.1–3.9 in (80–100 mm). Gray above, white below,white feet; scaly tail with short hairs more than twice length ofhead and body.

DISTRIBUTIONArid interior of western and central Australia.

HABITATRugged scree, boulders, and rocky plateau, sparsely vegetatedwith shrubs and spinifex hummocks.

BEHAVIORActive and capable climber with striated footpads.

FEEDING ECOLOGY AND DIETSmall to large insects and spiders.

REPRODUCTIVE BIOLOGYProbably promiscuous. Long breeding season, winter to spring.

CONSERVATION STATUSLower Risk. One of the most rarely recorded dasyurids, butwith a broad, undisturbed range. May be locally common.


Long-tailed planigalePlanigale ingrami


TAXONOMYPlanigale ingrami (Thomas, 1906), Alexandria, Northern Terri-tory, Australia.

OTHER COMMON NAMESEnglish: Northern planigale.

PHYSICAL CHARACTERISTICSLength 2.2–2.6 in (55–65 mm). Smallest of the planigales andthe smallest marsupial with very flat head and thin tail longerthan head and body.

DISTRIBUTIONNorthern Australia.

HABITATSeasonally flooded grasslands and savanna woodlands.

BEHAVIORForages and rests in crevices in moist, contracting (cracking)soils, under rocks, and in tussocks. Planigales may have evolvedthe very flat head to occupy the niche of foraging in seasonallyflooded cracking soils.

FEEDING ECOLOGY AND DIETRapacious appetite; insects, lizards, and even young mammalsalmost as large as itself. Larger insects are killed by persistentbiting.

REPRODUCTIVE BIOLOGYProbably promiscuous. Breeding throughout year but concen-trated in late summer. Four to eight young.

CONSERVATION STATUSLower Risk. Difficult to study on account of minute size. Noaccurate assessment of populations.

SIGNIFICANCE TO HUMANSNone known.








status

Not threatenedDusky antechinusAntechinus swainsonii;English: Dusky marsupial;Spanish: Antechino sombrio

Pale pinkish fawn through gray to copperybrown. Underparts creamy or white. Short,dense, and rather coarse hair and long-haired tail. Head and body length 3.0–6.9 in (7.5–17.5 cm), tail length 2.6–6.1 in (6.5–15.5 cm). Typical male 1.7–3.2 oz (48–90 g), female 1.1–1.9 oz (31–55 g).

Found mostly in dense, moistforest. Monestrous, breedingpattern of three months fol-lowed by a synchronized male die-off. One litter producedper year.

Southeast Queensland, east New South Wales, east and southeastVictoria, coastal south-east Australia, and Tasmania.

Mostly invertebrates thesize of small insects to domestic sparrows, butcan supplement diet with fruit, such as blackberries.

Yellow-footed antechinusAntechinus flavipesSpanish: Antechino de patas amarillas

Pale pinkish fawn through gray to copperybrown. Underparts creamy or white. Short, dense and rather coarse hair, short, hooked claws. Head and body length 3.0–6.9 in (7.5–17.5 cm), tail length 2.6–6.1 in (6.5–15.5 cm).

Found in wide variety of forest and brushland habitat with sufficient cover. Very active, climbs well. Monestrous, three month breeding period, one litter produced per year.

Cape York Peninsula (Queensland) to Victoria and southeast South Australia, southwest Western Australia.

Mostly invertebrates. Not threatened

Little red kalutaDasykaluta rosamondaeSpanish: Kalutica rojiza

Russet to coppery brown, rough fur. Headand body length 3.5–4.3 in (9–11 cm), tail length 2.2–2.8 in (5.5–7 cm), weight 0.7–1.4 oz (20–40 g).

Found in spinifex grassland. Mating occurs in September, followed by synchronized male die-off.

Pilbara region of north-western Western Australia.

Insects and small vertebrates.

Not threatened

Northern quollDasyurus hallucatusEnglish: Little northern cat; Spanish: Quoll norte'

Upperparts predominantly gray or darker brown. Tip and ventral surface of tail are dark brown or black. Head and body length9.4–13.8 in (24–35 cm), tail length 8.3–12.2 in (21–31 cm).

Found in woodland and rocky areas. Monestrous, winter breeders, one litter produceda year. Cats maintained in pairs except when female has young.

Australia, in north Northern Territory, northand northeast Queens-land, and north WesternAustralia.

Aggressive carnivores. Diet consists of mammals such as largerock rats, common rockrats, and sandstone antechinus, as well as reptiles, worms, ants,termites, grasshoppers, beetles, figs, and other soft fruits.


Spotted-tailed quollDasyurus maculatusEnglish: Tiger quoll;Spanish: Quoll de cola moteada

Upperparts grayish or dark brown, white spots or blotches on back and sides. Spotsusually extend well onto the tail. Head andbody length 15.7–29.9 in (40–76 cm), taillength 19.7–22.0 in (50–56 cm).

Found in dry forest and open country. Nocturnal hunter. Lengthy courtship. Mones-trous, winter breeders, six to eight young produced per year.

Australia, in east Queensland, east New South Wales, east and south Victoria, southeastSouth Australia, and Tasmania. Formerly found in South Australia.

Predatory animal, but will also eat vegetable matter. May consume mammals as large as wallabies.

Vulnerable

Eastern quollDasyurus viverrinusSpanish: Quoll oriental

Upperparts mostly grayish, or olive brownto dark rufous brown, underparts paler yellowish or white. Prominent white spotsor blotches on back and sides. Head and body length 13.8–17.7 in (35–45 cm), tail length 8.3–11.8 in (21–30 cm).

Variety of habitats, including rainforest, heathland, alpine areas, and scrub. Prefers dry grassland, forest mosaics bounded by agricultural land, drier forest, and open country.Shelters in rock piles or hollow logs. Five to six youngper litter. Maximum known lifespan is six years, ten months.

Probably survives only in Tasmania; formerly South Australia, New South Wales, and Victoria.

Predatory animal, but will also consume vegetable matter. Insectsand rodents also compose diet.


New Guinean quollDasyurus albopunctatusSpanish: Quoll de Nueva Guinea

Upperparts grayish or olive brown to darkrufous brown. Coat is coarse with little underfur. Head and body length 9.4–13.8 in (24–35 cm), tail length 8.3–12.2 in(21–31 cm).

Found in dense, moist forest in a variety of conditions up to an altitude of 11,480 ft (3,500 m) in New Guinea. Primarily terrestrial, can climbwell, nocturnal.

New Guinea. High proportion of insects.

Vulnerable

Short-furred dasyureMurexia longicaudataFrench: Phascogalin’s de Nouvelle-Guin’e;German: Neuguinea Beutelmäuse

Dull grayish brown upperparts, white underparts, long, sparsely haired tail, few long hairs at tip. Head and body length 4.1–11.2 in (10.5–28.5 cm) and tail length 5.7–9.4 in (14.5–24 cm).

Found in all lowland and midmountain forests of New Guinea, from sea level to 6,230 ft (1,900 m).

New Guinea, Aru Islands. Insectivorous and carnivorous.

Not threatened

Broad-striped dasyureMurexia rothschildi

Dark, grayish brown upperparts. Broad, black dorsal stripe is present. Underparts are light brown, fur is short and dense. Head and body length 4.1–11.2 in (10.5–28.5 cm), tail length 5.7–9.4 in (14.5–24 cm).

Known from only eight specimens, this species has an altitudinal range of 3,280–6,560 ft (1,000–2,000 m).

Southeast New Guinea. Presumed to be insectivorous and carnivorous.

Data Deficient

[continued]






status

Three-striped dasyureMyoictis melas

Upperparts richly variegated chestnut mixed with black and yellow, head is darkrusty red. Most colorful of all marsupials Long tapered tail and slender snout. Headand body length 6.7–9.8 in (17–25 cm), tail length 5.9–9.1 in (15–23 cm).

Occurs in most rainforests of the lowland and mid-mountains of New Guinea. Nocturnal and scansorial in habit.

New Guinea; Salawati Island and Aru Islands (Indonesia).

Plants and insects, mainly ants and termites.

Not threatened

Wongai ningauiNingaui rideiSpanish: Ningaui vongai

Upperparts dark brown to black, under-parts usually yellowish, sides of face salmon to brown. Thin tail. Length known only from two young samples: head and body length 1.9–2.1 in (4.9–5.3 cm), tail length 1.9–2.0 in (4.8–5 cm).

Found in dry grassland and savanna, mainly under dry conditions. Nocturnal. Uses dry, raspy sound to communicate.

Australia, in Western Australia to New South Wales and Victoria.

Insects and small invertebrates.

Not threatened

Sandstone dibblerParantechinus bilarniEnglish: Northern dibbler

Upperparts grizzled brown, underparts pale gray, cinnamon patches behind largeears. Head and body length 2.2–3.9 in (5.7–10 cm), tail length 3.2–4.5 in (8.2–11.5 cm), and weight 0.42–1.6 oz (12–44 g). Tail is long and thin.

Found in rugged, rocky country covered with eucalyptus forest, perennial grasses. Mating occurs late June to early July, four to five young constitute a litter.

Northern Territory, Australia.

Mostly insects. Not threatened

Red-tailed phascogale Phascogale calura English: Red-tailedwamberger; Spanish: Fascogale de cola roja

Grayish upper parts, white underparts. Head and body length 3.7–4.8 in (9.3–12.2 cm), tail length 4.7–1.8 in (11.9–4.5 cm), and weight 1.3–2.4 oz (38–68 g). Rear half covered by long, silky, black hairs.

Found in heavy, humid forest and more sparsely timbered arid regions. Nests consist of leaves and twigs in the forks or holes of trees, some are built on ground. Nocturnal.

Inland southwest Western Australia, formerly in Northern Territory. South Australia,northwest Victoria, southwest New South Wales. Most likely extinct,except in Western Australia wheat belt.

Small mammals, birds, lizards, and insects.

Endangered

Narrow-striped marsupial shrewPhascolosorex dorsalisSpanish: Murasà marsupial rayada

Grizzled gray-brown coloration withchestnut red underneath. Head and body length 2.6–5.3 in (6.7–13.4 cm), tail length 2.4–4.3 in (6–11 cm). Thin black stripe runs from head to tail.

Occur in mountain forests at high altitudes from 3,970 to 10,170 ft (1,210–3,100 m). Nocturnal and scansorial (climbing) in habit.

West and east interior of New Guinea.

Mainly insects. Not threatened

Pygmy planigalePlanigale maculata

Upperparts pale tawny olive, darker tawny,or brownish gray; underside olive buff, fuscous, or light tan. Head and body length 2.0–3.9 in (5–10 cm), tail length 1.8–3.5 in (4.5–9 cm), average weight 0.54 oz (15.3 g) for males, 0.38 oz (10.9 g) for females.

Can be found in savanna woodland and grassland, and reportedly in rainforests. Shelter consists of rocky areas, clumps of grass, basesof trees, or hollow logs. Nests are saucer-shaped, composed of dry grass. Most nocturnal, primarily terrestrial.

East Queensland, north-east New South Wales, and north Northern Territory, Australia.

Insects, spiders, andsmall mammals.

Not threatened

Gile's planigalePlanigale gilesiSpanish: Planigale de Gile

Upperparts pale tawny olive, darker tawny, or brownish gray, underparts are olive buff,fuscous, or light tan. Head and body length 2.0–3.9 in (5–10 cm), tail length 1.8–3.5 in (4.5–9 mm), weight 0.18 oz (5 g).

Can be found mainly in savanna woodland and grass-land. Seemingly nocturnal, but active throughout periods of the day. Avid predator.

Northeast South Australia, northwest NewSouth Wales, and southwest Queensland, Australia.

Insects, spiders, small lizards, and small mammals.

Not threatened

Fat-tailed pseudantechinusPseudantechinus macdonnellensisSpanish: Pseudantechino de cola ancha

Upperparts are grayish brown, chestnut patches behind ears, underparts are grayish white. Head and body length 3.7–4.1 in (9.5–10.5 cm), tail length 3.0–3.3 in (7.5–8.5 cm), and weight 0.71–1.6 oz (20–45 g).

Can be found mainly on rocky hills, breakaways and in termite mounds. Predominantly nocturnal. Females produce one litter annually. Mating occurs in winter and spring.

North Western Australia, Northern Territory, and central deserts in Australia.

Mainly insects. Not threatened

Fat-tailed dunnartSminthopsis crassicaudataSpanish: Dunart de cola gorda

Soft, fine, dense fur, buffy to grayish in color, underparts are white or grayish white. Feet usually white, tail is brownish or grayish. Some species have a median facial stripe. Head and body length 3.3 in (8.3 cm), weight 0.35–0.53 oz (10–15 g).

Can be found mainly in drycountry, but sometimes in moist areas. Dig burrows or construct nest of grasses and leaves. Mainly terrestrial, but some are agile climbers. Nocturnal.

South Australia, south-west Queensland, south-east Northern Territory, south Western Australia, west New South Wales, and west Victoria.

Mainly insectivorous, but also eats small vertebrates, such as lizards and mice.

Not threatened

[continued]






status

Not threatenedSlender-tailed dunnartSminthopsis murinaGerman: Kleine Schmalfussbeutelmaus;Spanish: Dunart de cola delgada

Back and sides buffy to grayish, under-parts white or grayish white. Feet usually white, tail is brownish or grayish. Head and body length 2.8–4.7 in (7–12 cm), and tail length 2.2–5.1 in (5.5–13 cm).

Can be found in moist forest or savanna. Terrestrial and nocturnal. Can be up to eight young in a litter.

Southwest Western Australia, southeast South Australia, Victoria, New South Wales, and east Queensland.

Mainly insectivorous, but also eats small vertebrates. May also jump high to catch moths.

Sandhill dunnartSminthopsis psammophila

Back and sides buffy to grayish, under-parts white or grayish white. Tail accumulates fat when food is scarce. Head and body length 2.8–4.7 in (7–12 cm), tail length 2.2–5.1 in (5.5–13 cm).

Can be found in moist forest or savanna, but also arid grassland and desert. Terrestrial and nocturnal.

Australia, in southwest Northern Territory (vicinity of Ayer's Rock) and Eyre Peninsula in South Australia.

Mainly insectivorous, but small vertebrates also eaten.

Endangered

White-footed dunnartSminthopsis leucopusSpanish: Dunart de patas blancas

Back and sides buffy to grayish, underparts white or grayish white. Head and body length 4.4 in (11.2 cm), weight 1.1 oz (30 g).

Can be found in moist forest or savanna. Terrestrial and nocturnal.

South and southeast Victoria, Tasmania, New South Wales, and Queensland, Australia.

Insects and small vertebrates.

Data Deficient

Resources

BooksArcher, M., T. Flannery, S. Hand, and J. Long. (2002).

Prehistoric Mammals of Australia and New Guinea: OneHundred Million Years of Evolution. Sydney: UNSW Press,2002.

Dickman, R. R. “Distributional Ecology of DasyuridMarsupials.” In Predators with Pouches: The Biology ofCarnivorous Marsupials, edited by M. E. Jones, C. R.Dickman, and M. Archer. Melbourne: CSIRO Publishing:2003.

Flannery, T. Mammals of New Guinea. Sydney: Reed Books,1995.

Geiser, F. “Thermal Biology and Energetics of CarnivorousMarsupials.” In Predators with Pouches: The Biology ofCarnivorous Marsupials, edited by M. E. Jones, C. R.Dickman, and M. Archer. Melbourne: CSIRO Books, 2003.

Krajewski, C., and M. Westerman. “Molecular Systematics ofDasyuromorphia.” In Predators with Pouches: The Biology ofCarnivorous Marsupials, edited by M. E. Jones, C. R.Dickman, and M. Archer. Melbourne: CSIRO Publishing,2003.

McAllan, B. “Timing of Reproduction in CarnivorousMarsupials.” In Predators with Pouches: The Biology ofCarnivorous Marsupials, edited by M. E. Jones, C. R.Dickman, and M. Archer. Melbourne: CSIRO Publishing,2003.

Morris, K., B. Johnson, P. Orell, A. Wayne, and G. Gaikorst.“Recovery of the Threatened Chuditch (Dasyurus geoffroiiGould, 1841: A Case Study.” In Predators with Pouches: TheBiology of Carnivorous Marsupials, edited by M. E. Jones, C.

R. Dickman, and M. Archer. Melbourne: CSIROPublishing, 2003.

Morton, S. R., C. R. Dickman, and T. P. Fletcher.“Dasyuridae.” In Fauna of Australia, edited by D. W.Walton, and B. J. Richardson. Canberra: AustralianGovernment Publishing Service, 1989.

Strahan, R., ed. The Mammals of Australia. Sydney: AustralianMuseum, Reed Books, 1995.

Wilson, B. A., C. R. Dickman, and T. P. Fletcher. “DasyuridDilemmas: Problems and Solutions for ConservingAustralia’s Small Carnivorous Marsupials.” In Predators withPouches: The Biology of Carnivorous Marsupials, edited by M.E. Jones, C. R. Dickman, and M. Archer. Melbourne:CSIRO Publishing, 2003.

Wroe, S. “Australian Marsupial Carnivores: An Overview ofRecent Advances in Paleontology.” In Predators with Pouches:The Biology of Carnivorous Marsupials, edited by M. E. Jones,C. R. Dickman, and M. Archer. Melbourne: CSIROPublishing, 2003.

PeriodicalsFisher, D. O., C. R. Dickman. (1993). “Body Size-Prey Size

Relationships in Insectivorous Marsupials: Tests of ThreeHypotheses.” Ecology 74 (1993): 1871–1883.

Jones, M. E., and L. A. Barmuta. “Diet Overlap andAbundance of Sympatric Dasyurid Carnivores: AHypothesis of Competition?” Journal of Animal Ecology 67(1998): 410–421.

Menna Jones, PhD

Evolution and systematicsThe evolutionary history of this family is poorly known.

There is only one known species, the living numbat (Myrme-cobius fasciatus), which is represented in a few Pleistocene cavedeposits in Western Australia and western New South Wales.Myrmecobiids appear to be a sister group of a combined thy-lacinid-dasyurid group within the Dasyuromorphia.

The taxonomy for this species is Myrmecobius fasciatus (Wa-terhouse, 1836), Mt. Kokeby, Western Australia, Australia.

Physical characteristicsNumbats are one of the more beautiful and strikingly

marked Australian mammals. Morphologically similar to thedasyurids, they are quadrupedal, place the heel of the hindfoot on the ground when standing, and the snout is elongatedand sharply pointed. Unique features of numbats include avery long tail, almost equal to the head and body length, andears that are furred, erect, and quite narrow. Numbats alsohave more teeth than dasyurids; with five structurally simplemolar teeth lacking defined cusps. Males and females are asimilar size (1–1.1 lb; 0.45–0.5 kg). The medium-length soft

fur is reddish brown in color, darker towards the rump andpaler below, with five to six transverse white stripes across thelower back and a white-bordered black stripe running fromthe snout to the base of the ear. Tail hairs are long and of-ten erect. The female has four teats surrounded by crimpedhair on the lower abdomen but there is no visible pouch. Thevery long, thin tongue can protrude several inches/centime-ters beyond the end of the snout when feeding.

DistributionAt the time of European settlement (late eighteenth cen-

tury to early nineteenth century), numbats were distributedin a broad band across the southern half of central andWestern Australia, the eastern and northern limits of theirrange represented by western New South Wales and south-western Northern Territory, respectively. By 1985, num-bats had disappeared from all but two small locations inthe southwest of Western Australia. A program of feral redfox (Vulpes vulpes) control, reintroduction, and transloca-tions has resulted in nine wild and two free-ranging fencedpopulations.


▲

Numbat(Myrmecobiidae)

Class Mammalia

Order Dasyuomorphia

Family Myrmecobiidae

Thumbnail descriptionMedium-sized reddish brown specialized termite-feeder with five to six striking white stripesacross lower back, and a very long tail withlong, erect hairs; long, thin tongue can protrudewell beyond end of snout

Size7.9–10.8 in (200–274 mm); 0.66–1.5 lb(0.3–0.7 kg)


HabitatForest, woodland, and spinifex

Conservation statusVulnerable

DistributionExtreme southwestern Australia; formerly broad band across western, southern halfof Australia

HabitatThe key to numbat presence is an abundance of termites,

their primary food. The second prerequisite seems to be ade-quate ground-level cover, in the form of thickets of dense veg-etation or hollow logs, which provides a refuge from predators.Primary predators would have been diurnal raptors, but foxesare now the major force driving extinction of populations. Hol-low logs, which provide complete protection from largerpredators, are probably more important in the presence offoxes. Numbats formerly occupied a variety of vegetationtypes, from open forest to woodland to hummock grasslandsin the arid zone, although most sites had eucalypt trees.

BehaviorThe numbat stands out among Australian mammals in be-

ing exclusively diurnal, probably as a consequence of their ter-mite diet. Seasonal patterns in daily activity correspond closelyto the abundance of termites in galleries close to the surface.Numbats are active in the warmer parts of the day, from mid-morning until late afternoon, except in the hottest part of sum-

mer, when they divide their activity into two periods: dawnuntil midday and then late afternoon. When not active, num-bats sleep in hollow logs or trees, or underground burrowsthat they have dug themselves. They make a nest in a den withgrass or shredded bark, and they regularly use more than oneden. Numbats are solitary except when females are rearingyoung and occupy home ranges from which other individualsof the same sex are excluded. Young disperse in December andhave been recorded moving in excess of 9 mi (15 km).

Feeding ecology and dietNumbats are highly specialized with a diet that consists al-

most entirely of termites, although some ants are taken inci-dentally. Numbats sniff out underground termite galleries andexpose termites by digging small holes and turning over sticksand branches. They have extremely sharp claws that they usefor digging but the forelimbs are not especially strong. Thelong, slender tongue is inserted deep into the winding ter-mite galleries and withdrawn rapidly, insects adhering to salivaon the tongue. Numbats have very large salivary glands tosupply the prodigious quantities of saliva required for thismode of feeding. The molar teeth are simple in structure withthree almost equal cusps and the number can vary in indi-viduals, and also from side to side in the same individual, sug-gesting that the molars receive light use. Unlike othermammalian anteaters, numbats show no obvious specializa-tions for termite-eating in the stomach.

Reproductive biologyBreeding is probably promiscuous and is seasonal with most

young born in summer, after a 14-day gestation. Males as wellas females show an annual cycle of fertility. The female usu-ally carries the full complement of four young that, in the ab-


Vol. 12: Mammals IFamily: Numbat

Numbat (Myrmecobius fasciatus). (Illustration by Marguette Dongvillo)

Foraging on the forest floor, the numbat (Myrmecobius fasciatus) un-earths insects. (Photo by H. & J. Beste/Nature Focus, Australian Mu-seum. Reproduced by permission.)

sence of a pouch, maintain attachment orally and by entwin-ing the forelimbs in the crimped fur of the mammary region.Development is slow and young are carried for six to sevenmonths, after which they are deposited in a nest. At this stagethey are furred with visible stripes, but their eyes are not yetopen. The young are suckled for another three months, untilat least late October. During this time they gradually exploreand forage within their mother’s home range. The female maymove them to another nest, particularly in response to distur-bance, and does so by carrying small young on her back.

Conservation statusThe decline of the numbat, from its formerly wide distri-

bution at the time of European settlement, is documented.Populations disappeared gradually in an east-west progression,with the expansion in range of introduced foxes. The rate ofdisappearance accelerated after 1920 when fox populationssuddenly exploded. By the 1960s, numbats persisted in onlytwo locations: the Gibson Desert and the southwest of West-ern Australia. The desert population disappeared first, leavingonly two populations to the southwest of Perth by 1985.

An experimental fox control program, initiated in the early1980s, demonstrated that numbat populations increased

when fox populations were suppressed by monthly poisonbaiting. Fox predation was confirmed as the primary factorin the decline of numbats. Since 1985, there has been a suc-cessful recovery program involving translocation of wild in-dividuals, supplemented with the reintroduction ofcaptive-bred numbats to suitable habitat in nature reserveswithin their former southwestern range. This program, com-bined with regular fox baiting, has increased wild populationsto nine localities. An additional two populations live withinlarge, fenced reserves in South Australia and New SouthWales. Rates of increase in translocated populations vary withthe levels of predation by (native) raptors, residual levels offoxes and feral cats, dispersal opportunities, and habitat typethat are related to food supply. Numbats probably never oc-curred in high density, even though they were widespread.Populations in which wide dispersal is limited by fencing orsurrounding farmland increase more rapidly. In 1994, num-bats were upgraded from an Endangered listing to Vulnera-ble under IUCN Red List criteria.

Significance to humansNumbat is an aboriginal name from South Australia. Cen-

tral Australian aboriginal peoples knew the animal as


Family: NumbatVol. 12: Mammals I

A numbat (Myrmecobius fasciatus) searches for termites. (Photo by Frans Lanting/Minden Pictures. Reproduced by permission.)

“walpurti” and hunted it to eat. Individuals were tracked toburrows where they were dug up. No commercial exploita-


Vol. 12: Mammals IFamily: Numbat

Two juvenile numbats (Myrmecobius fasciatus) in Western Australia.(Photo by Animals Animals ©A. Wells, OSF. Reproduced by permis-sion.)

Numbats (Myrmecobius fasciatus) use scent and a long sticky tongue tolocate their prey. The tongue can extend as far as 4 in (10 cm) from itsmouth. (Photo by Bill Bachman/Photo Researchers, Inc. Reproduced bypermission.)



Friend, J. A. “Myrmecobiidae.” In Fauna of Australia.Canberra: Australian Government Publishing Service, 1989.

Friend, J. A., and N. D. Thomas. “Conservation of theNumbat (Myrmecobius fasciatus).” In Predators with Pouches:The Biology of Carnivorous Marsupials, edited by M. E. Jones,

C. R. Dickman, and M. Archer. Melbourne: CSIROPublishing, 2003.

Krajewski, C., and M. Westerman. “Molecular Systematics ofDasyuromorphia.” In Predators with Pouches: The Biology ofCarnivorous Marsupials, edited by M. E. Jones, C. R.Dickman, and M. Archer. Melbourne: CSIRO Publishing,2003.

Strahan, R. The Mammals of Australia. Sydney: AustralianMuseum, Reed Books, 1995.

Menna Jones, PhD

tion of numbats is recorded, but up to 200 have been col-lected for museum specimens.

Evolution and systematicsAt least 14 species of Tasmanian wolves from six genera

are known from the fossil record, including Thylacinus, thelast species (T. cynocephalus), which persisted until historicaltimes. Thylacinids originated in the late Oligocene, reachedtheir greatest diversity, with coexisting species, in theMiocene, and then declined steadily with only two species,including the giant T. potens, living in the Pleistocene. Thylacinids ranged in size from small carnivores (4.4–11 lb;2–5 kg) to slightly larger than the thylacine (66 lb; 30 kg).Thylacinids are morphologically conservative among theDasyuromorphia, including T. cynocephalus, which were littlederived from the late Oligocene thylacinids, and are mostclosely related to the dasyurids, although they are conver-gent with the extinct South American marsupial borhyaenids.

The taxonomy for this species is Thylacinus cynocephalus(Harris, 1808), Tasmania, Australia.

Physical characteristicsTasmanian wolves are superficially dog-shaped. They

walk on four legs, although the legs are shorter than mostcanids. The head is doglike with a long, narrow snout,medium-sized (3 in; 80 mm) erect ears, and a strong jaw.The hindquarters slope and taper to a long, semi-rigid tail.The footpads extend to the heel and wrist joints. The re-

cently extinct T. cynocephalus was sexually size dimorphic: fe-males approximately 33 lb (15 kg), males up to 66 lb (30 kg).Body hair is short (to 0.6 in; 15 mm) and sandy brown incolor, with 15–20 brown stripes across the back, extendingfrom behind the shoulders to the base of the tail. The fe-


▲

Tasmanian wolves(Thylacinidae)

Class Mammalia

Order Dasyuromorphia

Family Thylacinidae

Thumbnail descriptionMedium-to-large carnivore, characterized by along, narrow snout, sloping hindquarters thattaper to a long, semi-rigid tail, with broad backstripes from shoulders to tail base

Size4.9–6.4 ft (1.5–2 m); 33–77 lb (15–35 kg)


HabitatForest and woodlands

Conservation statusExtinct

DistributionIsland of Tasmania, Australia; subfossil on Australian continent

Tasmanian wolf (Thylacinus cynocephalus). (Illustration by WendyBaker)


Vol. 12: Mammals IFamily: Tasmanian wolves

Tasmanian wolves had a large gape. (Illustration by Wendy Baker)

The pouch of the Tasmanian wolf faced backwards. When the pouchyoung were large, the pouch bulged downward from the animal. (Il-lustration by Wendy Baker)

male pouch opens slightly posteriorly and contains fourteats. Males also have a small pouch-like depression aroundthe scrotum. There are four upper and three lower incisorteeth, one set of canines, and three sets of premolars. Eachof the four molars is similar in form, with major slicing (car-nassial) and minor grinding surfaces.

DistributionRecords from diaries and bounty payments in the nine-

teenth century indicate a historic range that incorporated theentire island of Tasmania, although the wolves were veryscarce in the southwest and western regions, except on thecoastal strip. This distribution is similar to the current rangeof the Tasmanian devil (Sarcophilus laniarius) and correlateswith mean annual rainfall and associated vegetation. The thy-lacine reached its highest population densities in the low-to-moderate rainfall zones of the north, center, and east of thestate, and thylacines occurred at all altitudes. Thylacines havebeen extinct on the Australian continent for not less than2,000 years; subfossil and prehistoric distribution was broad.There are fossil records from New Guinea.

HabitatHistoric reports indicate a broad range of reasonably open

habitats: grassy woodlands, coastal and alpine scrub, and openforests. Thylacines seem to have avoided the dense, wet rain-forest of western and southwestern Tasmania. Their habitatpreferences completely overlap with those of the devil and areconsistent with the distribution of dense populations of prey.Tasmanian wolves are reported to have used dense vegetationand rocky outcrops during the day (probably for dens), hunt-

ing in adjacent open grassy woodlands and forests at night.The number of subfossil remains found in caves in Tasmaniaattest to the use of larger caves as lairs.

BehaviorSightings of thylacines were usually of solitary animals. Oc-

casional sightings of adult-sized animals together cannot beconstrued as evidence of pair-bonding, and there is no evidenceto support territorial defense of home ranges. Tasmanianwolves were mostly nocturnal but were occasionally observedactive during the day. Vocalizations included a coughing barkand a sigh emitted while hunting, and a warning hiss, a lowgrowl, and an undulating screech that were thought to be an-tagonistic. These vocalizations are not dissimilar in structureto the vocal repertoire of the Tasmanian devil.

Feeding ecology and dietUnfortunately, early research interest in the thylacine con-

cerned classical anatomy and the species became extinct with-out any serious study of its ecology. What is known of diet,hunting, and killing behaviors has been gleaned from histori-cal anecdotes or reconstructed from comparison of skeletal re-mains with its living relatives. Thylacines are reported to havetaken a wide variety of prey, including wombats, macropods,possums, bandicoots, small mammals, and birds, suggestingthey were generalist predators of prey between less than 2.2lb (1 kg) and probably not much more than 66 lb (30 kg). Tas-manian wolves had a long, thin snout relative to all other mam-malian carnivores, marsupial or placental, most like that of afox. This translates to a relatively weak bite force at the ca-nine teeth. Museum-collection skulls also have very low rates

with pouch young were trapped and kept in zoos. Breedingappears to have been timed, as with other dasyurid carnivores,so that young became independent in spring when food sup-ply is maximal. Gestation was probably less than one month,pouch life thought to be around four months. Neither the pe-riod of maternal care, post-pouch-vacation, nor the matingsystem is known.

Conservation statusThylacines are classified by IUCN criteria as Extinct.

The story of the decline and extinction of the thylacine is asad tale of a deliberate strategy of persecution and a conve-nient scapegoat. Eighteenth-century settlers, experiencingsignifiant sheep losses, employed “tiger men” to destroyTasmanian wolves on their properties and successfully lob-bied the government to instigate a bounty. While there isno doubt that thylacines killed sheep, it is thought thatpoaching and feral dogs were responsible for the majorityof missing and dead sheep. The intense pressure placed onpopulations (2,184 bounty payments in 22 years as well asunrecorded deaths) of this probably never-abundant toppredator would have driven thylacines to very low densities.Thylacines suddenly became very scarce in the first decade


Family: Tasmanian wolvesVol. 12: Mammals I

The Tasmanian wolf (Thylacinus cynocephalus) is believed to be extinct. This is one of very few known photos of the species alive and free-living. The date of the photo is unknown. (Photo by Photo Researchers, Inc. Reproduced by permission.)

of breakage of the canines. Combined with the dietary records,and in contrast to prey sizes taken by devils and the largerquolls (up to three times their body weight), this combinationof features suggests that thylacines did not routinely kill veryheavy-bodied prey or prey much larger than themselves (33–66lb; 15–30 kg). While they are recorded killing kangaroos, it isunlikely that they regularly killed healthy large males (up to155 lb; 70 kg) or the larger megafauna such as diprotodonts.A similar ovoid cross-sectional shape of the canine teeth to theliving larger dasyurid carnivores suggests that thylacines prob-ably killed their prey using a generalized crushing bite used inkilling. Tasmanian wolves were probably not swift runners,which is indicated by comparison of their leg bone ratios withother marsupial and placental carnivores. Unlikely to be ca-pable of sustained, fast pursuit, thylacines probably hunted us-ing a combination of stealth, short pursuit, and ambush.Putting all of these pieces of information together, it is likelythat the thylacine filled a niche more similar to a medium-sized canid such as a coyote than to a wolf.

Reproductive biologyLittle is known of reproduction in the Tasmanian wolves

and they were bred only once in captivity, although females

of the twentieth century, with bounty payments falling from100 to 150 per year to none between 1905 and 1910, andpopulations never recovered. The bounty scheme wasscrapped in 1912 and the species given official protection onJuly 14, 1936. The last confirmed living animal died in theHobart Zoo on September 7, 1936, and the last confirmedkilling of a wild Tasmanian wolf was in 1930. There havebeen and continue to be sightings that appear credible butno thylacine has turned up.

Significance to humansTasmanian wolves were deliberately killed and eaten by

aboriginal peoples both on the Australian mainland and inTasmania. Mainland aboriginal rock art depicts speared thy-lacines as well as females feeding young. Practices varied fromtribe to tribe. George Augustus Robinson, an early colonist,recorded consumption of thylacines by some tribes, but oth-ers seemed to revere the species, building shelters to coverthe body after skinning it and keeping the skull.


Vol. 12: Mammals IFamily: Tasmanian wolves



Dixon, J. M. “Thylacinidae.” In Fauna of Australia, edited byD. W. Walton, and B. J. Richardson. Canberra: AustralianGovernment Publishing Service, 1989.

Guiler, E., and P. Godard. Tasmanian Tiger, A Lesson to beLearnt. Perth, Western Australia: Abrolhos Publishing,1998.

Guiler, E. R. Thylacine: The Tragedy of the Tasmanian Tiger.Melbourne: Oxford University Press, 1985.

Jones, M. E. “Predators, Pouches and Partitioning:Ecomorphology and Guild Structure of Marsupial andPlacental Carnivores.” In Predators with Pouches: The Biologyof Carnivorous Marsupials, edited by M. E. Jones, C. R.Dickman, and M. Archer. Melbourne: CSIRO Books, 2003.

Krajewski, C., and M. Westerman. “Molecular Systematics ofDasyuromorphia.” In Predators with Pouches: The Biology ofCarnivorous Marsupials, edited by M. E. Jones, C. R.

Dickman, and M. Archer. Melbourne: CSIRO Publishing,2003.

Paddle, R. The Last Tasmanian Tiger. The History and Extinctionof the Thylacine. Cambridge: Cambridge University Press,2000.

Strahan, R. The Mammals of Australia. Sydney: AustralianMuseum Reed Books, 1995.

Wroe, S. “Australian Marsupial Carnivores: An Overview ofRecent Advances in Palaeontology.” In Predators withPouches: The Biology of Carnivorous Marsupials, edited by M.E. Jones, C. R. Dickman, and M. Archer. Melbourne:CSIRO Publishing, 2003.

PeriodicalsJones, M. E., and D. M. Stoddart. “Reconstruction of the

Predatory Behaviour of the Extinct Marsupial Thylacine.”Journal of Zoology 246 (1998): 239–246.

OtherThe Thylacine Museum. <http://naturalworlds.org/thylacine/>.

Menna Jones, PhD

The Tasmanian wolf (Thylacinus cynocephalus) lived in open forestsand grasslands of Australia. Shown here is a model. (Photo by Cre-ation Jacana/Photo Researchers, Inc. Reproduced by permission.)

Alcock, J. Animal Behavior. New York: Sinauer, 2001.

Alderton, D. Rodents of the World. New York: Facts on File,1996.

Alterman, L., G. A. Doyle, and M. K. Izard, eds. Creatures ofthe Dark: The Nocturnal Prosimians. New York: PlenumPress, 1995.

Altringham, J. D. Bats: Biology and Behaviour. New York:Oxford University Press, 2001.

Anderson, D. F., and S. Eberhardt. Understanding Flight. NewYork: McGraw-Hill, 2001.

Anderson, S., and J. K. Jones Jr., eds. Orders and Families ofRecent Mammals of the World. John Wiley & Sons, NewYork, 1984.

Apps, P. Smithers’ Mammals of Southern Africa. Cape Town:Struik Publishers, 2000.

Attenborough, D. The Life of Mammals. London: BBC, 2002.

Au, W. W. L. The Sonar of Dolphins. New York: Springer-Verlag, 1993.

Austin, C. R., and R. V. Short, eds. Reproduction in Mammals. 4vols. Cambridge: Cambridge University Press, 1972.

Avise, J. C. Molecular Markers, Natural History and Evolution.London: Chapman & Hall, 1994.

Barber, P. Vampires, Burial, and Death: Folklore and Reality.New Haven: Yale University Press, 1998.

Barnett, S. A. The Story of Rats. Crows Nest, Australia: Allen &Unwin, 2001.

Baskin, L., and K. Danell. Ecology of Ungulates. A Handbook ofSpecies in Eastern Europe, Northern and Central Asia.Heidelberg: Springer-Verlag, 2003.

Bates, P. J. J., and D. L. Harrison. Bats of the IndianSubcontinent. Sevenoaks, U. K.: Harrison ZoologicalMuseum, 1997.

Bekoff, M., C. Allen, and G. M. Burghardt, eds. The CognitiveAnimal. Cambridge: MIT Press, 2002.

Bennett, N. C., and C. G. Faulkes. African Mole-rats: Ecologyand Eusociality. Cambridge: Cambridge University Press,2000.

Benton, M. J. The Rise of the Mammals. New York: CrescentBooks, 1991.

Berta, A., and L. Sumich. Marine Mammals: EvolutionaryBiology. San Diego: Academic Press, 1999.

Bonaccorso, F. J. Bats of Papua New Guinea. Washington, DC:Conservation International, 1998.

Bonnichsen, R, and K. L. Turnmire, eds. Ice Age People of NorthAmerica. Corvallis: Oregon State University Press. 1999.

Bright, P. and P. Morris. Dormice London: The MammalSociety, 1992.

Broome, D., ed. Coping with Challenge. Berlin: DahlemUniversity Press, 2001.

Buchmann, S. L., and G. P. Nabhan. The Forgotten Pollinators.Washington, DC: Island Press, 1997.

Burnie, D., and D. E. Wilson, eds. Animal. Washington, DC:Smithsonian Institution, 2001.

Caro, T., ed. Behavioral Ecology and Conservation Biology.Oxford: Oxford University Press, 1998.

Carroll, R. L. Vertebrate Paleontology and Evolution. New York:W. H. Freeman and Co., 1998.

Cavalli-Sforza, L. L., P. Menozzi, and A. Piazza. The Historyand Geography of Human Genes. Princeton: PrincetonUniversity Press, 1994.

Chivers, R. E., and P. Lange. The Digestive System in Mammals:Food, Form and Function. New York: Cambridge UniversityPress, 1994.

Clutton-Brock, J. A Natural History of Domesticated Mammals.2nd ed. Cambridge: Cambridge University Press, 1999.

Conley, V. A. The War Against the Beavers. Minneapolis:University of Minnesota Press, 2003.

Cowlishaw, G., and R. Dunbar. Primate Conservation Biology.Chicago: University of Chicago Press, 2000.


• • • • •

For further reading

Craighead, L. Bears of the World Blaine, WA: Voyager Press,2000.

Crichton., E. G. and P. H. Krutzsch, eds. Reproductive Biologyof Bats. New York: Academic Press, 2000.

Croft, D. B., and U. Gansloßer, eds. Comparison of Marsupialand Placental Behavior. Fürth, Germany: Filander, 1996.

Darwin, C. The Autobiography of Charles Darwin 1809–1882with original omissions restored. Edited by Nora Barlow.London: Collins, 1958.

Darwin, C. On The Origin of Species by Means of NaturalSelection, or The Preservation of Favoured Races in the Strugglefor Life. London: John Murray, 1859.

Darwin, C. The Zoology of the Voyage of HMS Beagle under theCommand of Captain Robert FitzRoy RN During the Years1832-1836. London: Elder & Co., 1840.

Dawson, T. J. Kangaroos: The Biology of the Largest Marsupials.Kensington, Australia: University of New South WalesPress/Ithaca, 2002.

Duncan, P. Horses and Grasses. New York: Springer-VerlagInc., 1991.

Easteal, S., C. Collett, and D. Betty. The Mammalian MolecularClock. Austin, TX: R. G. Landes, 1995.

Eisenberg, J. F. Mammals of the Neotropics. Vol. 1, The NorthernNeotropics. Chicago: University of Chicago Press, 1989.

Eisenberg, J. F., and K. H. Redford. Mammals of the Neotropics.Vol. 3, The Central Neotropics. Chicago: University ofChicago Press, 1999.

Ellis, R. Aquagenesis. New York: Viking, 2001.

Estes, R. D. The Behavior Guide to African Mammals. Berkeley:The University of California Press, 1991.

Estes, R. D. The Safari Companion: A Guide to WatchingAfrican Mammals. White River Junction, VT: ChelseaGreen, 1999.

Evans, P. G. H., and J. A. Raga, eds. Marine Mammals: Biologyand Conservation. New York: Kluwer Academic/Plenum,2001.

Ewer, R. F. The Carnivores. Ithaca, NY: Comstock Publishing,1998.

Feldhamer, G. A., L. C. Drickamer, A. H. Vessey, and J. F.Merritt. Mammalogy. Adaptations, Diversity, and Ecology.Boston: McGraw Hill, 1999.

Fenton, M. B. Bats. Rev. ed. New York: Facts On File Inc.,2001.

Findley, J. S. Bats: A Community Perspective. Cambridge:Cambridge University Press, 1993.

Flannery, T. F. Mammals of New Guinea. Ithaca: CornellUniversity Press, 1995.

Flannery, T. F. Possums of the World: A Monograph of thePhalangeroidea. Sydney: GEO Productions, 1994.

Fleagle, J. G. Primate Adaptation and Evolution. New York:Academic Press, 1999.

Frisancho, A. R. Human Adaptation and Accommodation. AnnArbor: University of Michigan Press, 1993.

Garbutt, N. Mammals of Madagascar. New Haven: YaleUniversity Press, 1999.

Geist, V. Deer of the World: Their Evolution, Behavior, andEcology. Mechanicsburg, PA: Stackpole Books, 1998.

Geist, V. Life Strategies, Human Evolution, EnvironmentalDesign. New York: Springer Verlag, 1978.

Gillespie, J. H. The Causes of Molecular Evolution. Oxford:Oxford University Press, 1992.

Gittleman, J. L., ed. Carnivore Behavior, Ecology and Evolution. 2vols. Chicago: University of Chicago Press, 1996.

Gittleman, J. L., S. M. Funk, D. Macdonald, and R. K.Wayne, eds. Carnivore Conservation. Cambridge: CambridgeUniversity Press, 2001.

Givnish, T. I. and K. Sytsma. Molecular Evolution and AdaptiveRadiations. Cambridge: Cambridge University Press, 1997.

Goldingay, R. L., and J. H. Scheibe, eds. Biology of GlidingMammals. Fürth, Germany: Filander Verlag, 2000.

Goodman, S. M., and J. P. Benstead, eds. The Natural Historyof Madagascar. Chicago: The University of Chicago Press,2003.

Gosling, L. M., and W. J. Sutherland, eds. Behaviour andConservation. Cambridge: Cambridge University Press, 2000.

Gould, E., and G. McKay, eds. Encyclopedia of Mammals. 2nded. San Diego: Academic Press, 1998.

Groves, C. P. Primate Taxonomy. Washington, DC:Smithsonian Institute, 2001.

Guthrie, D. R. Frozen Fauna of the Mammoth Steppe. Chicago:University of Chicago Press. 1990.

Hall, L., and G. Richards. Flying Foxes: Fruit and Blossom Batsof Australia. Malabar, FL: Krieger Publishing Company,2000.

Hancocks, D. A Different Nature. The Paradoxical World of Zoosand Their Uncertain Future. Berkeley: University ofCalifornia Press, 2001.

Hartwig, W. C., ed. The Primate Fossil Record. New York:Cambridge University Press, 2002.

Hildebrand, M. Analysis of Vertebrate Structure. 4th ed. NewYork: John Wiley & Sons, 1994.

Hillis, D. M., and C. Moritz. Molecular Systematics. Sunderland,MA: Sinauer Associates, 1990.


For further reading

Hoelzel, A. R., ed. Marine Mammal Biology: An EvolutionaryApproach. Oxford: Blackwell Science, 2002.

Hunter, M. L., and A Sulzer. Fundamentals of ConservationBiology. Oxford, U. K.: Blackwell Science, Inc., 2001.

Jefferson, T. A., S. Leatherwood, and M. A. Webber, eds.Marine Mammals of the World. Heidelberg: Springer-Verlag,1993.

Jensen, P., ed. The Ethology of Domestic Animals: An IntroductoryText. Oxon, MD: CABI Publishing, 2002.

Jones, M. E., C. R. Dickman, and M. Archer. Predators withPouches: The Biology of Carnivorous Marsupials. Melbourne:CSIRO Books, 2003.

Kardong, K. V. Vertebrates: Comparative Anatomy, Function,Evolution. Dubuque, IA: William C. Brown Publishers,1995.

King, C. M. The Handbook of New Zealand Mammals. Auckland:Oxford University Press, 1990.

Kingdon, J. The Kingdon Field Guide to African Mammals.London: Academic Press, 1997.

Kingdon, J., D. Happold, and T. Butynski, eds. The Mammalsof Africa: A Comprehensive Synthesis. London: AcademicPress, 2003.

Kinzey, W. G., ed. New World Primates: Ecology, Evolution, andBehavior. New York: Aldine de Gruyter, 1997.

Kosco, M. Mammalian Reproduction. Eglin, PA: AlleghenyPress, 2000.

Krebs, J. R., and N. B. Davies. An Introduction to BehaviouralEcology. 3rd ed. Oxford: Blackwell Scientific Publications,1993.

Kunz, T. H., and M. B. Fenton, eds. Bat Ecology. Chicago:University of Chicago Press, 2003.

Lacey, E. A., J. L. Patton, and G. N. Cameron, eds. LifeUnderground: The Biology of Subterranean Rodents. Chicago:University of Chicago Press, 2000.

Lott, D. F. American Bison: A Natural History. Berkeley:University of California Press, 2002.

Macdonald, D. W. European Mammals: Evolution and Behavior.London: Collins, 1995.

Macdonald, D. W. The New Encyclopedia of Mammals. Oxford:Oxford University Press, 2001.

Macdonald, D. W. The Velvet Claw: A Natural History of theCarnivores. London: BBC Books, 1992.

Macdonald, D. W., and P. Barrett. Mammals of Britain andEurope. London: Collins, 1993.

Martin, R. E. A Manual of Mammalogy: With Keys to Families ofthe World. 3rd ed. Boston: McGraw-Hill, 2001.

Matsuzawa, T., ed. Primate Origins of Human Cognition andBehavior. Tokyo: Springer-Verlag, 2001.

Mayr, E. What Evolution Is. New York: Basic Books, 2001.

McCracken, G. F., A. Zubaid, and T. H. Kunz, eds. Functionaland Evolutionary Ecology of Bats. Oxford: Oxford UniversityPress, 2003.

McGrew, W. C., L. F. Marchant, and T. Nishida, eds. GreatApe Societies. Cambridge: Cambridge University Press,1996.

Meffe, G. K., and C. R. Carroll. Principles of ConservationBiology. Sunderland, MA: Sinauer Associates, Inc., 1997.

Menkhorst, P. W. A Field Guide to the Mammals of Australia.Melbourne: Oxford University Press, 2001.

Mills, G., and M. Harvey. African Predators. Cape Town:Struik Publishers, 2001.

Mills, G., and L. Hes. Complete Book of Southern AfricanMammals. Cape Town: Struik, 1997.

Mitchell-Jones, A. J., et al. The Atlas of European Mammals.London: Poyser Natural History/Academic Press, 1999.

Neuweiler, G. Biology of Bats. Oxford: Oxford University Press,2000.

Norton, B. G., et al. Ethics on the Ark. Washington, DC:Smithsonian Institution Press, 1995.

Nowak, R. M. Walker’s Bats of the World. Baltimore: The JohnsHopkins University Press, 1994.

Nowak, R. M. Walker’s Mammals of the World. 6th ed.Baltimore: Johns Hopkins University Press, 1999.

Nowak, R. M. Walker’s Primates of the World. Baltimore: TheJohns Hopkins University Press, 1999.

Payne, K. Silent Thunder: The Hidden Voice of Elephants.Phoenix: Wiedenfeld and Nicholson, 1999.

Pearce, J. D. Animal Learning and Cognition. New York:Lawrence Erlbaum, 1997.

Pereira, M. E., and L. A. Fairbanks, eds. Juvenile Primates: LifeHistory, Development, and Behavior. New York: OxfordUniversity Press, 1993.

Perrin, W. F., B. Würsig, and J. G. M. Thewissen. Encyclopediaof Marine Mammals. San Diego: Academic Press, 2002.

Popper, A. N., and R. R. Fay, eds. Hearing by Bats. New York:Springer-Verlag, 1995.

Pough, F. H., C. M. Janis, and J. B. Heiser. Vertebrate Life. 6thed. Upper Saddle River, NJ: Prentice Hall, 2002.

Premack, D., and A. J. Premack. Original Intelligence: TheArchitecture of the Human Mind. New York: McGraw-Hill/Contemporary Books, 2002.


For further readingFO

RFU

RTH

ER

REA

DIN

G

Price, E. O. Animal Domestication and Behavior. Cambridge,MA: CAB International, 2002.

Racey, P. A., and S. M. Swift, eds. Ecology, Evolution andBehaviour of Bats. Oxford: Clarendon Press, 1995.

Redford, K. H., and J. F. Eisenberg. Mammals of the Neotropics.Vol. 2, The Southern Cone. Chicago: University of ChicagoPress, 1992.

Reeve, N. Hedgehogs. London: Poyser Natural History, 1994.

Reeves, R., B. Stewart, P. Clapham, and J. Powell. SeaMammals of the World. London: A&C Black, 2002.

Reynolds, J. E. III, and D. K. Odell. Manatees and Dugongs.New York: Facts On File, 1991.

Reynolds, J. E. III, and S. A. Rommel, eds. Biology of MarineMammals. Washington, DC: Smithsonian Institution Press,1999.

Rice, D. W. Marine Mammals of the World. Lawrence, KS:Allen Press, 1998.

Ridgway, S. H., and R. Harrison, eds. Handbook of MarineMammals. 6 vols. New York: Academic Press, 1985-1999.

Riedman, M. The Pinnipeds. Berkeley: University of CaliforniaPress, 1990.

Rijksen, H., and E. Meijaard. Our Vanishing Relative: The Statusof Wild Orang-utans at the Close of the Twentieth Century.Dordrecht: Kluwer Academic Publishers, 1999.

Robbins, C. T. Wildlife Feeding and Nutrition. San Diego:Academic Press, 1992.

Robbins, M. M., P. Sicotte, and K. J. Stewart, eds. MountainGorillas: Three Decades of Research at Karisoke. Cambridge:Cambridge University Press, 2001.

Roberts, W. A. Principles of Animal Cognition. New York:McGraw-Hill, 1998.

Schaller, G. B. Wildlife of the Tibetan Steppe. Chicago:University of Chicago Press, 1998.

Seebeck, J. H., P. R. Brown, R. L. Wallis, and C. M. Kemper,eds. Bandicoots and Bilbies. Chipping Norton, Australia:Surrey Beatty & Sons, 1990.

Shepherdson, D. J., J. D. Mellen, and M. Hutchins. SecondNature: Environmental Enrichment for Captive Animals.Washington, DC: Smithsonian Institution Press, 1998.

Sherman, P. W., J. U. M. Jarvis, and R. D. Alexander, eds. TheBiology of the Naked Mole-rat. Princeton: PrincetonUniversity Press, 1991.

Shettleworth, S. J. Cognition, Evolution, and Behavior. Oxford:Oxford University Press, 1998.

Shoshani, J., ed. Elephants. London: Simon & Schuster, 1992.

Skinner, R., and R. H. N. Smithers. The Mammals of theSouthern African Subregion. 2nd ed. Pretoria, South Africa:University of Pretoria, 1998.

Sowls, L. K. The Peccaries. College Station: Texas A&M Press,1997.

Steele, M. A. and J. Koprowski. North American Tree Squirrels.Washington, DC: Smithsonian Institution Press, 2001.

Sunquist, M. and F. Sunquist. Wild Cats of the World Chicago:University of Chicago Press, 2002.

Sussman, R. W. Primate Ecology and Social Structure. 3 vols.Needham Heights, MA: Pearson Custom Publishing, 1999.

Szalay, F. S., M. J. Novacek, and M. C. McKenna, eds.Mammalian Phylogeny. New York: Springer-Verlag, 1992.

Thomas, J. A., C. A. Moss, and M. A. Vater, eds. Echolocationin Bats and Dolphins. Chicago: University of Chicago Press,2003.

Thompson, H. V., and C. M. King, eds. The European Rabbit:The History and Biology of a Successful Colonizer. Oxford:Oxford University Press, 1994.

Tomasello, M., and J. Calli. Primate Cognition. Chicago:University of Chicago Press, 1997.

Twiss, J. R. Jr., and R. R. Reeves, eds. Conservation andManagement of Marine Mammals. Washington, DC:Smithsonian Institution Press, 1999.

Van Soest, P. J. Nutritional Ecology of the Ruminant. 2nd ed.Ithaca, NY: Cornell University Press, 1994.

Vaughan, T., J. Ryan, and N. Czaplewski. Mammalogy. 4th ed.Philadelphia: Saunders College Publishing, 1999.

Vrba, E. S., G. H. Denton, T. C. Partridge, and L. H.Burckle, eds. Paleoclimate and Evolution, with Emphasis onHuman Origins. New Haven: Yale University Press, 1995.

Vrba, E. S., and G. G. Schaller, eds. Antelopes, Deer andRelatives: Fossil Record, Behavioral Ecology, Systematics andConservation. New Haven: Yale University Press, 2000.

Wallis, Janice, ed. Primate Conservation: The Role of ZoologicalParks. New York: American Society of Primatologists,1997.

Weibel, E. R., C. R. Taylor, and L. Bolis. Principles of AnimalDesign. New York: Cambridge University Press, 1998.

Wells, R. T., and P. A. Pridmore. Wombats. Sydney: SurreyBeatty & Sons, 1998.

Whitehead, G. K. The Whitehead Encyclopedia of Deer.Stillwater, MN: Voyager Press, 1993.

Wilson, D. E., and D. M. Reeder, eds. Mammal Species of theWorld: a Taxonomic and Geographic Reference. 2nd ed.Washington, DC: Smithsonian Institution Press, 1993.


For further reading

Wilson, D. E., and S. Ruff, eds. The Smithsonian Book of NorthAmerican Mammals. Washington, DC: SmithsonianInstitution Press, 1999.

Wilson, E. O. The Diversity of Life. Cambridge: HarvardUniversity Press, 1992.

Wójcik, J. M., and M. Wolsan, eds. Evolution of Shrews.Bialowieza, Poland: Mammal Research Institute, PolishAcademy of Sciences, 1998.

Woodford, J. The Secret Life of Wombats. Melbourne: TextPublishing, 2001.

Wrangham, R. W., W. C. McGrew, F. B. M. de Waal, and P.G. Heltne, eds. Chimpanzee Cultures. Cambridge: HarvardUniversity Press, 1994.

Wynne, C. D. L. Animal Cognition. Basingstoke, U. K.:Palgrave, 2001.


For further readingFO

RFU

RTH

ER

REA

DIN

G

African Wildlife Foundation1400 16th Street, NW, Suite 120Washington, DC 20036 USAPhone: (202) 939-3333Fax: (202) 939-3332E-mail: [email protected]<http://www.awf.org/>

The American Society of Mammalogists<http://www.mammalsociety.org/>

American Zoo and Aquarium Association8403 Colesville Road, Suite 710Silver Spring, MD 20910 USA.Phone: (301) 562-0777Fax: (301) 562-0888<http://www.aza.org/>

Australian Conservation Foundation Inc.340 Gore StreetFitzroy, Victoria 3065 AustraliaPhone: (3) 9416 1166<http://www.acfonline.org.au>

The Australian Mammal Society<http://www.australianmammals.org.au/>

Australian Regional Association of Zoological Parks andAquaria

PO Box 20Mosman, NSW 2088AustraliaPhone: 61 (2) 9978-4797Fax: 61 (2) 9978-4761<http://www.arazpa.org>

Bat Conservation InternationalP.O. Box 162603Austin, TX 78716 USAPhone: (512) 327-9721Fax: (512) 327-9724<http://www.batcon.org/>

Center for Ecosystem Survival699 Mississippi Street, Suite 106San Francisco, 94107 USAPhone: (415) 648-3392Fax: (415) 648-3392

E-mail: [email protected]<http://www.savenature.org/>

Conservation International1919 M Street NW, Ste. 600Washington, DC 20036Phone: (202) 912-1000<http://www.conservation.org>

The European Association for Aquatic MammalsE-mail: [email protected]<http://www.eaam.org/>

European Association of Zoos and AquariaPO Box 201641000 HD AmsterdamThe Netherlands<http://www.eaza.net>

IUCN-The World Conservation UnionRue Mauverney 28Gland 1196 SwitzerlandPhone: ++41(22) 999-0000Fax: ++41(22) 999-0002E-mail: [email protected]<http://www.iucn.org/>

The Mammal Society2B, Inworth StreetLondon SW11 3EP United KingdomPhone: 020 7350 2200Fax: 020 7350 2211<http://www.abdn.ac.uk/mammal/>

Mammals Trust UK15 Cloisters House8 Battersea Park RoadLondon SW8 4BG United KingdomPhone: (+44) 020 7498 5262Fax: (+44) 020 7498 4459E-mail: [email protected]<http://www.mtuk.org/>

The Marine Mammal CenterMarin Headlands1065 Fort CronkhiteSausalito, CA 94965 USAPhone: (415) 289-7325


• • • • •

Organizations

Fax: (415) 289-7333<http://www.marinemammalcenter.org/>

National Marine Mammal Laboratory7600 Sand Point Way N.E. F/AKC3Seattle, WA 98115-6349 USAPhone: (206) 526-4045Fax: (206) 526-6615<http://nmml.afsc.noaa.gov/>

National Wildlife Federation11100 Wildlife Center DriveReston, VA 20190-5362 USAPhone: (703) 438-6000<http://www.nwf.org/>

The Organization for Bat Conservation39221 Woodward AvenueBloomfield Hills, MI 48303 USAPhone: (248) 645-3232E-mail: [email protected]<http://www.batconservation.org/>

Scripps Institution of OceanographyUniversity of California-San Diego9500 Gilman DriveLa Jolla, CA 92093 USA<http://sio.ucsd.edu/gt;

Seal Conservation Society7 Millin Bay RoadTara, PortaferryCounty Down BT22 1QDUnited Kingdom

Phone: +44-(0)28-4272-8600Fax: +44-(0)28-4272-8600E-mail: [email protected]<http://www.pinnipeds.org>

The Society for Marine Mammalogy<http://www.marinemammalogy.org/>

The Wildlife Conservation Society2300 Southern BoulevardBronx, New York 10460Phone: (718) 220-5100

Woods Hole Oceanographic InstitutionInformation OfficeCo-op Building, MS #16Woods Hole, MA 02543 USAPhone: (508) 548-1400Fax: (508) 457-2034E-mail: [email protected]<http://www.whoi.edu/>

World Association of Zoos and AquariumsPO Box 23Liebefeld-Bern CH-3097Switzerland<http://www.waza.org>

World Wildlife Fund1250 24th Street N.W.Washington, DC 20037-1193 USAPhone: (202) 293-4800Fax: (202) 293-9211<http://www.panda.org/>


OrganizationsO

RG

AN

IZA

TION

S

Dr. Michael AbsCurator, Ruhr UniversityBochum, Germany

Dr. Salim AliBombay Natural History SocietyBombay, India

Dr. Rudolph AltevogtProfessor, Zoological Institute,University of MünsterMünster, Germany

Dr. Renate AngermannCurator, Institute of Zoology,Humboldt UniversityBerlin, Germany

Edward A. ArmstrongCambridge UniversityCambridge, England

Dr. Peter AxProfessor, Second Zoological Instituteand Museum, University of GöttingenGöttingen, Germany

Dr. Franz BachmaierZoological Collection of the State ofBavariaMunich, Germany

Dr. Pedru BanarescuAcademy of the Roumanian SocialistRepublic, Trajan Savulescu Institute ofBiologyBucharest, Romania

Dr. A. G. BannikowProfessor, Institute of VeterinaryMedicineMoscow, Russia

Dr. Hilde BaumgärtnerZoological Collection of the State ofBavariaMunich, Germany

C. W. BensonDepartment of Zoology, CambridgeUniversityCambridge, England

Dr. Andrew BergerChairman, Department of Zoology,University of HawaiiHonolulu, Hawaii, U.S.A.

Dr. J. BerliozNational Museum of Natural HistoryParis, France

Dr. Rudolf BerndtDirector, Institute for PopulationEcology, Hiligoland OrnithologicalStationBraunschweig, Germany

Dieter Blume Instructor of Biology, Freiherr-vom-Stein SchoolGladenbach, Germany

Dr. Maximilian BoeckerZoological Research Institute and A.Koenig MuseumBonn, Germany

Dr. Carl-Heinz BrandesCurator and Director, The Aquarium,Overseas MuseumBremen, Germany

Dr. Donald G. BroadleyCurator, Umtali MuseumMutare, Zimbabwe

Dr. Heinz BrüllDirector; Game, Forest, and FieldsResearch StationHartenholm, Germany

Dr. Herbert BrunsDirector, Institute of Zoology and theProtection of LifeSchlangenbad, Germany

Hans BubHeligoland Ornithological StationWilhelmshaven, Germany

A. H. ChisholmSydney, Australia

Herbert Thomas CondonCurator of Birds, South AustralianMuseumAdelaide, Australia

Dr. Eberhard CurioDirector, Laboratory of Ethology,Ruhr UniversityBochum, Germany

Dr. Serge DaanLaboratory of Animal Physiology,University of AmsterdamAmsterdam, The Netherlands

Dr. Heinrich DatheProfessor and Director, Animal Parkand Zoological Research Station,German Academy of SciencesBerlin, Germany

Dr. Wolfgang DierlZoological Collection of the State ofBavariaMunich, Germany


• • • • •

Contributors to the first editionThe following individuals contributed chapters to the original edition of Grzimek’s Animal Life Encyclopedia, which was edited byDr. Bernhard Grzimek, Professor, Justus Liebig University of Giessen, Germany; Director, Frankfurt Zoological Garden, Germany;

and Trustee, Tanzanian National Parks, Tanzania.

Dr. Fritz DieterlenZoological Research Institute and A.Koenig MuseumBonn, Germany

Dr. Rolf DircksenProfessor, Pedagogical InstituteBielefeld, Germany

Josef DonnerInstructor of BiologyKatzelsdorf, Austria

Dr. Jean DorstProfessor, National Museum ofNatural HistoryParis, France

Dr. Gerti DückerProfessor and Chief Curator,Zoological Institute, University ofMünsterMünster, Germany

Dr. Michael DzwilloZoological Institute and Museum,University of HamburgHamburg, Germany

Dr. Irenäus Eibl-EibesfeldtProfessor and Director, Institute ofHuman Ethology, Max PlanckInstitute for Behavioral PhysiologyPercha/Starnberg, Germany

Dr. Martin EisentrautProfessor and Director, ZoologicalResearch Institute and A. KoenigMuseumBonn, Germany

Dr. Eberhard ErnstSwiss Tropical InstituteBasel, Switzerland

R. D. EtchecoparDirector, National Museum ofNatural HistoryParis, France

Dr. R. A. FallaDirector, Dominion MuseumWellington, New Zealand

Dr. Hubert FechterCurator, Lower Animals, ZoologicalCollection of the State of BavariaMunich, Germany

Dr. Walter FiedlerDocent, University of Vienna, andDirector, Schönbrunn ZooVienna, Austria

Wolfgang FischerInspector of Animals, Animal ParkBerlin, Germany

Dr. C. A. FlemingGeological Survey Department ofScientific and Industrial ResearchLower Hutt, New Zealand

Dr. Hans FrädrichZoological GardenBerlin, Germany

Dr. Hans-Albrecht FreyeProfessor and Director, BiologicalInstitute of the Medical SchoolHalle a.d.S., Germany

Günther E. FreytagFormer Director, Reptile andAmphibian Collection, Museum ofCultural History in MagdeburgBerlin, Germany

Dr. Herbert FriedmannDirector, Los Angeles CountyMuseum of Natural HistoryLos Angeles, California, U.S.A.

Dr. H. FriedrichProfessor, Overseas MuseumBremen, Germany

Dr. Jan FrijlinkZoological Laboratory, University ofAmsterdamAmsterdam, The Netherlands

Dr. H. C. Karl Von FrischProfessor Emeritus and formerDirector, Zoological Institute,University of MunichMunich, Germany

Dr. H. J. FrithC.S.I.R.O. Research InstituteCanberra, Australia

Dr. Ion E. FuhnAcademy of the Roumanian SocialistRepublic, Trajan Savulescu Institute ofBiologyBucharest, Romania

Dr. Carl GansProfessor, Department of Biology,State University of New York atBuffaloBuffalo, New York, U.S.A.

Dr. Rudolf GeigyProfessor and Director, Swiss TropicalInstituteBasel, Switzerland

Dr. Jacques GerySt. Genies, France

Dr. Wolfgang GewaltDirector, Animal ParkDuisburg, Germany

Dr. H. C. Viktor GoerttlerProfessor Emeritus, University of JenaJena, Germany

Dr. Friedrich GoetheDirector, Institute of Ornithology,Heligoland Ornithological StationWilhelmshaven, Germany

Dr. Ulrich F. GruberHerpetological Section, ZoologicalResearch Institute and A. KoenigMuseumBonn, Germany

Dr. H. R. HaefelfingerMuseum of Natural HistoryBasel, Switzerland

Dr. Theodor HaltenorthDirector, Mammalology, ZoologicalCollection of the State of BavariaMunich, Germany

Barbara HarrissonSarawak Museum, Kuching, BorneoIthaca, New York, U.S.A.

Dr. Francois HaverschmidtPresident, High Court (retired)Paramaribo, Suriname

Dr. Heinz HeckDirector, Catskill Game FarmCatskill, New York, U.S.A.

Dr. Lutz HeckProfessor (retired), and Director,Zoological Garden, BerlinWiesbaden, Germany


Contributors to the first editionC

ON

TRIB

UTO

RS

TOTH

EFIR

ST

ED

ITION

Dr. H. C. Heini HedigerDirector, Zoological GardenZurich, Switzerland

Dr. Dietrich HeinemannDirector, Zoological Garden, MünsterDörnigheim, Germany

Dr. Helmut HemmerInstitute for Physiological Zoology,University of MainzMainz, Germany

Dr. W. G. HeptnerProfessor, Zoological Museum,University of MoscowMoscow, Russia

Dr. Konrad HerterProfessor Emeritus and Director(retired), Zoological Institute, FreeUniversity of BerlinBerlin, Germany

Dr. Hans Rudolf HeusserZoological Museum, University ofZurichZurich, Switzerland

Dr. Emil Otto HöhnAssociate Professor of Physiology,University of AlbertaEdmonton, Canada

Dr. W. HohorstProfessor and Director, ParasitologicalInstitute, Farbwerke Hoechst A.G.Frankfurt-Höchst, Germany

Dr. Folkhart HückinghausDirector, Senckenbergische Anatomy,University of Frankfurt a.M.Frankfurt a.M., Germany

Francois HüeNational Museum of Natural HistoryParis, France

Dr. K. ImmelmannProfessor, Zoological Institute,Technical University of BraunschweigBraunschweig, Germany

Dr. Junichiro ItaniKyoto UniversityKyoto, Japan

Dr. Richard F. JohnstonProfessor of Zoology, University ofKansasLawrence, Kansas, U.S.A.

Otto JostOberstudienrat, Freiherr-vom-SteinGymnasiumFulda, Germany

Dr. Paul KähsbauerCurator, Fishes, Museum of NaturalHistoryVienna, Austria

Dr. Ludwig KarbeZoological State Institute andMuseumHamburg, Germany

Dr. N. N. KartaschewDocent, Department of Biology,Lomonossow State UniversityMoscow, Russia

Dr. Werner KästleOberstudienrat, Gisela GymnasiumMunich, Germany

Dr. Reinhard KaufmannField Station of the Tropical Institute,Justus Liebig University, Giessen,GermanySanta Marta, Colombia

Dr. Masao KawaiPrimate Research Institute, KyotoUniversityKyoto, Japan

Dr. Ernst F. KilianProfessor, Giessen University andCatedratico Universidad Australia,Valdivia-ChileGiessen, Germany

Dr. Ragnar KinzelbachInstitute for General Zoology,University of MainzMainz, Germany

Dr. Heinrich KirchnerLandwirtschaftsrat (retired)Bad Oldesloe, Germany

Dr. Rosl KirchshoferZoological Garden, University ofFrankfurt a.M.Frankfurt a.M., Germany

Dr. Wolfgang KlausewitzCurator, Senckenberg NatureMuseum and Research InstituteFrankfurt a.M., Germany

Dr. Konrad KlemmerCurator, Senckenberg NatureMuseum and Research InstituteFrankfurt a.M., Germany

Dr. Erich KlinghammerLaboratory of Ethology, PurdueUniversityLafayette, Indiana, U.S.A.

Dr. Heinz-Georg KlösProfessor and Director, ZoologicalGardenBerlin, Germany

Ursula KlösZoological GardenBerlin, Germany

Dr. Otto KoehlerProfessor Emeritus, ZoologicalInstitute, University of FreiburgFreiburg i. BR., Germany

Dr. Kurt KolarInstitute of Ethology, AustrianAcademy of SciencesVienna, Austria

Dr. Claus KönigState Ornithological Station of Baden-WürttembergLudwigsburg, Germany

Dr. Adriaan KortlandtZoological Laboratory, University ofAmsterdamAmsterdam, The Netherlands

Dr. Helmut KraftProfessor and Scientific Councillor,Medical Animal Clinic, University ofMunichMunich, Germany


Contributors to the first edition

Dr. Helmut KramerZoological Research Institute and A.Koenig MuseumBonn, Germany

Dr. Franz KrappZoological Institute, University ofFreiburgFreiburg, Switzerland

Dr. Otto KrausProfessor, University of Hamburg,and Director, Zoological Institute andMuseumHamburg, Germany

Dr. Hans KriegProfessor and First Director (retired),Scientific Collections of the State ofBavariaMunich, Germany

Dr. Heinrich KühlFederal Research Institute forFisheries, Cuxhaven LaboratoryCuxhaven, Germany

Dr. Oskar KuhnProfessor, formerly UniversityHalle/SaaleMunich, Germany

Dr. Hans KumerloeveFirst Director (retired), StateScientific Museum, ViennaMunich, Germany

Dr. Nagamichi KurodaYamashina Ornithological Institute,Shibuya-KuTokyo, Japan

Dr. Fred KurtZoological Museum of ZurichUniversity, Smithsonian ElephantSurveyColombo, Ceylon

Dr. Werner LadigesProfessor and Chief Curator,Zoological Institute and Museum,University of HamburgHamburg, Germany

Leslie LaidlawDepartment of Animal Sciences,Purdue UniversityLafayette, Indiana, U.S.A.

Dr. Ernst M. LangDirector, Zoological GardenBasel, Switzerland

Dr. Alfredo LangguthDepartment of Zoology, Faculty ofHumanities and Sciences, Universityof the RepublicMontevideo, Uruguay

Leo LehtonenScience WriterHelsinki, Finland

Bernd LeislerSecond Zoological Institute,University of ViennaVienna, Austria

Dr. Kurt LillelundProfessor and Director, Institute forHydrobiology and Fishery Sciences,University of HamburgHamburg, Germany

R. LiversidgeAlexander MacGregor MemorialMuseumKimberley, South Africa

Dr. Konrad LorenzProfessor and Director, Max PlanckInstitute for Behavioral PhysiologySeewiesen/Obb., Germany

Dr. Martin LühmannFederal Research Institute for theBreeding of Small AnimalsCelle, Germany

Dr. Johannes LüttschwagerOberstudienrat (retired)Heidelberg, Germany

Dr. Wolfgang MakatschBautzen, Germany

Dr. Hubert MarklProfessor and Director, ZoologicalInstitute, Technical University ofDarmstadtDarmstadt, Germany

Basil J. Marlow , BSc (Hons)Curator, Australian MuseumSydney, Australia

Dr. Theodor MebsInstructor of BiologyWeissenhaus/Ostsee, Germany

Dr. Gerlof Fokko MeesCurator of Birds, Rijks Museum ofNatural HistoryLeiden, The Netherlands

Hermann MeinkenDirector, Fish Identification Institute,V.D.A.Bremen, Germany

Dr. Wilhelm MeiseChief Curator, Zoological Instituteand Museum, University of HamburgHamburg, Germany

Dr. Joachim MesstorffField Station of the Federal FisheriesResearch InstituteBremerhaven, Germany

Dr. Marian MlynarskiProfessor, Polish Academy ofSciences, Institute for Systematic andExperimental ZoologyCracow, Poland

Dr. Walburga MoellerNature MuseumHamburg, Germany

Dr. H. C. Erna MohrCurator (retired), Zoological StateInstitute and MuseumHamburg, Germany

Dr. Karl-Heinz MollWaren/Müritz, Germany

Dr. Detlev Müller-UsingProfessor, Institute for GameManagement, University of GöttingenHannoversch-Münden, Germany

Werner MünsterInstructor of BiologyEbersbach, Germany

Dr. Joachim MünzingAltona MuseumHamburg, Germany



ON

TRIB

UTO

RS

TOTH

EFIR

ST

ED

ITION

Dr. Wilbert NeugebauerWilhelma ZooStuttgart-Bad Cannstatt, Germany

Dr. Ian NewtonSenior Scientific Officer, The NatureConservancyEdinburgh, Scotland

Dr. Jürgen NicolaiMax Planck Institute for BehavioralPhysiologySeewiesen/Obb., Germany

Dr. Günther NiethammerProfessor, Zoological ResearchInstitute and A. Koenig MuseumBonn, Germany

Dr. Bernhard NievergeltZoological Museum, University ofZurichZurich, Switzerland

Dr. C. C. OlrogInstitut Miguel Lillo San Miguel deTucumánTucumán, Argentina

Alwin PedersenMammal Research and Arctic ExplorerHolte, Denmark

Dr. Dieter Stefan PetersNature Museum and SenckenbergResearch InstituteFrankfurt a.M., Germany

Dr. Nicolaus PetersScientific Councillor and Docent,Institute of Hydrobiology andFisheries, University of HamburgHamburg, Germany

Dr. Hans-Günter PetzoldAssistant Director, Zoological GardenBerlin, Germany

Dr. Rudolf PiechockiDocent, Zoological Institute,University of HalleHalle a.d.S., Germany

Dr. Ivo Poglayen-NeuwallDirector, Zoological GardenLouisville, Kentucky, U.S.A.

Dr. Egon PoppZoological Collection of the State ofBavariaMunich, Germany

Dr. H. C. Adolf PortmannProfessor Emeritus, ZoologicalInstitute, University of BaselBasel, Switzerland

Hans PsennerProfessor and Director, Alpine ZooInnsbruck, Austria

Dr. Heinz-Siburd RaethelOberveterinärratBerlin, Germany

Dr. Urs H. RahmProfessor, Museum of Natural HistoryBasel, Switzerland

Dr. Werner RathmayerBiology Institute, University ofKonstanzKonstanz, Germany

Walter ReinhardBiologistBaden-Baden, Germany

Dr. H. H. ReinschFederal Fisheries Research InstituteBremerhaven, Germany

Dr. Bernhard RenschProfessor Emeritus, ZoologicalInstitute, University of MünsterMünster, Germany

Dr. Vernon ReynoldsDocent, Department of Sociology,University of BristolBristol, England

Dr. Rupert RiedlProfessor, Department of Zoology,University of North CarolinaChapel Hill, North Carolina, U.S.A.

Dr. Peter RietschelProfessor (retired), ZoologicalInstitute, University of Frankfurt a.M.Frankfurt a.M., Germany

Dr. Siegfried RietschelDocent, University of Frankfurt;Curator, Nature Museum andResearch Institute SenckenbergFrankfurt a.M., Germany

Herbert RinglebenInstitute of Ornithology, HeligolandOrnithological StationWilhelmshaven, Germany

Dr. K. RohdeInstitute for General Zoology, RuhrUniversityBochum, Germany

Dr. Peter RöbenAcademic Councillor, ZoologicalInstitute, Heidelberg UniversityHeidelberg, Germany

Dr. Anton E. M. De RooRoyal Museum of Central AfricaTervuren, South Africa

Dr. Hubert Saint GironsResearch Director, Center forNational Scientific ResearchBrunoy (Essonne), France

Dr. Luitfried Von Salvini-PlawenFirst Zoological Institute, Universityof ViennaVienna, Austria

Dr. Kurt SanftOberstudienrat, Diesterweg-GymnasiumBerlin, Germany

Dr. E. G. Franz SauerProfessor, Zoological ResearchInstitute and A. Koenig Museum,University of BonnBonn, Germany

Dr. Eleonore M. SauerZoological Research Institute and A.Koenig Museum, University of BonnBonn, Germany

Dr. Ernst SchäferCurator, State Museum of LowerSaxonyHannover, Germany



Dr. Friedrich SchallerProfessor and Chairman, FirstZoological Institute, University ofViennaVienna, Austria

Dr. George B. SchallerSerengeti Research Institute, MichaelGrzimek LaboratorySeronera, Tanzania

Dr. Georg ScheerChief Curator and Director,Zoological Institute, State Museum ofHesseDarmstadt, Germany

Dr. Christoph ScherpnerZoological GardenFrankfurt a.M., Germany

Dr. Herbert SchifterBird Collection, Museum of NaturalHistoryVienna, Austria

Dr. Marco SchnitterZoological Museum, ZurichUniversityZurich, Switzerland

Dr. Kurt SchubertFederal Fisheries Research InstituteHamburg, Germany

Eugen SchuhmacherDirector, Animals Films, I.U.C.N.Munich, Germany

Dr. Thomas Schultze-WestrumZoological Institute, University ofMunichMunich, Germany

Dr. Ernst SchütProfessor and Director (retired), StateMuseum of Natural HistoryStuttgart, Germany

Dr. Lester L. Short , Jr.Associate Curator, American Museumof Natural HistoryNew York, New York, U.S.A.

Dr. Helmut SickNational MuseumRio de Janeiro, Brazil

Dr. Alexander F. SkutchProfessor of Ornithology, Universityof Costa RicaSan Isidro del General, Costa Rica

Dr. Everhard J. SlijperProfessor, Zoological Laboratory,University of AmsterdamAmsterdam, The Netherlands

Bertram E. SmythiesCurator (retired), Division of ForestryManagement, Sarawak-MalaysiaEstepona, Spain

Dr. Kenneth E. StagerChief Curator, Los Angeles CountyMuseum of Natural HistoryLos Angeles, California, U.S.A.

Dr. H. C. Georg H. W. SteinProfessor, Curator of Mammals,Institute of Zoology and ZoologicalMuseum, Humboldt UniversityBerlin, Germany

Dr. Joachim SteinbacherCurator, Nature Museum andSenckenberg Research InstituteFrankfurt a.M., Germany

Dr. Bernard StonehouseCanterbury UniversityChristchurch, New Zealand

Dr. Richard Zur StrassenCurator, Nature Museum andSenckenberg Research InstituteFrandfurt a.M., Germany

Dr. Adelheid Studer-ThierschZoological GardenBasel, Switzerland

Dr. Ernst SutterMuseum of Natural HistoryBasel, Switzerland

Dr. Fritz TerofalDirector, Fish Collection, ZoologicalCollection of the State of BavariaMunich, Germany

Dr. G. F. Van TetsWildlife ResearchCanberra, Australia

Ellen Thaler-KottekInstitute of Zoology, University ofInnsbruckInnsbruck, Austria

Dr. Erich TheniusProfessor and Director, Institute ofPaleontolgy, University of ViennaVienna, Austria

Dr. Niko TinbergenProfessor of Animal Behavior,Department of Zoology, OxfordUniversityOxford, England

Alexander TsurikovLecturer, University of MunichMunich, Germany

Dr. Wolfgang VillwockZoological Institute and Museum,University of HamburgHamburg, Germany

Zdenek VogelDirector, Suchdol HerpetologicalStationPrague, Czechoslovakia

Dieter VogtSchorndorf, Germany

Dr. Jiri VolfZoological GardenPrague, Czechoslovakia

Otto WadewitzLeipzig, Germany

Dr. Helmut O. WagnerDirector (retired), Overseas Museum,BremenMexico City, Mexico

Dr. Fritz WaltherProfessor, Texas A & M UniversityCollege Station, Texas, U.S.A.

John WarhamZoology Department, CanterburyUniversityChristchurch, New Zealand

Dr. Sherwood L. WashburnUniversity of California at BerkeleyBerkeley, California, U.S.A.



ON

TRIB

UTO

RS

TOTH

EFIR

ST

ED

ITION

Eberhard WawraFirst Zoological Institute, Universityof ViennaVienna, Austria

Dr. Ingrid WeigelZoological Collection of the State ofBavariaMunich, Germany

Dr. B. WeischerInstitute of Nematode Research,Federal Biological InstituteMünster/Westfalen, Germany

Herbert WendtAuthor, Natural HistoryBaden-Baden, Germany

Dr. Heinz WermuthChief Curator, State Nature Museum,StuttgartLudwigsburg, Germany

Dr. Wolfgang Von WesternhagenPreetz/Holstein, Germany

Dr. Alexander WetmoreUnited States National Museum,Smithsonian InstitutionWashington, D.C., U.S.A.

Dr. Dietrich E. WilckeRöttgen, Germany

Dr. Helmut WilkensProfessor and Director, Institute ofAnatomy, School of VeterinaryMedicineHannover, Germany

Dr. Michael L. WolfeUtah, U.S.A.

Hans Edmund WoltersZoological Research Institute and A.Koenig MuseumBonn, Germany

Dr. Arnfrid WünschmannResearch Associate, Zoological GardenBerlin, Germany

Dr. Walter WüstInstructor, Wilhelms GymnasiumMunich, Germany

Dr. Heinz WundtZoological Collection of the State ofBavariaMunich, Germany

Dr. Claus-Dieter ZanderZoological Institute and Museum,University of HamburgHamburg, Germany

Dr. Fritz ZumptDirector, Entomology andParasitology, South African Institutefor Medical ResearchJohannesburg, South Africa

Dr. Richard L. ZusiCurator of Birds, United StatesNational Museum, SmithsonianInstitutionWashington, D.C., U.S.A.



Adaptive radiation—Diversification of a species or singleancestral type into several forms that are each adaptivelyspecialized to a specific niche.

Agonistic—Behavioral patterns that are aggressive in con-text.

Allopatric—Occurring in separate, nonoverlapping geo-graphic areas.

Alpha breeder—The reproductively dominant member ofa social unit.

Altricial—An adjective referring to a mammal that is bornwith little, if any, hair, is unable to feed itself, and ini-tially has poor sensory and thermoregulatory abilities.

Amphibious—Refers to the ability of an animal to moveboth through water and on land.

Austral—May refer to “southern regions,” typicallymeaning Southern Hemisphere. May also refer to thegeographical region included within the Transition,Upper Austral, and Lower Austral Life Zones as de-fined by C. Hart Merriam in 1892–1898. These zonesare often characterized by specific plant and animalcommunities and were originally defined by tempera-ture gradients especially in the mountains of south-western North America.

Bergmann’s rule—Within a species or among closely re-lated species of mammals, those individuals in colder en-vironments often are larger in body size. Bergmann’srule is a generalization that reflects the ability of en-dothermic animals to more easily retain body heat (incold climates) if they have a high body surface to bodyvolume ratio, and to more easily dissipate excess bodyheat (in hot environments) if they have a low body sur-face to body volume ratio.

Bioacoustics—The study of biological sounds such as thesounds produced by bats or other mammals.

Biogeographic region—One of several major divisions ofthe earth defined by a distinctive assemblage of animalsand plants. Sometimes referred to as “zoogeographic re-gions or realms” (for animals) or “phytogeographic re-gions or realms” (for plants). Such terminology datesfrom the late nineteenth century and varies considerably.Major biogeographic regions each have a somewhat dis-tinctive flora and fauna. Those generally recognized in-clude Nearctic, Neotropical, Palearctic, Ethiopian,Oriental, and Australian.

Blow—Cloud of vapor and sea water exhaled by cetaceans.

Boreal—Often used as an adjective meaning “northern”;also may refer to the northern climatic zone immediatelysouth of the Arctic; may also include the Arctic, Hud-sonian, and Canadian Life Zones described by C. HartMerriam.

Brachiating ancestor—Ancestor that swung around by thearms.

Breaching—A whale behavior—leaping above the water’ssurface, then falling back into the water, landing on itsback or side.

Cephalopod—Member of the group of mollusks such assquid and octopus.

Cladistic—Evolutionary relationships suggested as “tree”branches to indicate lines of common ancestry.

Cline—A gradient in a measurable characteristic, such assize and color, showing geographic differentiation. Vari-ous patterns of geographic variation are reflected asclines or clinal variation, and have been described as“ecogeographic rules.”

Cloaca—A common opening for the digestive, urinary, andreproductive tracts found in monotreme mammals.

Colony—A group of mammals living in close proximity, in-teracting, and usually aiding in early warning of thepresence of predators and in group defense.


• • • • •

Glossary

Commensal—A relationship between species in which onebenefits and the other is neither benefited nor harmed.

Congeneric—Descriptive of two or more species that be-long to the same genus.

Conspecific—Descriptive of two or more individuals orpopulations that belong to the same species.

Contact call—Simple vocalization used to maintain com-munication or physical proximity among members of asocial unit.

Convergent evolution—When two evolutionarily unre-lated groups of organisms develop similar characteristicsdue to adaptation to similar aspects of their environmentor niche.

Coprophagy—Reingestion of feces to obtain nutrients thatwere not ingested the first time through the digestivesystem.

Cosmopolitan—Adjective describing the distribution pat-tern of an animal found around the world in suitablehabitats.

Crepuscular—Active at dawn and at dusk.

Critically Endangered—A technical category used byIUCN for a species that is at an extremely high risk ofextinction in the wild in the immediate future.

Cryptic—Hidden or concealed; i.e., well-camouflaged pat-terning.

Dental formula—A method for describing the number ofeach type of tooth found in an animal’s mouth: incisors(I), canines (C), premolars (P), and molars (M). The for-mula gives the number of each tooth found in an upperand lower quadrant of the mouth, and the total is multi-plied by two for the total number of teeth. For example,the formula for humans is: I2/2 C1/1 P2/2 M3/3 (total,16, times two is 32 teeth).

Dimorphic—Occurring in two distinct forms (e.g., in ref-erence to the differences in size between males and fe-males of a species).

Disjunct—A distribution pattern characterized by popula-tions that are geographically separated from one another.

Diurnal—Active during the day.

DNA-DNA hybridization—A technique whereby the ge-netic similarity of different animal groups is determinedbased on the extent to which short stretches of theirDNA, when mixed together in solution in the labora-tory, are able to join with each other.

Dominance hierarchy—The social status of individuals ina group; each animal can usually dominate those animalsbelow it in a hierarchy.

Dorso-ventrally—From back to front.

Duetting—Male and female singing and integrating theirsongs together.

Echolocation—A method of navigation used by somemammals (e.g., bats and marine mammals) to locate ob-jects and investigate surroundings. The animals emit au-dible “clicks” and determine pathways by using the echoof the sound from structures in the area.

Ecotourism—Travel for the primary purpose of viewingnature. Ecotourism is now “big business” and is used asa non-consumptive but financially rewarding way to pro-tect important areas for conservation.

Ectothermic—Using external energy and behavior to regu-late body temperature. “Cold-blooded.”

Endangered—A term used by IUCN and also under theEndangered Species Act of 1973 in the United States inreference to a species that is threatened with imminentextinction or extirpation over all or a significant portionof its range.

Endemic—Native to only one specific area.

Endothermic—Maintaining a constant body-temperatureusing metabolic energy. “Warm-blooded.”

Eocene—Geological time period; subdivision of the Ter-tiary, from about 55.5 to 33.7 million years ago.

Ethology—The study of animal behavior.

Exotic—Not native.

Extant—Still in existence; not destroyed, lost, or extinct.

Extinct—Refers to a species that no longer survives any-where.

Extirpated—Referring to a local extinction of a species thatcan still be found elsewhere.

Feral—A population of domesticated animal that lives inthe wild.

Flehmen—Lip curling and head raising after sniffing a fe-male’s urine.

Forb—Any herb that is not a grass or grass-like.

Fossorial—Adapted for digging.


Glossary

Frugivorous—Feeds on fruit.

Granivorous—Feeding on seeds.

Gravid—Pregnant.

Gregarious—Occuring in large groups.

Hibernation—A deep state of reduced metabolic activityand lowered body temperature that may last for weeks ormonths.

Holarctic—The Palearctic and Nearctic bigeographic re-gions combined.

Hybrid—The offspring resulting from a cross between twodifferent species (or sometimes between distinctive sub-species).

Innate—An inherited characteristic.

Insectivorous—Technically refers to animals that eat in-sects; generally refers to animals that feed primarily oninsects and other arthropods.

Introduced species—An animal or plant that has been in-troduced to an area where it normally does not occur.

Iteroparous—Breeds in multiple years.

Jacobson’s organ—Olfactory organ found in the upperpalate that first appeared in amphibians and is most de-veloped in these and in reptiles, but is also found insome birds and mammals.

Kiva—A large chamber wholly or partly underground, andoften used for religious ceremonies in Pueblo Indian vil-lages.

Mandible—Technically an animal’s lower jaw. The plural,mandibles, is used to refer to both the upper and lowerjaw. The upper jaw is technically the maxilla, but oftencalled the “upper mandible.”

Marsupial—A mammal whose young complete their em-bryonic development outside of the mother’s body,within a maternal pouch.

Matrilineal—Describing a social unit in which group mem-bers are descended from a single female.

Melon—The fat-filled forehead of aquatic mammals of theorder Cetacea.

Metabolic rate—The rate of chemical processes in livingorganisms, resulting in energy expenditure and growth.Metabolic rate decreases when an animal is resting andincreases during activity.

Migration—A two-way movement in some mammals, oftendramatically seasonal. Typically latitudinal, though insome species is altitudinal or longitudinal. May be short-distance or long-distance.

Miocene—The geological time period that lasted fromabout 23.8 to 5.6 million years ago.

Molecular phylogenetics—The use of molecular (usuallygenetic) techniques to study evolutionary relationshipsbetween or among different groups of organisms.

Monestrous—Experiencing estrus just once each year orbreeding season.

Monogamous—A breeding system in which a male and fe-male mate only with one another.

Monophyletic—A group (or clade) that shares a commonancestor.

Monotypic—A taxonomic category that includes only oneform (e.g., a genus that includes only one species; aspecies that includes no subspecies).

Montane—Of or inhabiting the biogeographic zone of rel-atively moist, cool upland slopes below timberline domi-nated by large coniferous trees.

Morphology—The form and structure of animals and plants.

Mutualism—Ecological relationship between two species inwhich both gain benefit.

Near Threatened—A category defined by the IUCN sug-gesting possible risk of extinction in the medium term(as opposed to long or short term) future.

Nearctic—The biogeographic region that includes temper-ate North America. faunal region.

Neotropical—The biogeographic region that includesSouth and Central America, the West Indies, and tropi-cal Mexico.

New World—A general descriptive term encompassing theNearctic and Neotropical biogeographic regions.

Niche—The role of an organism in its environment; multi-dimensional, with habitat and behavioral components.

Nocturnal—Active at night.

Old World—A general term that usually describes aspecies or group as being from Eurasia or Africa.

Oligocene—The geologic time period occurring fromabout 33.7 to 23.8 million years ago.


GlossaryG

LOSSA

RY

Omnivorous—Feeding on a broad range of foods, bothplant and animal matter.

Palearctic—A biogeographic region that includes temper-ate Eurasia and Africa north of the Sahara.

Paleocene—Geological period, subdivision of the Tertiary,from 65 to 55.5 million years ago.

Pelage—Coat, skin, and hair.

Pelagic—An adjective used to indicate a relationship to theopen sea.

Pestiferous—Troublesome or annoying; nuisance.

Phylogeny—A grouping of taxa based on evolutionary his-tory.

Piscivorous—Fish-eating.

Placental—A mammal whose young complete their embry-onic development within the mother’s uterus, joined toher by a placenta.

Pleistocene—In general, the time of the great ice ages; ge-ological period variously considered to include the last 1to 1.8 million years.

Pliocene—The geological period preceding the Pleisto-cence; the last subdivision of what is known as the Ter-tiary; lasted from 5.5 to 1.8 million years ago.

Polyandry—A breeding system in which one female mateswith two or more males.

Polygamy—A breeding system in which either or bothmale and female may have two or more mates.

Polygyny—A breeding system in which one male mateswith two or more females.

Polyphyletic—A taxonomic group that is believed to haveoriginated from more than one group of ancestors.

Post-gastric digestion—Refers to the type of fermentativedigestion of vegetative matter found in tapirs and otheranimals by which microorganisms decompose food in acaecum. This is not as thorough a decomposition as oc-curs in ruminant digesters.

Precocial—An adjective used to describe animals that areborn in an advanced state of development such that theygenerally can leave their birth area quickly and obtaintheir own food, although they are often led to food andguarded by a parent.

Proboscis—The prehensile trunk (a muscular hydrostat)found in tapirs, elephants, etc.

Quaternary—The geological period, from 1.8 million yearsago to the present, usually including two subdivisions:the Pleistocene, and the Holocene.

Refugium (pl. refugia) —An area relatively unaltered dur-ing a time of climatic change, from which dispersion andspeciation may occur after the climate readjusts.

Reproductive longevity—The length of an animal’s lifeover which it is capable of reproduction.

Ruminant—An even-toed, hoofed mammal with a four-chambered stomach that eats rapidly to regurgitate itsfood and chew the cud later.

Scansorial—Specialized for climbing.

Seed dispersal—Refers to how tapirs and other animalstransport viable seeds from their source to near or dis-tant, suitable habitats where they can successfully germi-nate. Such dispersal may occur through the feces,through sputum, or as the seeds are attached and laterreleased from fur, etc.

Semelparity—A short life span, in which a single instanceof breeding is followed by death in the first year of life.

Sexual dimorphism—Male and female differ in morphol-ogy, such as size, feather size or shape, or bill size orshape.

Sibling species—Two or more species that are very closelyrelated, presumably having differentiated from a com-mon ancestor in the recent past; often difficult to distin-guish, often interspecifically territorial.

Sonagram—A graphic representation of sound.

Speciation—The evolution of new species.

Spy-hopping—Positioning the body vertically in the water,with the head raised above the sea surface, sometimeswhile turning slowly.

Steppe—Arid land with vegetation that can thrive withvery little moisture; found usually in regions of extremetemperature range.

Suspensory—Moving around or hanging by the arms.

Sympatric—Inhabiting the same range.

Systematist—A specialist in the classification of organisms;systematists strive to classify organisms on the basis oftheir evolutionary relationships.

Taxon (pl. taxa) —Any unit of scientific classification (e.g.,species, genus, family, order).


Glossary

Taxonomist—A specialist in the naming and classificationof organisms. (See also Systematist. Taxonomy is theolder science of naming things; identification of evolu-tionary relationships has not always been the goal of tax-onomists. The modern science of systematics generallyincorporates taxonomy with the search for evolutionaryrelationships.)

Taxonomy—The science of identifying, naming, and clas-sifying organisms into groups.

Territoriality—Refers to an animal’s defense of a certainportion of its habitat against other conspecifics. This isoften undertaken by males in relation to one anotherand as a lure to females.

Territory—Any defended area. Territorial defense is typi-cally male against male, female against female, andwithin a species or between sibling species. Area de-fended varies greatly among taxa, seasons, and habitats.A territory may include the entire home range, only thearea immediately around a nest, or only a feeding area.

Tertiary—The geological period including most of theCenozoic; from about 65 to 1.8 million years ago.

Thermoregulation—The ability to regulate body tempera-ture; can be either behavioral or physiological.

Tribe—A unit of classification below the subfamily andabove the genus.

Truncal erectness—Sitting, hanging, arm-swinging(brachiating), walking bipedally with the backbone heldvertical.

Ungulate—A hoofed mammal.

Upper cone—The circle in which the arm can rotate whenraised above the head.

Viable population—A population that is capable of main-taining itself over a period of time. One of the majorconservation issues of the twenty-first century is deter-mining what is a minimum viable population size. Popu-lation geneticists have generally come up with estimatesof about 500 breeding pairs.

Vulnerable—A category defined by IUCN as a species thatis not Critically Endangered or Endangered, but is stillfacing a threat of extinction.


GlossaryG

LOSSA

RY

Monotremata [Order]

Tachyglossidae [Family]Tachyglossus [Genus]

T. aculeatus [Species]Zaglossus [Genus]

Z. bruijni [Species]

Ornithorhynchidae [Family]Ornithorhynchus [Genus]

O. anatinus [Species]

Didelphimorphia [Order]

Didelphidae [Family]Caluromys [Genus]

C. derbianus [Species]C. lanatusC. philander

Caluromysiops [Genus]C. irrupta [Species]

Chironectes [Genus]C. minimus [Species]

Didelphis [Genus]D. albiventris [Species]D. auritaD. marsupialisD. virginiana

Glironia [Genus]G. venusta [Species]

Gracilinanus [Genus]G. aceramarcae [Species]G. agilisG. dryasG. emiliaeG. maricaG. microtarsus

Lestodelphys [Genus]L. halli [Species]

Lutreolina [Genus]L. crassicaudata [Species]

Marmosa [Genus]M. andersoni [Species]M. canescensM. lepida

M. mexicanaM. murinaM. robinsoniM. rubraM. tylerianaM. xerophila

Marmosops [Genus]M. cracens [Species]M. dorotheaM. fuscatusM. handleyiM. impavidusM. incanusM. invictusM. noctivagusM. parvidens

Metachirus [Genus]M. nudicaudatus [Species]

Micoureus [Genus]M. alstoni [Species]M. constantiaeM. demeraraeM. regina

Monodelphis [Genus]M. adusta [Species]M. americanaM. brevicaudataM. dimidiataM. domesticaM. emiliaeM. iheringiM. kunsiM. maraxinaM. osgoodiM. rubidaM. scalopsM. sorexM. theresaM. unistriata

Philander [Genus]P. andersoni [Species]P. opossum

Thylamys [Genus]T. elegans [Species]

T. macruraT. pallidiorT. pusillaT. velutinus

Paucituberculata [Order]

Caenolestidae [Family]Caenolestes [Genus]

C. caniventer [Species]C. convelatusC. fuliginosus

Lestoros [Genus]L. inca [Species]

Rhyncholestes [Genus]R. raphanurus [Species]

Microbiotheria [Order]

Microbiotheriidae [Family]Dromiciops [Genus]

D. gliroides [Species]

Dasyuromorphia [Order]

Dasyuridae [Family]Antechinus [Genus]

A. bellus [Species]A. flavipesA. godmaniA. leoA. melanurusA. minimusA. nasoA. stuartiiA. swainsoniiA. wilhelmina

Dasycercus [Genus]D. byrnei [Species]D. cristicauda

Dasykaluta [Genus]D. rosamondae [Species]

Dasyurus [Genus]D. albopunctatus [Species]D. geoffroiiD. hallucatus


• • • • •

Mammals species list

D. maculatusD. spartacusD. viverrinus

Murexia [Genus]M. longicaudata [Species]M. rothschildi

Myoictis [Genus]M. melas [Species]

Neophascogale [Genus]N. lorentzi [Species]

Ningaui [Genus]N. ridei [Species]N. timealeyiN. yvonnae

Parantechinus [Genus]P. apicalis [Species]P. bilarni

Phascogale [Genus]P. calura [Species]P. tapoatafa

Phascolosorex [Genus]P. doriae [Species]P. dorsalis

Planigale [Genus]P. gilesi [Species]P. ingramiP. maculataP. novaeguineaeP. tenuirostris

Pseudantechinus [Genus]P. macdonnellensis [Species]P. ningbingP. woolleyae

Sarcophilus [Genus]S. laniarius [Species]

Sminthopsis [Genus]S. aitkeni [Species]S. archeriS. butleriS. crassicaudataS. dolichuraS. douglasiS. fuliginosusS. gilbertiS. granulipesS. griseoventerS. hirtipesS. lanigerS. leucopusS. longicaudataS. macrouraS. murinaS. ooldeaS. psammophilaS. virginiaeS. youngsoni

Myrmecobiidae [Family]Myrmecobius [Genus]

M. fasciatus [Species]

Thylacinidae [Family]Thylacinus [Genus]

T. cynocephalus [Species]

Peramelemorphia [Order]

Peramelidae [Family]Chaeropus [Genus]

C. ecaudatus [Species]Isoodon [Genus]

I. auratus [Species]I. macrourusI. obesulus

Macrotis [Genus]M. lagotis [Species]M. leucura

Perameles [Genus]P. bougainville [Species]P. eremianaP. gunniiP. nasuta

Peroryctidae [Family]Echymipera [Genus]

E. clara [Species]E. davidiE. echinistaE. kalubuE. rufescens

Microperoryctes [Genus]M. longicauda [Species]M. murinaM. papuensis

Peroryctes [Genus]P. broadbenti [Species]P. raffrayana

Rhynchomeles [Genus]R. prattorum [Species]

Notoryctemorphia [Order]

Notoryctidae [Family]Notoryctes [Genus]

N. caurinus [Species]N. typhlops

Diprotodontia [Order]

Phascolarctidae [Family]Phascolarctos [Genus]

P. cinereus [Species]

Vombatidae [Family]Lasiorhinus [Genus]

L. krefftii [Species]L. latifrons

Vombatus [Genus]V. ursinus [Species]

Phalangeridae [Family]Ailurops [Genus]

A. ursinus [Species]

Phalanger [Genus]P. carmelitae [Species]P. lullulaeP. matanimP. orientalisP. ornatusP. pelengensisP. rothschildiP. sericeusP. vestitus

Spilocuscus [Genus]S. maculatus [Species]S. rufoniger

Strigocuscus [Genus]S. celebensis [Species]S. gymnotis

Trichosurus [Genus]T. arnhemensis [Species]T. caninusT. vulpecula

Wyulda [Genus]W. squamicaudata [Species]

Hypsiprymnodontidae [Family]Hypsiprymnodon [Genus]

H. moschatus [Species]

Potoroidae [Family]Aepyprymnus [Genus]

A. rufescens [Species]Bettongia [Genus]

B. gaimardi [Species]B. lesueurB. penicillata

Caloprymnus [Genus]C. campestris [Species]

Potorous [Genus]P. longipes [Species]P. platyopsP. tridactylus

Macropodidae [Family]Dendrolagus [Genus]

D. bennettianus [Species]D. dorianusD. goodfellowiD. inustusD. lumholtziD. matschieiD. scottaeD. spadixD. ursinus

Dorcopsis [Genus]D. atrata [Species]D. hageniD. luctuosaD. muelleri

Dorcopsulus [Genus]D. macleayi [Species]D. vanheurni

Lagorchestes [Genus]


Mammals species listM

AM

MA

LSSP

EC

IES

LIST

L. asomatus [Species]L. conspicillatusL. hirsutusL. leporides

Lagostrophus [Genus]L. fasciatus [Species]

Macropus [Genus]M. agilis [Species]M. antilopinusM. bernardusM. dorsalisM. eugeniiM. fuliginosusM. giganteusM. greyiM. irmaM. parmaM. parryiM. robustusM. rufogriseusM. rufus

Onychogalea [Genus]O. fraenata [Species]O. lunataO. unguifera

Petrogale [Genus]P. assimilis [Species]P. brachyotisP. burbidgeiP. concinnaP. godmaniP. inornataP. lateralisP. penicillataP. persephoneP. rothschildiP. xanthopus

Setonix [Genus]S. brachyurus [Species]

Thylogale [Genus]T. billardierii [Species]T. bruniiT. stigmaticaT. thetis

Wallabia [Genus]W. bicolor [Species]

Burramyidae [Family]Burramys [Genus]

B. parvus [Species]Cercartetus [Genus]

C. caudatus [Species]C. concinnusC. lepidusC. nanus

Pseudocheiridae [Family]Hemibelideus [Genus]

H. lemuroides [Species]Petauroides [Genus]

P. volans [Species]

Petropseudes [Genus]P. dahli [Species]

Pseudocheirus [Genus]P. canescens [Species]P. caroliP. forbesiP. herbertensisP. mayeriP. peregrinusP. schlegeli

Pseudochirops [Genus]P. albertisii [Species]P. archeriP. corinnaeP. cupreus

Petauridae [Family]Dactylopsila [Genus]

D. megalura [Species]D. palpatorD. tateiD. trivirgata

Gymnobelideus [Genus]G. leadbeateri [Species]

Petaurus [Genus]P. abidi [Species]P. australisP. brevicepsP. gracilisP. norfolcensis

Tarsipedidae [Family]Tarsipes [Genus]

T. rostratus [Species]

Acrobatidae [Family]Acrobates [Genus]

A. pygmaeus [Species]Distoechurus [Genus]

D. pennatus [Species]

Xenarthra [Order]

Megalonychidae [Family]Choloepus [Genus]

C. didactylus [Species]C. hoffmanni

Bradypodidae [Family]Bradypus [Genus]

B. torquatus [Species]B. tridactylusB. variegatus

Myrmecophagidae [Family]Cyclopes [Genus]

C. didactylus [Species]Myrmecophaga [Genus]

M. tridactyla [Species]Tamandua [Genus]

T. mexicana [Species]T. tetradactyla

Dasypodidae [Family]Chlamyphorus [Genus]

C. retusus [Species]C. truncatus

Cabassous [Genus]C. centralis [Species]C. chacoensisC. tatouayC. unicinctus

Chaetophractus [Genus]C. nationi [Species]C. vellerosusC. villosus

Dasypus [Genus]D. hybridus [Species]D. kappleriD. novemcinctusD. pilosusD. sabanicolaD. septemcinctus

Euphractus [Genus]E. sexcinctus [Species]

Priodontes [Genus]P. maximus [Species]

Tolypeutes [Genus]T. matacus [Species]T. tricinctus

Zaedyus [Genus]Z. pichiy [Species]

Insectivora [Order]

Erinaceidae [Family]Atelerix [Genus]

A. albiventris [Species]A. algirusA. frontalisA. sclateri

Erinaceus [Genus]E. amurensis [Species]E. concolorE. europaeus

Hemiechinus [Genus]H. aethiopicus [Species]H. auritusH. collarisH. hypomelasH. micropusH. nudiventris

Mesechinus [Genus]M. dauuricus [Species]M. hughi

Echinosorex [Genus]E. gymnura [Species]

Hylomys [Genus]H. hainanensis [Species]H. sinensisH. suillus

Podogymnura [Genus]P. aureospinula [Species]P. truei



Chrysochloridae [Family]Amblysomus [Genus]

A. gunningi [Species]A. hottentotusA. irisA. julianae

Calcochloris [Genus]C. obtusirostris [Species]

Chlorotalpa [Genus]C. arendsi [Species]C. duthieaeC. leucorhinaC. sclateriC. tytonis

Chrysochloris [Genus]C. asiatica [Species]C. stuhlmanniC. visagiei

Chrysospalax [Genus]C. trevelyani [Species]C. villosus

Cryptochloris [Genus]C. wintoni [Species]C. zyli

Eremitalpa [Genus]E. granti [Species]

Tenrecidae [Family]Echinops [Genus]

E. telfairi [Species]Geogale [Genus]

G. aurita [Species]Hemicentetes [Genus]

H. semispinosus [Species]Limnogale [Genus]

L. mergulus [Species]Microgale [Genus]

M. brevicaudata [Species]M. cowaniM. dobsoniM. dryasM. gracilisM. longicaudataM. parvulaM. principulaM. pullaM. pusillaM. talazaciM. thomasi

Micropotamogale [Genus]M. lamottei [Species]M. ruwenzorii

Oryzorictes [Genus]O. hova [Species]O. talpoidesO. tetradactylus

Potamogale [Genus]P. velox [Species]

Setifer [Genus]S. setosus [Species]

Tenrec [Genus]T. ecaudatus [Species]

Solenodontidae [Family]Solenodon [Genus]

S. cubanus [Species]S. marcanoiS. paradoxus

Nesophontidae [Family]Nesophontes [Genus]

N. edithae [Species]N. hypomicrusN. longirostrisN. majorN. micrusN. paramicrusN. submicrusN. zamicrus

Soricidae [Family]Anourosorex [Genus]

A. squamipes [Species]Blarina [Genus]

B. brevicauda [Species]B. carolinensisB. hylophaga

Blarinella [Genus]B. quadraticauda [Species]B. wardi

Chimarrogale [Genus]C. hantu [Species]C. himalayicaC. phaeuraC. platycephalaC. styaniC. sumatrana

Congosorex [Genus]C. polli [Species]

Crocidura [Genus]C. aleksandrisi [Species]C. allexC. andamanensisC. ansellorumC. arabicaC. armenicaC. attenuataC. attilaC. baileyiC. batesiC. beatusC. beccariiC. bottegiC. bottegoidesC. buettikoferiC. caligineaC. canariensisC. cinderellaC. congobelgicaC. cossyrensisC. crenata

C. crosseiC. cyaneaC. dentiC. desperataC. dhofarensisC. dolichuraC. doucetiC. dsinezumiC. eisentrautiC. elgoniusC. elongataC. ericaC. fischeriC. flavescensC. floweriC. foxiC. fuliginosaC. fulvastraC. fumosaC. fuscomurinaC. glassiC. goliathC. gracilipesC. grandicepsC. grandisC. grasseiC. grayiC. greenwoodiC. gueldenstaedtiiC. harennaC. hildegardeaeC. hirtaC. hispidaC. horsfieldiiC. jacksoniC. jenkinsiC. kivuanaC. lamotteiC. lanosaC. lasiuraC. latonaC. leaC. leucodonC. leviculaC. littoralisC. longipesC. lucinaC. ludiaC. lunaC. lusitaniaC. macarthuriC. macmillaniC. macowiC. malayanaC. manengubaeC. maquassiensisC. mariquensisC. mauriscaC. maxiC. mindorus



AM

MA

LSSP

EC

IES

LIST

C. minutaC. miyaC. monaxC. monticolaC. montisC. muricaudaC. mutesaeC. nanaC. nanillaC. neglectaC. negrinaC. nicobaricaC. nigeriaeC. nigricansC. nigripesC. nigrofuscaC. nimbaeC. niobeC. obscuriorC. olivieriC. oriiC. osorioC. palawanensisC. paradoxuraC. parvipesC. pashaC. pergriseaC. phaeuraC. piceaC. pitmaniC. planicepsC. poensisC. poliaC. pullataC. raineyiC. religiosaC. rhoditisC. rooseveltiC. russulaC. selinaC. serezkyensisC. sibiricaC. siculaC. silaceaC. smithiiC. somalicaC. stenocephalaC. suaveolensC. susianaC. tansanianaC. tarellaC. tarfayensisC. telfordiC. tenuisC. thaliaC. theresaeC. thomensisC. turbaC. ultimaC. usambarae

C. viariaC. voiC. whitakeriC. wimmeriC. xantippeC. yankariensisC. zaphiriC. zarudnyiC. zimmeriC. zimmermanni

Cryptotis [Genus]C. avia [Species]C. endersiC. goldmaniC. goodwiniC. gracilisC. hondurensisC. magnaC. meridensisC. mexicanaC. montivagaC. nigrescensC. parvaC. squamipesC. thomasi

Diplomesodon [Genus]D. pulchellum [Species]

Feroculus [Genus]F. feroculus [Species]

Megasorex [Genus]M. gigas [Species]

Myosorex [Genus]M. babaulti [Species]M. blarinaM. caferM. eisentrautiM. geataM. longicaudatusM. okuensisM. rumpiiM. schalleriM. sclateriM. tenuisM. varius

Nectogale [Genus]N. elegans [Species]

Neomys [Genus]N. anomalus [Species]N. fodiensN. schelkovnikovi

Notiosorex [Genus]N. crawfordi [Species]

Paracrocidura [Genus]P. graueri [Species]P. maximaP. schoutedeni

Ruwenzorisorex [Genus]R. suncoides [Species]

Scutisorex [Genus]S. somereni [Species]

Solisorex [Genus]S. pearsoni [Species]

Sorex [Genus]S. alaskanus [Species]S. alpinusS. araneusS. arcticusS. arizonaeS. asperS. bairdiiS. bedfordiaeS. bendiriiS. buchariensisS. caecutiensS. camtschaticaS. cansulusS. cinereusS. coronatusS. cylindricaudaS. daphaenodonS. disparS. emarginatusS. excelsusS. fumeusS. gaspensisS. gracillimusS. granariusS. haydeniS. hosonoiS. hoyiS. hydrodromusS. isodonS. jacksoniS. kozloviS. leucogasterS. longirostrisS. lyelliS. macrodonS. merriamiS. milleriS. minutissimusS. minutusS. mirabilisS. monticolusS. nanusS. oreopolusS. ornatusS. pacificusS. palustrisS. planicepsS. portenkoiS. prebleiS. raddeiS. roboratusS. sadonisS. samniticusS. satuniniS. saussureiS. sclateriS. shinto



S. sinalisS. sonomaeS. stizodonS. tenellusS. thibetanusS. trowbridgiiS. tundrensisS. ugyunakS. unguiculatusS. vagransS. ventralisS. veraepacisS. volnuchini

Soriculus [Genus]S. caudatus [Species]S. fumidusS. hypsibiusS. lamulaS. leucopsS. macrurusS. nigrescensS. parcaS. salenskiiS. smithii

Suncus [Genus]S. ater [Species]S. dayiS. etruscusS. fellowesgordoniS. hoseiS. infinitesimusS. lixusS. madagascariensisS. malayanusS. mertensiS. montanusS. murinusS. remyiS. stoliczkanusS. varillaS. zeylanicus

Surdisorex [Genus]S. norae [Species]S. polulus

Sylvisorex [Genus]S. granti [Species]S. howelliS. isabellaeS. johnstoniS. lunarisS. megaluraS. morioS. ollulaS. oriundusS. vulcanorum

Talpidae [Family]Desmana [Genus]

D. moschata [Species]Galemys [Genus]

G. pyrenaicus [Species]

Condylura [Genus]C. cristata [Species]

Euroscaptor [Genus]E. grandis [Species]E. klossiE. longirostrisE. micruraE. mizuraE. parvidens

Mogera [Genus]M. etigo [Species]M. insularisM. kobeaeM. minorM. robustaM. tokudaeM. wogura

Nesoscaptor [Genus]N. uchidai [Species]

Neurotrichus [Genus]N. gibbsii [Species]

Parascalops [Genus]P. breweri [Species]

Parascaptor [Genus]P. leucura [Species]

Scalopus [Genus]S. aquaticus [Species]

Scapanulus [Genus]S. oweni [Species]

Scapanus [Genus]S. latimanus [Species]S. orariusS. townsendii

Scaptochirus [Genus]S. moschatus [Species]

Scaptonyx [Genus]S. fusicaudus [Species]

Talpa [Genus]T. altaica [Species]T. caecaT. caucasicaT. europaeaT. levantisT. occidentalisT. romanaT. stankoviciT. streeti

Urotrichus [Genus]U. pilirostris [Species]U. talpoides

Uropsilus [Genus]U. andersoni [Species]U. gracilisU. investigatorU. soricipes

Scandentia [Order]

Tupaiidae [Family]Anathana [Genus]

A. ellioti [Species]

Dendrogale [Genus]D. melanura [Species]D. murina

Ptilocercus [Genus]P. lowii [Species]

Tupaia [Genus]T. belangeri [Species]T. chrysogasterT. dorsalisT. glisT. gracilisT. javanicaT. longipesT. minorT. montanaT. nicobaricaT. palawanensisT. pictaT. splendidulaT. tana

Urogale [Genus]U. everetti [Species]

Dermoptera [Order]

Cynocephalidae [Family]Cynocephalus [Genus]

C. variegatus [Species]C. volans

Chiroptera [Order]

Pteropodidae [Family]Acerodon [Genus]

A. celebensis [Species]A. humilisA. jubatusA. leucotisA. luciferA. mackloti

Aethalops [Genus]A. alecto [Species]

Alionycteris [Genus]A. paucidentata [Species]

Aproteles [Genus]A. bulmerae [Species]

Balionycteris [Genus]B. maculata [Species]

Boneia [Genus]B. bidens [Species]

Casinycteris [Genus]C. argynnis [Species]

Chironax [Genus]C. melanocephalus [Species]

Cynopterus [Genus]C. brachyotis [Species]C. horsfieldiC. nusatenggaraC. sphinxC. titthaecheileus

Dobsonia [Genus]



AM

MA

LSSP

EC

IES

LIST

D. beauforti [Species]D. chapmaniD. emersaD. exoletaD. inermisD. minorD. moluccensisD. pannietensisD. peroniD. praedatrixD. viridis

Dyacopterus [Genus]D. spadiceus [Species]

Eidolon [Genus]E. dupreanum [Species]E. helvum

Eonycteris [Genus]E. major [Species]E. spelaea

Epomophorus [Genus]E. angolensis [Species]E. gambianusE. grandisE. labiatusE. minimusE. wahlbergi

Epomops [Genus]E. buettikoferi [Species]E. dobsoniE. franqueti

Haplonycteris [Genus]H. fischeri [Species]

Harpyionycteris [Genus]H. celebensis [Species]H. whiteheadi

Hypsignathus [Genus]H. monstrosus [Species]

Latidens [Genus]L. salimalii [Species]

Macroglossus [Genus]M. minimus [Species]M. sobrinus

Megaerops [Genus]M. ecaudatus [Species]M. kusnotoiM. niphanaeM. wetmorei

Megaloglossus [Genus]M. woermanni [Species]

Melonycteris [Genus]M. aurantius [Species]M. melanopsM. woodfordi

Micropteropus [Genus]M. intermedius [Species]M. pusillus

Myonycteris [Genus]M. brachycephala [Species]M. relictaM. torquata

Nanonycteris [Genus]N. veldkampi [Species]

Neopteryx [Genus]N. frosti [Species]

Notopteris [Genus]N. macdonaldi [Species]

Nyctimene [Genus]N. aello [Species]N. albiventerN. celaenoN. cephalotesN. certansN. cyclotisN. draconillaN. majorN. malaitensisN. masalaiN. minutusN. raboriN. robinsoniN. sanctacrucisN. vizcaccia

Otopteropus [Genus]O. cartilagonodus [Species]

Paranyctimene [Genus]P. raptor [Species]

Penthetor [Genus]P. lucasi [Species]

Plerotes [Genus]P. anchietai [Species]

Ptenochirus [Genus]P. jagori [Species]P. minor

Pteralopex [Genus]P. acrodonta [Species]P. ancepsP. atrataP. pulchra

Pteropus [Genus]P. admiralitatum [Species]P. aldabrensisP. alectoP. anetianusP. argentatusP. brunneusP. canicepsP. chrysoproctusP. conspicillatusP. dasymallusP. faunulusP. fundatusP. giganteusP. gilliardiP. griseusP. howensisP. hypomelanusP. insularisP. leucopterusP. livingstoneiP. lombocensis

P. lyleiP. macrotisP. mahaganusP. mariannusP. mearnsiP. melanopogonP. melanotusP. molossinusP. neohibernicusP. nigerP. nitendiensisP. ocularisP. ornatusP. personatusP. phaeocephalusP. pilosusP. pohleiP. poliocephalusP. pselaphonP. pumilusP. rayneriP. rodricensisP. rufusP. samoensisP. sanctacrucisP. scapulatusP. seychellensisP. speciosusP. subnigerP. temminckiP. tokudaeP. tonganusP. tuberculatusP. vampyrusP. vetulusP. voeltzkowiP. woodfordi

Rousettus [Genus]R. aegyptiacus [Species]R. amplexicaudatusR. angolensisR. celebensisR. lanosusR. leschenaultiR. madagascariensisR. obliviosusR. spinalatus

Scotonycteris [Genus]S. ophiodon [Species]S. zenkeri

Sphaerias [Genus]S. blanfordi [Species]

Styloctenium [Genus]S. wallacei [Species]

Syconycteris [Genus]S. australis [Species]S. carolinaeS. hobbit

Thoopterus [Genus]T. nigrescens [Species]



Rhinopomatidae [Family]Rhinopoma [Genus]

R. hardwickei [Species]R. microphyllumR. muscatellum

Emballonuridae [Family]Balantiopteryx [Genus]

B. infusca [Species]B. ioB. plicata

Centronycteris [Genus]C. maximiliani [Species]

Coleura [Genus]C. afra [Species]C. seychellensis

Cormura [Genus]C. brevirostris [Species]

Cyttarops [Genus]C. alecto [Species]

Diclidurus [Genus]D. albus [Species]D. ingensD. isabellusD. scutatus

Emballonura [Genus]E. alecto [Species]E. atrataE. beccariiE. dianaeE. furaxE. monticolaE. raffrayanaE. semicaudata

Mosia [Genus]M. nigrescens [Species]

Peropteryx [Genus]P. kappleri [Species]P. leucopteraP. macrotis

Rhynchonycteris [Genus]R. naso [Species]

Saccolaimus [Genus]S. flaviventris [Species]S. mixtusS. peliS. plutoS. saccolaimus

Saccopteryx [Genus]S. bilineata [Species]S. canescensS. gymnuraS. leptura

Taphozous [Genus]T. australis [Species]T. georgianusT. hamiltoniT. hildegardeaeT. hilliT. kapalgensisT. longimanus

T. mauritianusT. melanopogonT. nudiventrisT. perforatusT. philippinensisT. theobaldi

Craseonycteridae [Family]Craseonycteris [Genus]

C. thonglongyai [Species]

Nycteridae [Family]Nycteris [Genus]

N. arge [Species]N. gambiensisN. grandisN. hispidaN. intermediaN. javanicaN. macrotisN. majorN. nanaN. thebaicaN. tragataN. woodi

Megadermatidae [Family]Cardioderma [Genus]

C. cor [Species]Lavia [Genus]

L. frons [Species]Macroderma [Genus]

M. gigas [Species]Megaderma [Genus]

M. lyra [Species]M. spasma

Rhinolophidae [Family]Rhinolophus [Genus]

R. acuminatus [Species]R. adamiR. affinisR. alcyoneR. anderseniR. arcuatusR. blasiiR. borneensisR. canutiR. capensisR. celebensisR. clivosusR. coelophyllusR. cognatusR. cornutusR. creaghiR. darlingiR. deckeniiR. dentiR. eloquensR. euryaleR. euryotis

R. ferrumequinumR. fumigatusR. guineensisR. hildebrandtiR. hipposiderosR. imaizumiiR. inopsR. keyensisR. landeriR. lepidusR. luctusR. maclaudiR. macrotisR. malayanusR. marshalliR. megaphyllusR. mehelyiR. mitratusR. monocerosR. nereisR. osgoodiR. paradoxolophusR. pearsoniR. philippinensisR. pusillusR. rexR. robinsoniR. rouxiR. rufusR. sedulusR. shameliR. silvestrisR. simplexR. simulatorR. sthenoR. subbadiusR. subrufusR. swinnyiR. thomasiR. trifoliatusR. virgoR. yunanensis

Hipposideridae [Family]Anthops [Genus]

A. ornatus [Species]Asellia [Genus]

A. patrizii [Species]A. tridens

Aselliscus [Genus]A. stoliczkanus [Species]A. tricuspidatus

Cloeotis [Genus]C. percivali [Species]

Coelops [Genus]C. frithi [Species]C. hirsutusC. robinsoni

Hipposideros [Genus]H. abae [Species]H. armiger



AM

MA

LSSP

EC

IES

LIST

H. aterH. beatusH. bicolorH. brevicepsH. cafferH. calcaratusH. camerunensisH. cervinusH. cineraceusH. commersoniH. coronatusH. corynophyllusH. coxiH. crumeniferusH. curtusH. cyclopsH. diademaH. dinopsH. doriaeH. dyacorumH. fuliginosusH. fulvusH. galeritusH. halophyllusH. inexpectatusH. jonesiH. lamotteiH. lankadivaH. larvatusH. lekaguliH. lyleiH. macrobullatusH. maggietayloraeH. marisaeH. megalotisH. muscinusH. nequamH. obscurusH. papuaH. pomonaH. prattiH. pygmaeusH. ridleyiH. ruberH. sabanusH. schistaceusH. semoniH. speorisH. stenotisH. turpisH. wollastoni

Paracoelops [Genus]P. megalotis [Species]

Rhinonicteris [Genus]R. aurantia [Species]

Triaenops [Genus]T. furculus [Species]T. persicus

Phyllostomidae [Family]Ametrida [Genus]

A. centurio [Species]Anoura [Genus]

A. caudifer [Species]A. cultrataA. geoffroyiA. latidens

Ardops [Genus]A. nichollsi [Species]

Ariteus [Genus]A. flavescens [Species]

Artibeus [Genus]A. amplus [Species]A. anderseniA. aztecusA. cinereusA. concolorA. fimbriatusA. fraterculusA. glaucusA. hartiiA. hirsutusA. inopinatusA. jamaicensisA. lituratusA. obscurusA. phaeotisA. planirostrisA. toltecus

Brachyphylla [Genus]B. cavernarum [Species]B. nana

Carollia [Genus]C. brevicauda [Species]C. castaneaC. perspicillataC. subrufa

Centurio [Genus]C. senex [Species]

Chiroderma [Genus]C. doriae [Species]C. improvisumC. salviniC. trinitatumC. villosum

Choeroniscus [Genus]C. godmani [Species]C. intermediusC. minorC. periosus

Choeronycteris [Genus]C. mexicana [Species]

Chrotopterus [Genus]C. auritus [Species]

Desmodus [Genus]D. rotundus [Species]

Diaemus [Genus]D. youngi [Species]

Diphylla [Genus]D. ecaudata [Species]

Ectophylla [Genus]

E. alba [Species]Erophylla [Genus]

E. sezekorni [Species]Glossophaga [Genus]

G. commissarisi [Species]G. leachiiG. longirostrisG. morenoiG. soricina

Hylonycteris [Genus]H. underwoodi [Species]

Leptonycteris [Genus]L. curasoae [Species]L. nivalis

Lichonycteris [Genus]L. obscura [Species]

Lionycteris [Genus]L. spurrelli [Species]

Lonchophylla [Genus]L. bokermanni [Species]L. dekeyseriL. handleyiL. hesperiaL. mordaxL. robustaL. thomasi

Lonchorhina [Genus]L. aurita [Species]L. fernandeziL. marinkelleiL. orinocensis

Macrophyllum [Genus]M. macrophyllum [Species]

Macrotus [Genus]M. californicus [Species]M. waterhousii

Mesophylla [Genus]M. macconnelli [Species]

Micronycteris [Genus]M. behnii [Species]M. brachyotisM. daviesiM. hirsutaM. megalotisM. minutaM. niceforiM. pusillaM. schmidtorumM. sylvestris

Mimon [Genus]M. bennettii [Species]M. crenulatum

Monophyllus [Genus]M. plethodon [Species]M. redmani

Musonycteris [Genus]M. harrisoni [Species]

Phylloderma [Genus]P. stenops [Species]

Phyllonycteris [Genus]



P. aphylla [Species]P. poeyi

Phyllops [Genus]P. falcatus [Species]

Phyllostomus [Genus]P. discolor [Species]P. elongatusP. hastatusP. latifolius

Platalina [Genus]P. genovensium [Species]

Platyrrhinus [Genus]P. aurarius [Species]P. brachycephalusP. chocoensisP. dorsalisP. helleriP. infuscusP. lineatusP. recifinusP. umbratusP. vittatus

Pygoderma [Genus]P. bilabiatum [Species]

Rhinophylla [Genus]R. alethina [Species]R. fischeraeR. pumilio

Scleronycteris [Genus]S. ega [Species]

Sphaeronycteris [Genus]S. toxophyllum [Species]

Stenoderma [Genus]S. rufum [Species]

Sturnira [Genus]S. aratathomasi [Species]S. bidensS. bogotensisS. erythromosS. liliumS. ludoviciS. luisiS. magnaS. mordaxS. nanaS. thomasiS. tildae

Tonatia [Genus]T. bidens [Species]T. brasilienseT. carrikeriT. evotisT. schulziT. silvicola

Trachops [Genus]T. cirrhosus [Species]

Uroderma [Genus]U. bilobatum [Species]U. magnirostrum

Vampyressa [Genus]

V. bidens [Species]V. brockiV. melissaV. nymphaeaV. pusilla

Vampyrodes [Genus]V. caraccioli [Species]

Vampyrum [Genus]V. spectrum [Species]

Mormoopidae [Family]Mormoops [Genus]

M. blainvillii [Species]M. megalophylla

Pteronotus [Genus]P. davyi [Species]P. gymnonotusP. macleayiiP. parnelliiP. personatusP. quadridens

Noctilionidae [Family]Noctilio [Genus]

N. albiventris [Species]N. leporinus

Mystacinidae [Family]Mystacina [Genus]

M. robusta [Species]M. tuberculata

Natalidae [Family]Natalus [Genus]

N. lepidus [Species]N. micropusN. stramineusN. tumidifronsN. tumidirostris

Furipteridae [Family]Amorphochilus [Genus]

A. schnablii [Species]Furipterus [Genus]

F. horrens [Species]

Thyropteridae [Family]Thyroptera [Genus]

T. discifera [Species]T. tricolor

Myzopodidae [Family]Myzopoda [Genus]

M. aurita [Species]

Molossidae [Family]Chaerephon [Genus]

C. aloysiisabaudiae [Species]C. ansorgeiC. bemmeleniC. bivittataC. chapiniC. gallagheri

C. jobensisC. johorensisC. majorC. nigeriaeC. plicataC. pumilaC. russata

Cheiromeles [Genus]C. torquatus [Species]

Eumops [Genus]E. auripendulus [Species]E. bonariensisE. dabbeneiE. glaucinusE. hansaeE. maurusE. perotisE. underwoodi

Molossops [Genus]M. abrasus [Species]M. aequatorianusM. greenhalliM. mattogrossensisM. neglectusM. planirostrisM. temminckii

Molossus [Genus]M. ater [Species]M. bondaeM. molossusM. pretiosusM. sinaloae

Mops [Genus]M. brachypterus [Species]M. condylurusM. congicusM. demonstratorM. midasM. mopsM. nanulusM. niangaraeM. niveiventerM. petersoniM. sarasinorumM. spurrelliM. thersitesM. trevori

Mormopterus [Genus]M. acetabulosus [Species]M. beccariiM. doriaeM. jugularisM. kalinowskiiM. minutusM. norfolkensisM. petrophilusM. phrudusM. planicepsM. setiger

Myopterus [Genus]



AM

MA

LSSP

EC

IES

LIST

M. daubentonii [Species]M. whitleyi

Nyctinomops [Genus]N. aurispinosus [Species]N. femorosaccusN. laticaudatusN. macrotis

Otomops [Genus]O. formosus [Species]O. martiensseniO. papuensisO. secundusO. wroughtoni

Promops [Genus]P. centralis [Species]P. nasutus

Tadarida [Genus]T. aegyptiaca [Species]T. australisT. brasiliensisT. espiritosantensisT. fulminansT. lobataT. teniotisT. ventralis

Vespertilionidae [Family]Antrozous [Genus]

A. dubiaquercus [Species]A. pallidus

Barbastella [Genus]B. barbastellus [Species]B. leucomelas

Chalinolobus [Genus]C. alboguttatus [Species]C. argentatusC. beatrixC. dwyeriC. egeriaC. gleniC. gouldiiC. kenyacolaC. morioC. nigrogriseusC. picatusC. poensisC. superbusC. tuberculatusC. variegatus

Eptesicus [Genus]E. baverstocki [Species]E. bobrinskoiE. bottaeE. brasiliensisE. brunneusE. capensisE. demissusE. diminutusE. douglasorumE. flavescensE. floweri

E. furinalisE. fuscusE. guadeloupensisE. guineensisE. hottentotusE. innoxiusE. kobayashiiE. melckorumE. nasutusE. nilssoniE. pachyotisE. platyopsE. pumilusE. regulusE. rendalliE. sagittulaE. serotinusE. somalicusE. tateiE. tenuipinnisE. vulturnus

Euderma [Genus]E. maculatum [Species]

Eudiscopus [Genus]E. denticulus [Species]

Glischropus [Genus]G. javanus [Species]G. tylopus

Harpiocephalus [Genus]H. harpia [Species]

Hesperoptenus [Genus]H. blanfordi [Species]H. doriaeH. gaskelliH. tickelliH. tomesi

Histiotus [Genus]H. alienus [Species]H. macrotusH. montanusH. velatus

Ia [Genus]I. io [Species]

Idionycteris [Genus]I. phyllotis [Species]

Kerivoula [Genus]K. aerosa [Species]K. africanaK. agnellaK. argentataK. atroxK. cuprosaK. eriophoraK. floraK. hardwickeiK. intermediaK. jagoriK. lanosaK. minutaK. muscina

K. myrellaK. papillosaK. papuensisK. pellucidaK. phalaenaK. pictaK. smithiK. whiteheadi

Laephotis [Genus]L. angolensis [Species]L. botswanaeL. namibensisL. wintoni

Lasionycteris [Genus]L. noctivagans [Species]

Lasiurus [Genus]L. borealis [Species]L. castaneusL. cinereusL. egaL. egregiusL. intermediusL. seminolus

Mimetillus [Genus]M. moloneyi [Species]

Miniopterus [Genus]M. australis [Species]M. fraterculusM. fuscusM. inflatusM. magnaterM. minorM. pusillusM. robustiorM. schreibersiM. tristis

Murina [Genus]M. aenea [Species]M. aurataM. cyclotisM. floriumM. fuscaM. griseaM. huttoniM. leucogasterM. putaM. rozendaaliM. silvaticaM. suillaM. tenebrosaM. tubinarisM. ussuriensis

Myotis [Genus]M. abei [Species]M. adversusM. aelleniM. albescensM. altariumM. annectansM. atacamensis



M. auriculusM. australisM. austroripariusM. bechsteiniM. blythiiM. bocageiM. bombinusM. brandtiM. californicusM. capacciniiM. chiloensisM. chinensisM. cobanensisM. dasycnemeM. daubentoniM. dominicensisM. elegansM. emarginatusM. evotisM. findleyiM. formosusM. fortidensM. fraterM. goudotiM. grisescensM. hasseltiiM. horsfieldiiM. hosonoiM. ikonnikoviM. insularumM. keaysiM. keeniiM. leibiiM. lesueuriM. levisM. longipesM. lucifugusM. macrodactylusM. macrotarsusM. martiniquensisM. milleriM. montivagusM. morrisiM. muricolaM. myotisM. mystacinusM. nattereriM. nesopolusM. nigricansM. oreiasM. oxyotusM. ozensisM. peninsularisM. pequiniusM. planicepsM. pruinosusM. rickettiM. ridleyiM. ripariusM. rosseti

M. ruberM. schaubiM. scottiM. seabraiM. sicariusM. siligorensisM. simusM. sodalisM. stalkeriM. thysanodesM. tricolorM. veliferM. vivesiM. volansM. welwitschiiM. yesoensisM. yumanensis

Nyctalus [Genus]N. aviator [Species]N. azoreumN. lasiopterusN. leisleriN. montanusN. noctula

Nycticeius [Genus]N. balstoni [Species]N. greyiiN. humeralisN. rueppelliiN. sanborniN. schlieffeni

Nyctophilus [Genus]N. arnhemensis [Species]N. geoffroyiN. gouldiN. heranN. microdonN. microtisN. timoriensisN. walkeri

Otonycteris [Genus]O. hemprichi [Species]

Pharotis [Genus]P. imogene [Species]

Philetor [Genus]P. brachypterus [Species]

Pipistrellus [Genus]P. aegyptius [Species]P. aeroP. affinisP. anchietaiP. anthonyiP. arabicusP. arielP. babuP. bodenheimeriP. cadornaeP. ceylonicusP. circumdatusP. coromandra

P. crassulusP. cuprosusP. dormeriP. eisentrautiP. endoiP. hesperusP. imbricatusP. inexspectatusP. javanicusP. joffreiP. kitcheneriP. kuhliiP. lophurusP. macrotisP. maderensisP. mimusP. minahassaeP. mordaxP. musciculusP. nanulusP. nanusP. nathusiiP. paterculusP. peguensisP. permixtusP. petersiP. pipistrellusP. pulveratusP. rueppelliP. rusticusP. saviiP. societatisP. stenopterusP. sturdeeiP. subflavusP. tasmaniensisP. tenuis

Plecotus [Genus]P. auritus [Species]P. austriacusP. mexicanusP. rafinesquiiP. taivanusP. teneriffaeP. townsendii

Rhogeessa [Genus]R. alleni [Species]R. genowaysiR. gracilisR. minutillaR. miraR. parvulaR. tumida

Scotoecus [Genus]S. albofuscus [Species]S. hirundoS. pallidus

Scotomanes [Genus]S. emarginatus [Species]S. ornatus



AM

MA

LSSP

EC

IES

LIST

Scotophilus [Genus]S. borbonicus [Species]S. celebensisS. dinganiiS. heathiS. kuhliiS. leucogasterS. nigritaS. nuxS. robustusS. viridis

Tomopeas [Genus]T. ravus [Species]

Tylonycteris [Genus]T. pachypus [Species]T. robustula

Vespertilio [Genus]V. murinus [Species]V. superans

Primates [Order]

Lorisidae [Family]Arctocebus [Genus]

A. aureus [Species]A. calabarensis

Loris [Genus]L. tardigradus [Species]

Nycticebus [Genus]N. coucang [Species]N. pygmaeus

Perodicticus [Genus]P. potto [Species]

Galagidae [Family]Euoticus [Genus]

E. elegantulus [Species]E. pallidus

Galago [Genus]G. alleni [Species]G. gallarumG. matschieiG. moholiG. senegalensis

Galagoides [Genus]G. demidoff [Species]G. zanzibaricus

Otolemur [Genus]O. crassicaudatus [Species]O. garnettii

Cheirogaleidae [Family]Allocebus [Genus]

A. trichotis [Species]Cheirogaleus [Genus]

C. major [Species]C. medius

Microcebus [Genus]Microcebus coquereli [Species]Microcebus murinusMicrocebus rufus

Phaner [Genus]P. furcifer [Species]

Lemuridae [Family]Eulemur [Genus]

E. coronatus [Species]E. fulvusE. macacoE. mongozE. rubriventer

Hapalemur [Genus]H. aureus [Species]H. griseusH. simus

Lemur [Genus]L. catta [Species]

Varecia [Genus]V. variegata [Species]

Indriidae [Family]Avahi [Genus]

A. laniger [Species]Indri [Genus]

I. indri [Species]Propithecus [Genus]

P. diadema [Species]P. tattersalliP. verreauxi

Lepilemuridae [Family]Lepilemur [Genus]

L. dorsalis [Species]L. edwardsiL. leucopusL. microdonL. mustelinusL. ruficaudatusL. septentrionalis

Daubentoniidae [Family]Daubentonia [Genus]

D. madagascariensis [Species]

Tarsiidae [Family]Tarsius [Genus]

T. bancanus [Species]T. dianaeT. pumilusT. spectrumT. syrichta

Cebidae [Family]Alouatta [Genus]

A. belzebul [Species]A. carayaA. coibensisA. fuscaA. palliataA. pigraA. saraA. seniculus

Callicebus [Genus]

C. brunneus [Species]C. caligatusC. cinerascensC. cupreusC. donacophilusC. dubiusC. hoffmannsiC. modestusC. molochC. oenantheC. olallaeC. personatusC. torquatus

Cebus [Genus]C. albifrons [Species]C. apellaC. capucinusC. olivaceus

Saimiri [Genus]S. boliviensis [Species]S. oerstediiS. sciureusS. ustusS. vanzolinii

Callitrichidae [Family]Callimico [Genus]

C. goeldii [Species]Callithrix [Genus]

C. argentata [Species]C. auritaC. flavicepsC. geoffroyiC. humeraliferC. jacchusC. kuhliiC. penicillataC. pygmaea

Leontopithecus [Genus]L. caissara [Species]L. chrysomelaL. chrysopygusL. rosalia

Saguinus [Genus]S. bicolor [Species]S. fuscicollisS. geoffroyiS. imperatorS. inustusS. labiatusS. leucopusS. midasS. mystaxS. nigricollisS. oedipusS. tripartitus

Aotidae [Family]Aotus [Genus]

A. azarai [Species]A. brumbacki



A. hershkovitziA. infulatusA. lemurinusA. miconaxA. nancymaaeA. nigricepsA. trivirgatusA. vociferans

Pitheciidae [Family]Cacajao [Genus]

C. calvus [Species]C. melanocephalus

Chiropotes [Genus]C. albinasus [Species]C. satanas

Pithecia [Genus]P. aequatorialis [Species]P. albicansP. irrorataP. monachusP. pithecia

Atelidae [Family]Ateles [Genus]

A. belzebuth [Species]A. chamekA. fuscicepsA. geoffroyiA. marginatusA. paniscus

Brachyteles [Genus]B. arachnoides [Species]

Lagothrix [Genus]L. flavicauda [Species]L. lagotricha

Cercopithecidae [Family]Allenopithecus [Genus]

A. nigroviridis [Species]Cercocebus [Genus]

C. agilis [Species]C. galeritusC. torquatus

Cercopithecus [Genus]C. ascanius [Species]C. campbelliC. cephusC. dianaC. dryasC. erythrogasterC. erythrotisC. hamlyniC. lhoestiC. mitisC. monaC. neglectusC. nictitansC. petauristaC. pogoniasC. preussiC. sclateri

C. solatusC. wolfi

Chlorocebus [Genus]C. aethiops [Species]

Colobus [Genus]C. angolensis [Species]C. guerezaC. polykomosC. satanas

Erythrocebus [Genus]E. patas [Species]

Lophocebus [Genus]L. albigena [Species]

Macaca [Genus]M. arctoides [Species]M. assamensisM. cyclopisM. fascicularisM. fuscataM. mauraM. mulattaM. nemestrinaM. nigraM. ochreataM. radiataM. silenusM. sinicaM. sylvanusM. thibetanaM. tonkeana

Mandrillus [Genus]M. leucophaeus [Species]M. sphinxMiopithecusM. talapoin

Nasalis [Genus]N. concolor [Species]N. larvatus

Papio [Genus]P. hamadryas [Species]

Presbytis [Genus]P. comata [Species]P. femoralisP. frontataP. hoseiP. melalophosP. potenzianiP. rubicundaP. thomasi

Procolobus [Genus]P. badius [Species]P. pennantiiP. preussiP. rufomitratusP. verus

Pygathrix [Genus]P. avunculus [Species]P. bietiP. brelichiP. nemaeus

P. roxellanaSemnopithecus [Genus]

S. entellus [Species]Theropithecus [Genus]

T. gelada [Species]Trachypithecus [Genus]

T. auratus [Species]T. cristatusT. francoisiT. geeiT. johniiT. obscurusT. phayreiT. pileatusT. vetulus

Hylobatidae [Family]Hylobates [Genus]

H. agilis [Species]H. concolorH. gabriellaeH. hoolockH. klossiiH. larH. leucogenysH. molochH. muelleriH. pileatusH. syndactylus

Hominidae [Family]Gorilla [Genus]

G. gorilla [Species]Homo [Genus]

H. sapiens [Species]Pan [Genus]

P. paniscus [Species]P. troglodytes

Pongo [Genus]P. pygmaeus [Species]

Carnivora [Order]

Canidae [Family]Alopex [Genus]

A. lagopus [Species]AtelocynusA. microtis

Canis [Genus]C. adustus [Species]C. aureusC. latransC. lupusC. mesomelasC. rufusC. simensis

Cerdocyon [Genus]C. thous [Species]

Chrysocyon [Genus]C. brachyurus [Species]

Cuon [Genus]



AM

MA

LSSP

EC

IES

LIST

C. alpinus [Species]Dusicyon [Genus]

D. australis [Species]Lycaon [Genus]

L. pictus [Species]Nyctereutes [Genus]

N. procyonoides [Species]Otocyon [Genus]

O. megalotis [Species]Pseudalopex [Genus]

P. culpaeus [Species]P. griseusP. gymnocercusP. sechuraeP. vetulus

Speothos [Genus]S. venaticus [Species]

Urocyon [Genus]U. cinereoargenteus [Species]U. littoralis

Vulpes [Genus]V. bengalensis [Species]V. canaV. chamaV. corsacV. ferrilataV. pallidaV. rueppelliV. veloxV. vulpesV. zerda

Ursidae [Family]Ailuropoda [Genus]

A. melanoleuca [Species]Ailurus [Genus]

A. fulgens [Species]Helarctos [Genus]

H. malayanus [Species]Melursus [Genus]

M. ursinus [Species]Tremarctos [Genus]

T. ornatus [Species]Ursus [Genus]

U. americanus [Species]U. arctosU. maritimusU. thibetanus

Procyonidae [Family]Bassaricyon [Genus]

B. alleni [Species]B. beddardiB. gabbiiB. lasiusB. pauli

Potos [Genus]P. flavus [Species]

Bassariscus [Genus]B. astutus [Species]B. sumichrasti

Nasua [Genus]N. narica [Species]N. nasua

Nasuella [Genus]N. olivacea [Species]

Procyon [Genus]P. cancrivorus [Species]P. gloveralleniP. insularisP. lotorP. maynardiP. minorP. pygmaeus

Mustelidae [Family]Amblonyx [Genus]

A. cinereus [Species]Aonyx [Genus]

A. capensis [Species]A. congicus

Arctonyx [Genus]A. collaris [Species]

Conepatus [Genus]C. chinga [Species]C. humboldtiiC. leuconotusC. mesoleucusC. semistriatus

Eira [Genus]E. barbara [Species]

Enhydra [Genus]E. lutris [Species]

Galictis [Genus]G. cuja [Species]G. vittata

Gulo [Genus]G. gulo [Species]

Ictonyx [Genus]I. libyca [Species]I. striatus

Lontra [Genus]L. canadensis [Species]L. felinaL. longicaudisL. provocax

Lutra [Genus]L. lutra [Species]L. maculicollisL. sumatrana

Lutrogale [Genus]L. perspicillata [Species]

Lyncodon [Genus]L. patagonicus [Species]

Martes [Genus]M. americana [Species]M. flavigulaM. foinaM. gwatkinsiiM. martesM. melampusM. pennanti

M. zibellinaMeles [Genus]

M. meles [Species]Mellivora [Genus]

M. capensis [Species]Melogale [Genus]

M. everetti [Species]M. moschataM. orientalisM. personata

Mephitis [Genus]M. macroura [Species]M. mephitis

Mustela [Genus]M. africana [Species]M. altaicaM. ermineaM. eversmanniiM. felipeiM. frenataM. kathiahM. lutreolaM. lutreolinaM. nigripesM. nivalisM. nudipesM. putoriusM. sibiricaM. strigidorsaM. vison

Mydaus [Genus]M. javanensis [Species]M. marchei

Poecilogale [Genus]P. albinucha [Species]

Pteronura [Genus]P. brasiliensis [Species]

Spilogale [Genus]S. putorius [Species]S. pygmaea

Taxidea [Genus]T. taxus [Species]

Vormela [Genus]V. peregusna [Species]

Viverridae [Family]Arctictis [Genus]

A. binturong [Species]Arctogalidia [Genus]

A. trivirgata [Species]Chrotogale [Genus]

C. owstoni [Species]Civettictis [Genus]

C. civetta [Species]Cryptoprocta [Genus]

C. ferox [Species]Cynogale [Genus]

C. bennettii [Species]Diplogale [Genus]

D. hosei [Species]Eupleres [Genus]



E. goudotii [Species]Fossa [Genus]

F. fossana [Species]Genetta [Genus]

G. abyssinica [Species]G. angolensisG. genettaG. johnstoniG. maculataG. servalinaG. thierryiG. tigrinaG. victoriae

Hemigalus [Genus]H. derbyanus [Species]

Nandinia [Genus]N. binotata [Species]

Macrogalidia [Genus]M. musschenbroekii [Species]

Paguma [Genus]P. larvata [Species]

Paradoxurus [Genus]P. hermaphroditus [Species]P. jerdoniP. zeylonensis

Osbornictis [Genus]O. piscivora [Species]

Poiana [Genus]P. richardsonii [Species]

Prionodon [Genus]P. linsang [Species]P. pardicolor

Viverra [Genus]V. civettina [Species]V. megaspilaV. tangalungaV. zibetha

Viverricula [Genus]V. indica [Species]

Herpestidae [Family]Atilax [Genus]

A. paludinosus [Species]Bdeogale [Genus]

B. crassicauda [Species]B. jacksoniB. nigripes

Crossarchus [Genus]C. alexandri [Species]C. ansorgeiC. obscurus

Cynictis [Genus]C. penicillata [Species]

Dologale [Genus]D. dybowskii [Species]

Galerella [Genus]G. flavescens [Species]G. pulverulentaG. sanguineaG. swalius

Galidia [Genus]

G. elegans [Species]Galidictis [Genus]

G. fasciata [Species]G. grandidieri

Helogale [Genus]H. hirtula [Species]H. parvula

Herpestes [Genus]H. brachyurus [Species]H. edwardsiiH. ichneumonH. javanicusH. nasoH. palustrisH. semitorquatusH. smithiiH. urvaH. vitticollis

Ichneumia [Genus]I. albicauda [Species]

Liberiictis [Genus]L. kuhni [Species]

Mungos [Genus]M. gambianus [Species]M. mungo

Mungotictis [Genus]M. decemlineata [Species]

Paracynictis [Genus]P. selousi [Species]

Rhynchogale [Genus]R. melleri [Species]

Salanoia [Genus]S. concolor [Species]

Suricata [Genus]S. suricatta [Species]

Hyaenidae [Family]Crocuta [Genus]

C. crocuta [Species]Hyaena [Genus]

H. hyaena [Species]Parahyaena [Genus]

P. brunnea [Species]Proteles [Genus]

P. cristatus [Species]

Felidae [Family]Acinonyx [Genus]

A. jubatus [Species]Caracal [Genus]

C. caracal [Species]Catopuma [Genus]

C. badia [Species]C. temminckii

Felis [Genus]F. bieti [Species]F. chausF. margaritaF. nigripesF. silvestris

Herpailurus [Genus]H. yaguarondi [Species]

Leopardus [Genus]L. pardalis [Species]L. tigrinusL. wiedii

Leptailurus [Genus]L. serval [Species]

Lynx [Genus]L. canadensis [Species]L. lynxL. pardinusL. rufus

Neofelis [Genus]N. nebulosa [Species]

Oncifelis [Genus]O. colocolo [Species]O. geoffroyiO. guigna

Oreailurus [Genus]O. jacobita [Species]

Otocolobus [Genus]O. manul [Species]

Panthera [Genus]P. leo [Species]P. oncaP. pardusP. tigrisPardofelisP. marmorata

Prionailurus [Genus]P. bengalensis [Species]P. planicepsP. rubiginosusP. viverrinus

Profelis [Genus]P. aurata [Species]

Puma [Genus]P. concolor [Species]

Uncia [Genus]U. uncia [Species]

Otariidae [Family]Arctocephalus [Genus]

A. australis [Species]A. forsteriA. galapagoensisA. gazellaA. philippiiA. pusillusA. townsendiA. tropicalis

Callorhinus [Genus]C. ursinus [Species]

Eumetopias [Genus]E. jubatus [Species]

Neophoca [Genus]N. cinerea [Species]

Otaria [Genus]O. byronia [Species]



AM

MA

LSSP

EC

IES

LIST

Phocarctos [Genus]P. hookeri [Species]

Zalophus [Genus]Z. californianus [Species]

Odobenidae [Family]Odobenus [Genus]

O. rosmarus [Species]

Phocidae [Family]Cystophora [Genus]

C. cristata [Species]Erignathus [Genus]

E. barbatus [Species]Halichoerus [Genus]

H. grypus [Species]Hydrurga [Genus]

H. leptonyx [Species]Leptonychotes [Genus]

L. weddellii [Species]Lobodon [Genus]

L. carcinophagus [Species]Mirounga [Genus]

M. angustirostris [Species]M. leonina

Monachus [Genus]M. monachus [Species]M. schauinslandiM. tropicalis

Ommatophoca [Genus]O. rossii [Species]

Phoca [Genus]P. caspica [Species]P. fasciataP. groenlandicaP. hispidaP. larghaP. sibiricaP. vitulina

Cetacea [Order]

Platanistidae [Family]Platanista [Genus]

P. gangetica [Species]P. minor

Lipotidae [Family]Lipotes [Genus]

L. vexillifer [Species]

Pontoporiidae [Family]Pontoporia [Genus]

P. blainvillei [Species]

Iniidae [Family]Inia [Genus]

I. geoffrensis [Species]

Phocoenidae [Family]Australophocaena [Genus]

A. dioptrica [Species]Neophocaena [Genus]

N. phocaenoides [Species]Phocoena [Genus]

P. phocoena [Species]P. sinusP. spinipinnis

Phocoenoides [Genus]P. dalli [Species]

Delphinidae [Family]Cephalorhynchus [Genus]

C. commersonii [Species]C. eutropiaC. heavisidiiC. hectori

Delphinus [Genus]D. delphis [Species]

Feresa [Genus]F. attenuata [Species]

Globicephala [Genus]G. macrorhynchus [Species]G. melas

Grampus [Genus]G. griseus [Species]

Lagenodelphis [Genus]L. hosei [Species]

Lagenorhynchus [Genus]L. acutus [Species]L. albirostrisL. australisL. crucigerL. obliquidensL. obscurus

Lissodelphis [Genus]L. borealis [Species]L. peronii

Orcaella [Genus]O. brevirostris [Species]

Orcinus [Genus]O. orca [Species]

Peponocephala [Genus]P. electra [Species]

Pseudorca [Genus]P. crassidens [Species]

Sotalia [Genus]S. fluviatilis [Species]

Sousa [Genus]S. chinensis [Species]S. teuszii

Stenella [Genus]S. attenuata [Species]S. clymeneS. coeruleoalbaS. frontalisS. longirostris

Steno [Genus]S. bredanensis [Species]

Tursiops [Genus]T. truncatus [Species]

Ziphiidae [Family]Berardius [Genus]

B. arnuxii [Species]B. bairdii

Hyperoodon [Genus]H. ampullatus [Species]H. planifrons

Indopacetus [Genus]I. pacificus [Species]

Mesoplodon [Genus]M. bidens [Species]M. bowdoiniM. carlhubbsiM. densirostrisM. europaeusM. ginkgodensM. grayiM. hectoriM. layardiiM. mirusM. peruvianusM. stejnegeri

Tasmacetus [Genus]T. shepherdi [Species]

Ziphius [Genus]Z. cavirostris [Species]

Physeteridae [Family]Kogia [Genus]

K. breviceps [Species]K. simus

Physeter [Genus]P. catodon [Species]

Monodontidae [Family]Delphinapterus [Genus]

D. leucas [Species]Monodon [Genus]

M. monoceros [Species]

Eschrichtiidae [Family]Eschrichtius [Genus]

E. robustus [Species]

Neobalaenidae [Family]Caperea [Genus]

C. marginata [Species]

Balaenidae [Family]Balaena [Genus]

B. mysticetus [Species]Eubalaena [Genus]

E. australis [Species]E. glacialis

Balaenopteridae [Family]Balaenoptera [Genus]

B. acutorostrata [Species]B. borealisB. edeniB. musculusB. physalus

Megaptera [Genus]M. novaeangliae [Species]



Tubulidentata [Order]

Orycteropodidae [Family]Orycteropus [Genus]

O. afer [Species]

Proboscidea [Order]

Elephantidae [Family]Elephas [Genus]

E. maximus [Species]Loxodonta [Genus]

L. africana [Species]L. cyclotis

Hyracoidea [Order]

Procaviidae [Family]Dendrohyrax [Genus]

D. arboreus [Species]D. dorsalisD. validus

Heterohyrax [Genus]H. antineae [Species]H. brucei

Procavia [Genus]P. capensis [Species]

Sirenia [Order]

Dugongidae [Family]Dugong [Genus]

D. dugon [Species]Hydrodamalis [Genus]

H. gigas [Species]

Trichechidae [Family]Trichechus [Genus]

T. inunguis [Species]T. manatusT. senegalensis

Perissodactyla [Order]

Equidae [Family]Equus [Genus]

E. asinus [Species]E. burchelliiE. caballusE. grevyiE. hemionusE. kiangE. onagerE. quaggaE. zebra

Tapiridae [Family]Tapirus [Genus]

T. bairdii [Species]T. indicusT. pinchaqueT. terrestris

Rhinocerotidae [Family]Ceratotherium [Genus]

C. simum [Species]

Dicerorhinus [Genus]D. sumatrensis [Species]

Diceros [Genus]D. bicornis [Species]

Rhinoceros [Genus]R. sondaicus [Species]R. unicornis

Artiodactyla [Order]

Suidae [Family]Babyrousa [Genus]

B. babyrussa [Species]Phacochoerus [Genus]

P. aethiopicus [Species]P. africanus

Hylochoerus [Genus]H. meinertzhageni [Species]

Potamochoerus [Genus]P. larvatus [Species]P. porcus

Sus [Genus]S. barbatus [Species]S. bucculentusS. cebifronsS. celebensisS. heureniS. philippensisS. salvaniusS. scrofaS. timoriensisS. verrucosus

Tayassuidae [Family]Catagonus [Genus]

C. wagneri [Species]Pecari [Genus]

P. tajacu [Species]Tayassu [Genus]

T. pecari [Species]

Hippopotamidae [Family]Hexaprotodon [Genus]

H. liberiensis [Species]H. madagascariensis

Hippopotamus [Genus]H. amphibius [Species]H. lemerlei

Camelidae [Family]Camelus [Genus]

C. bactrianus [Species]C. dromedarius

Lama [Genus]L. glama [Species]L. guanicoeL. pacos

Vicugna [Genus]V. vicugna [Species]

Tragulidae [Family]Hyemoschus [Genus]

H. aquaticus [Species]Moschiola [Genus]

M. meminna [Species]Tragulus [Genus]

T. javanicus [Species]T. napu

Cervidae [Family]Alces [Genus]

A. alces [Species]Axis [Genus]

A. axis [Species]A. calamianensisA. kuhliiA. porcinus

Blastocerus [Genus]B. dichotomus [Species]

Capreolus [Genus]C. capreolus [Species]C. pygargus

Cervus [Genus]C. albirostris [Species]C. alfrediC. duvauceliiC. elaphusC. eldiiC. mariannusC. nipponC. schomburgkiC. timorensisC. unicolor

Dama [Genus]D. dama [Species]D. mesopotamica

Elaphodus [Genus]E. cephalophus [Species]

Elaphurus [Genus]E. davidianus [Species]

Hippocamelus [Genus]H. antisensis [Species]H. bisulcus

Hydropotes [Genus]H. inermis [Species]

Mazama [Genus]M. americana [Species]M. briceniiM. chunyiM. gouazoupiraM. nanaM. rufina

Moschus [Genus]M. berezovskii [Species]M. chrysogasterM. fuscusM. moschiferus

Muntiacus [Genus]M. atherodes [Species]M. crinifronsM. feaeM. gongshanensis



AM

MA

LSSP

EC

IES

LIST

M. muntjakM. reevesi

Odocoileus [Genus]O. hemionus [Species]O. virginianus

Ozotoceros [Genus]O. bezoarticus [Species]

Pudu [Genus]P. mephistophiles [Species]P. puda

Rangifer [Genus]R. tarandus [Species]

Giraffidae [Family]Giraffa [Genus]

G. camelopardalis [Species]Okapia [Genus]

O. johnstoni [Species]

Antilocapridae [Family]Antilocapra [Genus]

A. americana [Species]

Bovidae [Family]Addax [Genus]

A. nasomaculatus [Species]Aepyceros [Genus]

A. melampus [Species]Alcelaphus [Genus]

A. buselaphus [Species]Ammodorcas [Genus]

A. clarkei [Species]Ammotragus [Genus]

A. lervia [Species]Antidorcas [Genus]

A. marsupialis [Species]Antilope [Genus]

A. cervicapra [Species]Bison [Genus]

B. bison [Species]B. bonasus

Bos [Genus]B. frontalis [Species]B. grunniensB. javanicusB. sauveliB. taurus

Boselaphus [Genus]B. tragocamelus [Species]

Bubalus [Genus]B. bubalis [Species]B. depressicornisB. mephistophelesB. mindorensisB. quarlesi

Budorcas [Genus]B. taxicolor [Species]

Capra [Genus]C. caucasica [Species]C. cylindricornisC. falconeriC. hircus

C. ibexC. nubianaC. pyrenaicaC. sibiricaC. walie

Cephalophus [Genus]C. adersi [Species]C. callipygusC. dorsalisC. harveyiC. jentinkiC. leucogasterC. maxwelliiC. monticolaC. natalensisC. nigerC. nigrifronsC. ogilbyiC. rubidusC. rufilatusC. silvicultorC. spadixC. weynsiC. zebra

Connochaetes [Genus]C. gnou [Species]C. taurinus

Damaliscus [Genus]D. hunteri [Species]D. lunatusD. pygargus

Dorcatragus [Genus]D. megalotis [Species]

Gazella [Genus]G. arabica [Species]G. bennettiiG. bilkisG. cuvieriG. damaG. dorcasG. gazellaG. grantiG. leptocerosG. rufifronsG. rufinaG. saudiyaG. soemmerringiiG. spekeiG. subgutturosaG. thomsonii

Hemitragus [Genus]H. hylocrius [Species]H. jayakariH. jemlahicus

Hippotragus [Genus]H. equinus [Species]H. leucophaeusH. niger

Kobus [Genus]K. ellipsiprymnus [Species]

K. kobK. lecheK. megacerosK. vardonii

Litocranius [Genus]L. walleri [Species]

Madoqua [Genus]M. guentheri [Species]M. kirkiiM. piacentiniiM. saltiana

Naemorhedus [Genus]N. baileyi [Species]N. caudatusN. crispusN. goralN. sumatraensisN. swinhoei

Neotragus [Genus]N. batesi [Species]N. moschatusN. pygmaeus

Oreamnos [Genus]O. americanus [Species]

Oreotragus [Genus]O. oreotragus [Species]

Oryx [Genus]O. dammah [Species]O. gazellaO. leucoryx

Ourebia [Genus]O. ourebi [Species]

Ovibos [Genus]O. moschatus [Species]

Ovis [Genus]O. ammon [Species]O. ariesO. canadensisO. dalliO. nivicolaO. vignei

Pantholops [Genus]P. hodgsonii [Species]

Pelea [Genus]P. capreolus [Species]

Procapra [Genus]P. gutturosa [Species]P. picticaudataP. przewalskii

Pseudois [Genus]P. nayaur [Species]P. schaeferi

Raphicerus [Genus]R. campestris [Species]R. melanotisR. sharpei

Redunca [Genus]R. arundinum [Species]R. fulvorufulaR. redunca



Rupicapra [Genus]R. pyrenaica [Species]R. rupicapra

Saiga [Genus]S. tatarica [Species]

Sigmoceros [Genus]S. lichtensteinii [Species]

Sylvicapra [Genus]S. grimmia [Species]

Syncerus [Genus]S. caffer [Species]

Taurotragus [Genus]T. derbianus [Species]T. oryx

Tetracerus [Genus]T. quadricornis [Species]

Tragelaphus [Genus]T. angasii [Species]T. buxtoniT. eurycerusT. imberbisT. scriptusT. spekiiT. strepsiceros

Pholidota [Order]

Manidae [Family]Manis [Genus]

M. crassicaudata [Species]M. giganteaM. javanicaM. pentadactylaM. temminckiiM. tetradactylaM. tricuspis

Rodentia [Order]

Aplodontidae [Family]Aplodontia [Genus]

A. rufa [Species]

Sciuridae [Family]Aeretes [Genus]

A. melanopterus [Species]Aeromys [Genus]

A. tephromelas [Species]A. thomasi

Ammospermophilus [Genus]A. harrisii [Species]A. insularisA. interpresA. leucurusA. nelsoni

Atlantoxerus [Genus]A. getulus [Species]

Belomys [Genus]B. pearsonii [Species]

Biswamoyopterus [Genus]B. biswasi [Species]

Callosciurus [Genus]C. adamsi [Species]C. albescensC. baluensisC. canicepsC. erythraeusC. finlaysoniiC. inornatusC. melanogasterC. nigrovittatusC. notatusC. orestesC. phayreiC. prevostiiC. pygerythrusC. quinquestriatus

Cynomys [Genus]C. gunnisoni [Species]C. leucurusC. ludovicianusC. mexicanusC. parvidens

Dremomys [Genus]D. everetti [Species]D. lokriahD. pernyiD. pyrrhomerusD. rufigenis

Epixerus [Genus]E. ebii [Species]E. wilsoni

Eupetaurus [Genus]E. cinereus [Species]

Exilisciurus [Genus]E. concinnus [Species]E. exilisE. whiteheadi

Funambulus [Genus]F. layardi [Species]F. palmarumF. pennantiiF. sublineatusF. tristriatus

Funisciurus [Genus]F. anerythrus [Species]F. bayoniiF. carruthersiF. congicusF. isabellaF. lemniscatusF. leucogenysF. pyrropusF. substriatus

Glaucomys [Genus]G. sabrinus [Species]G. volans

Glyphotes [Genus]G. simus [Species]

Heliosciurus [Genus]H. gambianus [Species]

H. mutabilisH. punctatusH. rufobrachiumH. ruwenzoriiH. undulatus

Hylopetes [Genus]H. alboniger [Species]H. baberiH. bartelsiH. fimbriatusH. lepidusH. nigripesH. phayreiH. siporaH. spadiceusH. winstoni

Hyosciurus [Genus]H. heinrichi [Species]H. ileile

Iomys [Genus]I. horsfieldi [Species]I. sipora

Lariscus [Genus]L. hosei [Species]L. insignisL. niobeL. obscurus

Marmota [Genus]M. baibacina [Species]M. bobakM. broweriM. caligataM. camtschaticaM. caudataM. flaviventrisM. himalayanaM. marmotaM. menzbieriM. monaxM. olympusM. sibiricaM. vancouverensis

Menetes [Genus]M. berdmorei [Species]

Microsciurus [Genus]M. alfari [Species]M. flaviventerM. mimulusM. santanderensis

Myosciurus [Genus]M. pumilio [Species]

Nannosciurus [Genus]N. melanotis [Species]

Paraxerus [Genus]P. alexandri [Species]P. boehmiP. cepapiP. cooperiP. flavovittisP. lucifer



AM

MA

LSSP

EC

IES

LIST

P. ochraceusP. palliatusP. poensisP. vexillariusP. vincenti

Petaurillus [Genus]P. emiliae [Species]P. hoseiP. kinlochii

Petaurista [Genus]P. alborufus [Species]P. elegansP. leucogenysP. magnificusP. nobilisP. petauristaP. philippensisP. xanthotis

Petinomys [Genus]P. crinitus [Species]P. fuscocapillusP. genibarbisP. hageniP. lugensP. sagittaP. setosusP. vordermanni

Prosciurillus [Genus]P. abstrusus [Species]P. leucomusP. murinusP. weberi

Protoxerus [Genus]P. aubinnii [Species]P. stangeri

Pteromys [Genus]P. momonga [Species]P. volans

Pteromyscus [Genus]P. pulverulentus [Species]

Ratufa [Genus]R. affinis [Species]R. bicolorR. indicaR. macroura

Rheithrosciurus [Genus]R. macrotis [Species]

Rhinosciurus [Genus]R. laticaudatus [Species]

Rubrisciurus [Genus]R. rubriventer [Species]

Sciurillus [Genus]S. pusillus [Species]

Sciurotamias [Genus]S. davidianus [Species]S. forresti

Sciurus [Genus]S. aberti [Species]S. aestuansS. alleni

S. anomalusS. arizonensisS. aureogasterS. carolinensisS. colliaeiS. deppeiS. flammiferS. gilvigularisS. granatensisS. griseusS. ignitusS. igniventrisS. lisS. nayaritensisS. nigerS. oculatusS. pucheraniiS. pyrrhinusS. richmondiS. sanborniS. spadiceusS. stramineusS. variegatoidesS. vulgarisS. yucatanensis

Spermophilopsis [Genus]S. leptodactylus [Species]

Spermophilus [Genus]S. adocetus [Species]S. alashanicusS. annulatusS. armatusS. atricapillusS. beecheyiS. beldingiS. brunneusS. canusS. citellusS. columbianusS. dauricusS. elegansS. erythrogenysS. frankliniiS. fulvusS. lateralisS. madrensisS. majorS. mexicanusS. mohavensisS. mollisS. musicusS. parryiiS. perotensisS. pygmaeusS. relictusS. richardsoniiS. saturatusS. spilosomaS. suslicusS. tereticaudus

S. townsendiiS. tridecemlineatusS. undulatusS. variegatusS. washingtoniS. xanthoprymnus

Sundasciurus [Genus]S. brookei [Species]S. davensisS. fraterculusS. hippurusS. hoogstraaliS. jentinkiS. juvencusS. lowiiS. mindanensisS. moellendorffiS. philippinensisS. raboriS. samarensisS. steeriiS. tenuis

Syntheosciurus [Genus]S. brochus [Species]

Tamias [Genus]T. alpinus [Species]T. amoenusT. bulleriT. canipesT. cinereicollisT. dorsalisT. durangaeT. merriamiT. minimusT. obscurusT. ochrogenysT. palmeriT. panamintinusT. quadrimaculatusT. quadrivittatusT. ruficaudusT. rufusT. senexT. sibiricusT. siskiyouT. sonomaeT. speciosusT. striatusT. townsendiiT. umbrinus

Tamiasciurus [Genus]T. douglasii [Species]T. hudsonicusT. mearnsi

Tamiops [Genus]T. macclellandi [Species]T. maritimusT. rodolpheiT. swinhoei

Trogopterus [Genus]



T. xanthipes [Species]Xerus [Genus]

X. erythropus [Species]X. inaurisX. princepsX. rutilus

Castoridae [Family]Castor [Genus]

C. canadensis [Species]C. fiber

Geomyidae [Family]Geomys [Genus]

G. arenarius [Species]G. bursariusG. personatusG. pinetisG. tropicalis

Orthogeomys [Genus]O. cavator [Species]O. cherrieiO. cuniculusO. dariensisO. grandisO. heterodusO. hispidusO. laniusO. matagalpaeO. thaeleriO. underwoodi

Pappogeomys [Genus]P. alcorni [Species]P. bulleriP. castanopsP. fumosusP. gymnurusP. merriamiP. neglectusP. tylorhinusP. zinseri

Thomomys [Genus]T. bottae [Species]T. bulbivorusT. clusiusT. idahoensisT. mazamaT. monticolaT. talpoidesT. townsendiiT. umbrinus

Zygogeomys [Genus]Z. trichopus [Species]

Heteromyidae [Family]Chaetodipus [Genus]

C. arenarius [Species]C. artusC. baileyiC. californicus

C. fallaxC. formosusC. goldmaniC. hispidusC. intermediusC. lineatusC. nelsoniC. penicillatusC. pernixC. spinatus

Dipodomys [Genus]D. agilis [Species]D. californicusD. compactusD. desertiD. elatorD. elephantinusD. gravipesD. heermanniD. ingensD. insularisD. margaritaeD. merriamiD. micropsD. nelsoniD. nitratoidesD. ordiiD. panamintinusD. phillipsiiD. spectabilisD. stephensiD. venustus

Microdipodops [Genus]M. megacephalus [Species]M. pallidus

Heteromys [Genus]H. anomalus [Species]H. australisH. desmarestianusH. gaumeriH. goldmaniH. nelsoniH. oresterus

Liomys [Genus]L. adspersus [Species]L. irroratusL. pictusL. salviniL. spectabilis

Perognathus [Genus]P. alticola [Species]P. amplusP. fasciatusP. flavescensP. flavusP. inornatusP. longimembrisP. merriamiP. parvusP. xanthanotus

Dipodidae [Family]Allactaga [Genus]

A. balikunica [Species]A. bullataA. elaterA. euphraticaA. firouziA. hotsoniA. majorA. severtzoviA. sibiricaA. tetradactylaA. vinogradovi

Allactodipus [Genus]A. bobrinskii [Species]

Cardiocranius [Genus]C. paradoxus [Species]

Dipus [Genus]D. sagitta [Species]

Eozapus [Genus]E. setchuanus [Species]

Eremodipus [Genus]E. lichtensteini [Species]

Euchoreutes [Genus]E. naso [Species]

Jaculus [Genus]J. blanfordi [Species]J. jaculusJ. orientalisJ. turcmenicus

Napaeozapus [Genus]N. insignis [Species]

Paradipus [Genus]P. ctenodactylus [Species]

Pygeretmus [Genus]P. platyurus [Species]P. pumilioP. shitkovi

Salpingotus [Genus]S. crassicauda [Species]S. heptneriS. kozloviS. michaelisS. pallidusS. thomasi

Sicista [Genus]S. armenica [Species]S. betulinaS. caucasicaS. caudataS. concolorS. kazbegicaS. kluchoricaS. napaeaS. pseudonapaeaS. severtzoviS. strandiS. subtilisS. tianshanica

Stylodipus [Genus]



AM

MA

LSSP

EC

IES

LIST

S. andrewsi [Species]S. sungorusS. telum

Zapus [Genus]Z. hudsonius [Species]Z. princepsZ. trinotatus

Muridae [Family]Abditomys [Genus]

A. latidens [Species]Abrawayaomys [Genus]

A. ruschii [Species]Acomys [Genus]

A. cahirinus [Species]A. cilicicusA. cinerasceusA. ignitusA. kempiA. louisaeA. minousA. mullahA. nesiotesA. percivaliA. russatusA. spinosissimusA. subspinosusA. wilsoni

Aepeomys [Genus]A. fuscatus [Species]A. lugens

Aethomys [Genus]A. bocagei [Species]A. chrysophilusA. grantiA. hindeiA. kaiseriA. namaquensisA. nyikaeA. silindensisA. stannariusA. thomasi

Akodon [Genus]A. aerosus [Species]A. affinisA. albiventerA. azaraeA. bogotensisA. boliviensisA. budiniA. cursorA. dayiA. doloresA. fumeusA. hershkovitziA. illuteusA. iniscatusA. juninensisA. kempiA. kofordiA. lanosus

A. latebricolaA. lindberghiA. longipilisA. mansoensisA. markhamiA. mimusA. molinaeA. mollisA. neocenusA. nigritaA. olivaceusA. orophilusA. puerA. sanborniA. sanctipaulensisA. serrensisA. siberiaeA. simulatorA. spegazziniiA. subfuscusA. surdusA. sylvanusA. tobaA. torquesA. urichiA. variusA. xanthorhinus

Allocricetulus [Genus]A. curtatus [Species]A. eversmanni

Alticola [Genus]A. albicauda [Species]A. argentatusA. barakshinA. lemminusA. macrotisA. montosaA. royleiA. semicanusA. stoliczkanusA. stracheyiA. strelzowiA. tuvinicus

Ammodillus [Genus]A. imbellis [Species]

Andalgalomys [Genus]A. olrogi [Species]A. pearsoni

Andinomys [Genus]A. edax [Species]

Anisomys [Genus]A. imitator [Species]

Anonymomys [Genus]A. mindorensis [Species]

Anotomys [Genus]A. leander [Species]

Apodemus [Genus]A. agrarius [Species]A. alpicolaA. argenteus

A. arianusA. chevrieriA. dracoA. flavicollisA. fulvipectusA. gurkhaA. hermonensisA. hyrcanicusA. latronumA. mystacinusA. peninsulaeA. ponticusA. rusigesA. semotusA. speciosusA. sylvaticusA. uralensisA. wardi

Apomys [Genus]A. abrae [Species]A. dataeA. hylocoetesA. insignisA. littoralisA. microdonA. musculusA. sacobianus

Arborimus [Genus]A. albipes [Species]A. longicaudusA. pomo

Archboldomys [Genus]A. luzonensis [Species]

Arvicanthis [Genus]A. abyssinicus [Species]A. blickiA. nairobaeA. niloticusA. somalicus

Arvicola [Genus]A. sapidus [Species]A. terrestris

Auliscomys [Genus]A. boliviensis [Species]A. micropusA. pictusA. sublimis

Baiomys [Genus]B. musculus [Species]B. taylori

Bandicota [Genus]B. bengalensis [Species]B. indicaB. savilei

Batomys [Genus]B. dentatus [Species]B. grantiB. salomonseni

Beamys [Genus]B. hindei [Species]



B. majorBerylmys [Genus]

B. berdmorei [Species]B. bowersiB. mackenzieiB. manipulus

Bibimys [Genus]B. chacoensis [Species]B. labiosusB. torresi

Blanfordimys [Genus]B. afghanus [Species]B. bucharicus

Blarinomys [Genus]B. breviceps [Species]

Bolomys [Genus]B. amoenus [Species]B. lactensB. lasiurusB. obscurusB. punctulatusB. temchuki

Brachiones [Genus]B. przewalskii [Species]

Brachytarsomys [Genus]B. albicauda [Species]

Brachyuromys [Genus]B. betsileoensis [Species]B. ramirohitra

Bullimus [Genus]B. bagobus [Species]B. luzonicus

Bunomys [Genus]B. andrewsi [Species]B. chrysocomusB. coelestisB. fratrorumB. heinrichiB. penitusB. prolatus

Calomys [Genus]C. boliviae [Species]C. callidusC. callosusC. hummelinckiC. lauchaC. lepidusC. musculinusC. sorellusC. tener

Calomyscus [Genus]C. bailwardi [Species]C. baluchiC. hotsoniC. mystaxC. tsoloviC. urartensis

Canariomys [Genus]C. tamarani [Species]

Cannomys [Genus]

C. badius [Species]Cansumys [Genus]

C. canus [Species]Carpomys [Genus]

C. melanurus [Species]C. phaeurus

Celaenomys [Genus]C. silaceus [Species]

Chelemys [Genus]C. macronyx [Species]C. megalonyx

Chibchanomys [Genus]C. trichotis [Species]

Chilomys [Genus]C. instans [Species]

Chiromyscus [Genus]C. chiropus [Species]

Chinchillula [Genus]C. sahamae [Species]

Chionomys [Genus]C. gud [Species]C. nivalisC. roberti

Chiropodomys [Genus]C. calamianensis [Species]C. gliroidesC. karlkoopmaniC. majorC. muroidesC. pusillus

Chiruromys [Genus]C. forbesi [Species]C. lamiaC. vates

Chroeomys [Genus]C. andinus [Species]C. jelskii

Chrotomys [Genus]C. gonzalesi [Species]C. mindorensisC. whiteheadi

Clethrionomys [Genus]C. californicus [Species]C. centralisC. gapperiC. glareolusC. rufocanusC. rutilusC. sikotanensis

Coccymys [Genus]C. albidens [Species]C. ruemmleri

Colomys [Genus]C. goslingi [Species]

Conilurus [Genus]C. albipes [Species]C. penicillatus

Coryphomys [Genus]C. buhleri [Species]

Crateromys [Genus]

C. australis [Species]C. paulusC. schadenbergi

Cremnomys [Genus]C. blanfordi [Species]C. cutchicusC. elvira

Cricetomys [Genus]C. emini [Species]C. gambianus

Cricetulus [Genus]C. alticola [Species]C. barabensisC. kamensisC. longicaudatusC. migratoriusC. sokolovi

Cricetus [Genus]C. cricetus [Species]

Crossomys [Genus]C. moncktoni [Species]

Crunomys [Genus]C. celebensis [Species]C. fallaxC. melaniusC. rabori

Dacnomys [Genus]D. millardi [Species]

Dasymys [Genus]D. foxi [Species]D. incomtusD. montanusD. nudipesD. rufulus

Delanymys [Genus]D. brooksi [Species]

Delomys [Genus]D. dorsalis [Species]D. sublineatus

Dendromus [Genus]D. insignis [Species]D. kahuziensisD. kivuD. lovatiD. melanotisD. mesomelasD. messoriusD. mystacalisD. nyikaeD. oreasD. vernayi

Dendroprionomys [Genus]D. rousseloti [Species]

Deomys [Genus]D. ferrugineus [Species]

Dephomys [Genus]D. defua [Species]D. eburnea

Desmodilliscus [Genus]D. braueri [Species]



AM

MA

LSSP

EC

IES

LIST

Desmodillus [Genus]D. auricularis [Species]

Dicrostonyx [Genus]D. exsul [Species]D. groenlandicusD. hudsoniusD. kilangmiutakD. nelsoniD. nunatakensisD. richardsoniD. rubricatusD. torquatusD. unalascensisD. vinogradovi

Desmomys [Genus]D. harringtoni [Species]

Dinaromys [Genus]D. bogdanovi [Species]

Diomys [Genus]D. crumpi [Species]

Diplothrix [Genus]D. legatus [Species]

Echiothrix [Genus]E. leucura [Species]

Eropeplus [Genus]E. canus [Species]

Eligmodontia [Genus]E. moreni [Species]E. morganiE. puerulusE. typus

Eliurus [Genus]E. majori [Species]E. minorE. myoxinusE. penicillatusE. tanalaE. webbi

Ellobius [Genus]E. alaicus [Species]E. fuscocapillusE. lutescensE. talpinusE. tancrei

Eolagurus [Genus]E. luteus [Species]E. przewalskii

Eothenomys [Genus]E. chinensis [Species]E. custosE. evaE. inezE. melanogasterE. olitorE. proditorE. regulusE. shanseius

Euneomys [Genus]E. chinchilloides [Species]E. fossor

E. mordaxE. petersoni

Galenomys [Genus]G. garleppi [Species]

Geoxus [Genus]G. valdivianus [Species]

Gerbillurus [Genus]G. paeba [Species]G. setzeriG. tytonisG. vallinus

Gerbillus [Genus]G. acticola [Species]G. allenbyiG. andersoniG. bilensisG. bottaiG. burtoniG. cheesmaniG. dalloniG. diminutusG. dunniG. floweriG. gerbillusG. grobbeniG. henleyiG. hoogstraaliG. julianiG. loweiG. maghrebiG. mesopotamiaeG. nancillusG. nigeriaeG. percivaliG. poecilopsG. pulvinatusG. pyramidumG. riggenbachiG. ruberrimusG. somalicusG. syrticusG. vivax

Golunda [Genus]G. ellioti [Species]

Grammomys [Genus]G. aridulus [Species]G. canicepsG. dolichurusG. gigasG. macmillaniG. rutilans

Graomys [Genus]G. domorum [Species]G. griseoflavus

Gymnuromys [Genus]G. roberti [Species]

Habromys [Genus]H. chinanteco [Species]H. lepturusH. lophurus

H. simulatusHadromys [Genus]

H. humei [Species]Haeromys [Genus]

H. margarettae [Species]H. minahassaeH. pusillus

Hapalomys [Genus]H. delacouri [Species]H. longicaudatus

Heimyscus [Genus]H. fumosus [Species]

Hodomys [Genus]H. alleni [Species]

Holochilus [Genus]H. brasiliensis [Species]H. chacariusH. magnusH. sciureus

Hybomys [Genus]H. basilii [Species]H. eisentrautiH. lunarisH. planifronsH. trivirgatusH. univittatus

Hydromys [Genus]H. chrysogaster [Species]H. habbemaH. hussoniH. neobrittanicusH. shawmayeri

Hylomyscus [Genus]H. aeta [Species]H. alleniH. baeriH. carillusH. denniaeH. parvusH. stella

Hyomys [Genus]H. dammermani [Species]H. goliath

Hyperacrius [Genus]H. fertilis [Species]H. wynnei

Hypogeomys [Genus]H. antimena [Species]

Ichthyomys [Genus]I. hydrobates [Species]I. pittieriI. stolzmanniI. tweedii

Irenomys [Genus]I. tarsalis [Species]

Isthmomys [Genus]I. flavidus [Species]I. pirrensis

Juscelinomys [Genus]J. candango [Species]



J. vulpinusKadarsanomys [Genus]

K. sodyi [Species]Komodomys [Genus]

K. rintjanus [Species]Kunsia [Genus]

K. fronto [Species]K. tomentosus

Lagurus [Genus]L. lagurus [Species]

Lamottemys [Genus]L. okuensis [Species]

Lasiopodomys [Genus]L. brandtii [Species]L. fuscusL. mandarinus

Leggadina [Genus]L. forresti [Species]L. lakedownensis

Leimacomys [Genus]L. buettneri [Species]

Lemmiscus [Genus]L. curtatus [Species]

Lemmus [Genus]L. amurensis [Species]L. lemmusL. sibiricus

Lemniscomys [Genus]L. barbarus [Species]L. bellieriL. griseldaL. hoogstraaliL. linulusL. macculusL. mittendorfiL. rosaliaL. roseveariL. striatus

Lenomys [Genus]L. meyeri [Species]

Lenothrix [Genus]L. canus [Species]

Lenoxus [Genus]L. apicalis [Species]

Leopoldamys [Genus]L. edwardsi [Species]L. neilliL. sabanusL. siporanus

Leporillus [Genus]L. apicalis [Species]L. conditor

Leptomys [Genus]L. elegans [Species]L. ernstmayriL. signatus

Limnomys [Genus]L. sibuanus [Species]

Lophiomys [Genus]L. imhausi [Species]

Lophuromys [Genus]L. cinereus [Species]L. flavopunctatusL. luteogasterL. medicaudatusL. melanonyxL. nudicaudusL. rahmiL. sikapusiL. woosnami

Lorentzimys [Genus]L. nouhuysi [Species]

Macrotarsomys [Genus]M. bastardi [Species]M. ingens

Macruromys [Genus]M. elegans [Species]M. major

Malacomys [Genus]M. cansdalei [Species]M. edwardsiM. longipesM. lukolelaeM. verschureni

Malacothrix [Genus]M. typica [Species]

Mallomys [Genus]M. aroaensis [Species]M. gunungM. istapantapM. rothschildi

Malpaisomys [Genus]M. insularis [Species]

Margaretamys [Genus]M. beccarii [Species]M. elegansM. parvus

Mastomys [Genus]M. angolensis [Species]M. couchaM. erythroleucusM. hildebrandtiiM. natalensisM. pernanusM. shortridgeiM. verheyeni

Maxomys [Genus]M. alticola [Species]M. baeodonM. bartelsiiM. dollmaniM. hellwaldiiM. hylomyoidesM. inasM. inflatusM. moiM. musschenbroekiiM. ochraceiventerM. pagensisM. panglima

M. rajahM. suriferM. wattsiM. whiteheadi

Mayermys [Genus]M. ellermani [Species]

Megadendromus [Genus]M. nikolausi [Species]

Megadontomys [Genus]M. cryophilus [Species]M. nelsoniM. thomasi

Megalomys [Genus]M. desmarestii [Species]M. luciae

Melanomys [Genus]M. caliginosus [Species]M. robustulusM. zunigae

Melasmothrix [Genus]M. naso [Species]

Melomys [Genus]M. aerosus [Species]M. bougainvilleM. burtoniM. capensisM. cervinipesM. fellowsiM. fraterculusM. gracilisM. lanosusM. leucogasterM. levipesM. lorentziiM. mollisM. moncktoniM. obiensisM. platyopsM. rattoidesM. rubexM. rubicolaM. rufescensM. spechti

Meriones [Genus]M. arimalius [Species]M. chengiM. crassusM. dahliM. hurrianaeM. libycusM. meridianusM. persicusM. rexM. sacramentiM. shawiM. tamariscinusM. tristramiM. unguiculatusM. vinogradoviM. zarudnyi



AM

MA

LSSP

EC

IES

LIST

Mesembriomys [Genus]M. gouldii [Species]M. macrurus

Mesocricetus [Genus]M. auratus [Species]M. brandtiM. newtoniM. raddei

Microdillus [Genus]M. peeli [Species]

Microhydromys [Genus]M. musseri [Species]M. richardsoni

Micromys [Genus]M. minutus [Species]

Microryzomys [Genus]M. altissimus [Species]M. minutus

Microtus [Genus]M. abbreviatus [Species]M. agrestisM. arvalisM. bavaricusM. breweriM. cabreraeM. californicusM. canicaudusM. chrotorrhinusM. daghestanicusM. duodecimcostatusM. evoronensisM. felteniM. fortisM. gerbeiM. gregalisM. guatemalensisM. guentheriM. hyperboreusM. iraniM. ireneM. juldaschiM. kermanensisM. kirgisorumM. leucurusM. limnophilusM. longicaudusM. lusitanicusM. majoriM. maximowicziiM. mexicanusM. middendorffiM. miurusM. mongolicusM. montanusM. montebelliM. mujanensisM. multiplexM. nasaroviM. oaxacensisM. obscurus

M. ochrogasterM. oeconomusM. oregoniM. pennsylvanicusM. pinetorumM. quasiaterM. richardsoniM. rossiaemeridionalisM. sachalinensisM. saviiM. schelkovnikoviM. sikimensisM. socialisM. subterraneusM. tatricusM. thomasiM. townsendiiM. transcaspicusM. umbrosusM. xanthognathus

Millardia [Genus]M. gleadowi [Species]M. kathleenaeM. kondanaM. meltada

Muriculus [Genus]M. imberbis [Species]

Mus [Genus]M. baoulei [Species]M. boodugaM. bufoM. callewaertiM. caroliM. cervicolorM. cookiiM. crociduroidesM. famulusM. fernandoniM. goundaeM. haussaM. indutusM. kasaicusM. macedonicusM. mahometM. mattheyiM. mayoriM. minutoidesM. musculoidesM. musculusM. neaveiM. orangiaeM. oubanguiiM. pahariM. phillipsiM. platythrixM. saxicolaM. setulosusM. setzeriM. shortridgeiM. sorella

M. spicilegusM. spretusM. tenellusM. terricolorM. tritonM. vulcani

Mylomys [Genus]M. dybowskii [Species]

Myomys [Genus]M. albipes [Species]M. daltoniM. derooiM. fumatusM. ruppiM. verreauxiiM. yemeni

Myopus [Genus]M. schisticolor [Species]

Myospalax [Genus]M. aspalax [Species]M. epsilanusM. fontanieriiM. myospalaxM. psilurusM. rothschildiM. smithii

Mystromys [Genus]M. albicaudatus [Species]

Nannospalax [Genus]N. ehrenbergi [Species]N. leucodonN. nehringi

Neacomys [Genus]N. guianae [Species]N. pictusN. spinosusN. tenuipes

Nectomys [Genus]N. palmipes [Species]N. parvipesN. squamipes

Nelsonia [Genus]N. goldmani [Species]N. neotomodon

Neofiber [Genus]N. alleni [Species]

Neohydromys [Genus]N. fuscus [Species]

Neotoma [Genus]N. albigula [Species]N. angustapalataN. anthonyiN. bryantiN. bunkeriN. chrysomelasN. cinereaN. deviaN. floridanaN. fuscipesN. goldmani



N. lepidaN. martinensisN. mexicanaN. micropusN. nelsoniN. palatinaN. phenaxN. stephensiN. varia

Neotomodon [Genus]N. alstoni [Species]

Neotomys [Genus]N. ebriosus [Species]

Nesomys [Genus]N. rufus [Species]

Nesokia [Genus]N. bunnii [Species]N. indica

Nesoryzomys [Genus]N. darwini [Species]N. fernandinaeN. indefessusN. swarthi

Neusticomys [Genus]N. monticolus [Species]N. mussoiN. oyapockiN. peruviensisN. venezuelae

Niviventer [Genus]N. andersoni [Species]N. brahmaN. confucianusN. coxingiN. cremoriventerN. culturatusN. ehaN. excelsiorN. fulvescensN. hinpoonN. langbianisN. lepturusN. niviventerN. rapitN. tenaster

Notiomys [Genus]N. edwardsii [Species]

Notomys [Genus]N. alexis [Species]N. amplusN. aquiloN. cervinusN. fuscusN. longicaudatusN. macrotisN. mitchelliiN. mordax

Nyctomys [Genus]N. sumichrasti [Species]

Ochrotomys [Genus]

O. nuttalli [Species]Oecomys [Genus]

O. bicolor [Species]O. cleberiO. concolorO. flavicansO. mamoraeO. paricolaO. phaeotisO. rexO. robertiO. rutilusO. speciosusO. superansO. trinitatis

Oenomys [Genus]O. hypoxanthus [Species]O. ornatus

Oligoryzomys [Genus]O. andinus [Species]O. arenalisO. chacoensisO. delticolaO. destructorO. eliurusO. flavescensO. fulvescensO. griseolusO. longicaudatusO. magellanicusO. microtisO. nigripesO. vegetusO. victus

Ondatra [Genus]O. zibethicus [Species]

Onychomys [Genus]O. arenicola [Species]O. leucogasterO. torridus

Oryzomys [Genus]O. albigularis [Species]O. alfaroiO. auriventerO. balneatorO. bolivarisO. buccinatusO. capitoO. chapmaniO. couesiO. deviusO. dimidiatusO. galapagoensisO. gorgasiO. hammondiO. intectusO. intermediusO. keaysiO. kelloggiO. lamia

O. legatusO. levipesO. macconnelliO. melanotisO. nelsoniO. nitidusO. oniscusO. palustrisO. poliusO. ratticepsO. rhabdopsO. rostratusO. saturatiorO. subflavusO. talamancaeO. xantheolusO. yunganus

Osgoodomys [Genus]O. banderanus [Species]

Otomys [Genus]O. anchietae [Species]O. angoniensisO. dentiO. irroratusO. laminatusO. maximusO. occidentalisO. saundersiaeO. sloggettiO. tropicalisO. typusO. unisulcatus

Otonyctomys [Genus]O. hatti [Species]

Ototylomys [Genus]O. phyllotis [Species]

Oxymycterus [Genus]O. akodontius [Species]O. angularisO. delatorO. hiskaO. hispidusO. hucuchaO. iheringiO. incaO. nasutusO. paramensisO. robertiO. rufus

Pachyuromys [Genus]P. duprasi [Species]

Palawanomys [Genus]P. furvus [Species]

Papagomys [Genus]P. armandvillei [Species]P. theodorverhoeveni

Parahydromys [Genus]P. asper [Species]

Paraleptomys [Genus]P. rufilatus [Species]



AM

MA

LSSP

EC

IES

LIST

P. wilhelminaParotomys [Genus]

P. brantsii [Species]P. littledalei

Paruromys [Genus]P. dominator [Species]P. ursinus

Paulamys [Genus]P. naso [Species]

Pelomys [Genus]P. campanae [Species]P. fallaxP. hopkinsiP. isseliP. minor

Peromyscus [Genus]P. attwateri [Species]P. aztecusP. boyliiP. bullatusP. californicusP. canicepsP. crinitusP. dickeyiP. difficilisP. eremicusP. evaP. furvusP. gossypinusP. grandisP. gratusP. guardiaP. guatemalensisP. gymnotisP. hooperiP. interparietalisP. leucopusP. levipesP. madrensisP. maniculatusP. mayensisP. megalopsP. mekisturusP. melanocarpusP. melanophrysP. melanotisP. melanurusP. merriamiP. mexicanusP. nasutusP. ochraventerP. oreasP. pectoralisP. pembertoniP. perfulvusP. polionotusP. poliusP. pseudocrinitusP. sejugisP. simulus

P. sitkensisP. sleviniP. spicilegusP. stephaniP. stirtoniP. trueiP. winkelmanniP. yucatanicusP. zarhynchus

Petromyscus [Genus]P. barbouri [Species]P. collinusP. monticularisP. shortridgei

Phaenomys [Genus]P. ferrugineus [Species]

Phaulomys [Genus]P. andersoni [Species]P. smithii

Phenacomys [Genus]P. intermedius [Species]P. ungava

Phloeomys [Genus]P. cumingi [Species]P. pallidus

Phyllotis [Genus]P. amicus [Species]P. andiumP. bonaeriensisP. caprinusP. darwiniP. definitusP. gerbillusP. haggardiP. magisterP. osgoodiP. osilaeP. wolffsohniP. xanthopygus

Pithecheir [Genus]P. melanurus [Species]P. parvus

Phodopus [Genus]P. campbelli [Species]P. roborovskiiP. sungorus

Platacanthomys [Genus]P. lasiurus [Species]

Podomys [Genus]P. floridanus [Species]

Podoxymys [Genus]P. roraimae [Species]

Pogonomelomys [Genus]P. bruijni [Species]P. mayeriP. sevia

Pogonomys [Genus]P. championi [Species]P. loriaeP. macrourus

P. sylvestrisPraomys [Genus]

P. delectorum [Species]P. hartwigiP. jacksoniP. minorP. misonneiP. morioP. mutoniP. rostratusP. tullbergi

Prionomys [Genus]P. batesi [Species]

Proedromys [Genus]P. bedfordi [Species]

Prometheomys [Genus]P. schaposchnikowi [Species]

Psammomys [Genus]P. obesus [Species]P. vexillaris

Pseudohydromys [Genus]P. murinus [Species]P. occidentalis

Pseudomys [Genus]P. albocinereus [Species]P. apodemoidesP. australisP. bolamiP. chapmaniP. delicatulusP. desertorP. fieldiP. fumeusP. fuscusP. glaucusP. gouldiiP. gracilicaudatusP. hermannsburgensisP. higginsiP. johnsoniP. laborifexP. nanusP. novaehollandiaeP. occidentalisP. oralisP. patriusP. pilligaensisP. praeconisP. shortridgei

Pseudoryzomys [Genus]P. simplex [Species]

Punomys [Genus]P. lemminus [Species]

Rattus [Genus]R. adustus [Species]R. annandaleiR. argentiventerR. baluensisR. bontanusR. burrus



R. collettiR. elaphinusR. enganusR. everettiR. exulansR. feliceusR. foramineusR. fuscipesR. giluwensisR. hainaldiR. hoffmanniR. hoogerwerfiR. jobiensisR. koopmaniR. korinchiR. leucopusR. loseaR. lugensR. lutreolusR. macleariR. marmosurusR. mindorensisR. mollicomulusR. montanusR. mordaxR. morotaiensisR. nativitatisR. nitidusR. norvegicusR. novaeguineaeR. osgoodiR. palmarumR. pelurusR. praetorR. ranjiniaeR. rattusR. sanilaR. sikkimensisR. simalurensisR. sordidusR. steiniR. stoicusR. tanezumiR. tawitawiensisR. timorensisR. tiomanicusR. tunneyiR. turkestanicusR. villosissimusR. xanthurus

Reithrodon [Genus]R. auritus [Species]

Reithrodontomys [Genus]R. brevirostris [Species]R. burtiR. chrysopsisR. creperR. darienensisR. fulvescensR. gracilis

R. hirsutusR. humulisR. megalotisR. mexicanusR. microdonR. montanusR. paradoxusR. raviventrisR. rodrigueziR. spectabilisR. sumichrastiR. tenuirostrisR. zacatecae

Rhabdomys [Genus]R. pumilio [Species]

Rhagomys [Genus]R. rufescens [Species]

Rheomys [Genus]R. mexicanus [Species]R. raptorR. thomasiR. underwoodi

Rhipidomys [Genus]R. austrinus [Species]R. caucensisR. couesiR. fulviventerR. latimanusR. leucodactylusR. macconnelliR. mastacalisR. nitelaR. ochrogasterR. scandensR. venezuelaeR. venustusR. wetzeli

Rhizomys [Genus]R. pruinosus [Species]R. sinensisR. sumatrensis

Rhombomys [Genus]R. opimus [Species]

Rhynchomys [Genus]R. isarogensis [Species]R. soricoides

Saccostomus [Genus]S. campestris [Species]S. mearnsi

Scapteromys [Genus]S. tumidus [Species]

Scolomys [Genus]S. melanops [Species]S. ucayalensis

Scotinomys [Genus]S. teguina [Species]S. xerampelinus

Sekeetamys [Genus]S. calurus [Species]

Sigmodon [Genus]

S. alleni [Species]S. alstoniS. arizonaeS. fulviventerS. hispidusS. inopinatusS. leucotisS. mascotensisS. ochrognathus

Sigmodontomys [Genus]S. alfari [Species]S. aphrastus

Solomys [Genus]S. ponceleti [Species]S. salamonisS. salebrosusS. sapientisS. spriggsarum

Spalax [Genus]S. arenarius [Species]S. giganteusS. graecusS. microphthalmusS. zemni

Spelaeomys [Genus]S. florensis [Species]

Srilankamys [Genus]S. ohiensis [Species]

Stenocephalemys [Genus]S. albocaudata [Species]S. griseicauda

Steatomys [Genus]S. caurinus [Species]S. cuppediusS. jacksoniS. krebsiiS. parvusS. pratensis

Stenomys [Genus]S. ceramicus [Species]S. niobeS. richardsoniS. vandeuseniS. verecundus

Stochomys [Genus]S. longicaudatus [Species]

Sundamys [Genus]S. infraluteus [Species]S. maxiS. muelleri

Synaptomys [Genus]S. borealis [Species]S. cooperi

Tachyoryctes [Genus]T. ankoliae [Species]T. annectensT. audaxT. daemonT. macrocephalusT. naivashae



AM

MA

LSSP

EC

IES

LIST

T. rexT. ruandaeT. ruddiT. spalacinusT. splendens

Taeromys [Genus]T. arcuatus [Species]T. callitrichusT. celebensisT. hamatusT. punicansT. taerae

Tarsomys [Genus]T. apoensis [Species]T. echinatus

Tateomys [Genus]T. macrocercus [Species]T. rhinogradoides

Tatera [Genus]T. afra [Species]T. boehmiT. brantsiiT. guineaeT. inclusaT. indicaT. kempiT. leucogasterT. nigricaudaT. phillipsiT. robustaT. valida

Taterillus [Genus]T. arenarius [Species]T. congicusT. eminiT. gracilisT. harringtoniT. lacustrisT. petteriT. pygargus

Tscherskia [Genus]T. triton [Species]

Thallomys [Genus]T. loringi [Species]T. nigricaudaT. paedulcusT. shortridgei

Thalpomys [Genus]T. cerradensis [Species]T. lasiotis

Thamnomys [Genus]T. kempi [Species]T. venustus

Thomasomys [Genus]T. aureus [Species]T. baeopsT. bombycinusT. cinereiventerT. cinereusT. daphne

T. eleusisT. gracilisT. hylophilusT. incanusT. ischyurusT. kalinowskiiT. ladewiT. lanigerT. monochromosT. niveipesT. notatusT. oreasT. paramorumT. pyrrhonotusT. rhoadsiT. rosalindaT. silvestrisT. taczanowskiiT. vestitus

Tokudaia [Genus]T. muenninki [Species]T. osimensis

Tryphomys [Genus]T. adustus [Species]

Tylomys [Genus]T. bullaris [Species]T. fulviventerT. miraeT. nudicaudusT. panamensisT. tumbalensisT. watsoni

Typhlomys [Genus]T. chapensis [Species]T. cinereus

Uranomys [Genus]U. ruddi [Species]

Uromys [Genus]U. anak [Species]U. caudimaculatusU. hadrourusU. imperatorU. neobritanicusU. porculusU. rex

Vandeleuria [Genus]V. nolthenii [Species]V. oleracea

Vernaya [Genus]V. fulva [Species]

Volemys [Genus]V. clarkei [Species]V. kikuchiiV. millicensV. musseri

Wiedomys [Genus]W. pyrrhorhinos [Species]

Wilfredomys [Genus]W. oenax [Species]W. pictipes

Xenomys [Genus]X. nelsoni [Species]

Xenuromys [Genus]X. barbatus [Species]

Xeromys [Genus]X. myoides [Species]

Zelotomys [Genus]Z. hildegardeae [Species]Z. woosnami

Zygodontomys [Genus]Z. brevicauda [Species]Z. brunneus

Zyzomys [Genus]Z. argurus [Species]Z. mainiZ. palatilisZ. pedunculatusZ. woodwardi

Anomaluridae [Family]Anomalurus [Genus]

A. beecrofti [Species]A. derbianusA. peliiA. pusillus

Idiurus [Genus]I. macrotis [Species]I. zenkeri

Zenkerella [Genus]Z. insignis [Species]

Pedetidae [Family]Pedetes [Genus]

P. capensis [Species]

Ctenodactylidae [Family]Ctenodactylus [Genus]

C. gundi [Species]C. vali

Felovia [Genus]F. vae [Species]

Massoutiera [Genus]M. mzabi [Species]

Pectinator [Genus]P. spekei [Species]

Myoxidae [Family]Dryomys [Genus]

D. laniger [Species]D. nitedulaD. sichuanensis

Eliomys [Genus]E. melanurus [Species]E. quercinus

Glirulus [Genus]G. japonicus [Species]

Graphiurus [Genus]G. christyi [Species]G. huetiG. lorraineusG. monardiG. ocularis



G. parvusG. rupicola

Muscardinus [Genus]M. avellanarius [Species]

Myomimus [Genus]M. personatus [Species]M. roachiM. setzeri

Myoxus [Genus]M. glis [Species]

Selevinia [Genus]S. betpakdalaensis [Species]

Petromuridae [Family]Petromus [Genus]

P. typicus [Species]

Thryonomyidae [Family]Thryonomys [Genus]

T. gregorianus [Species]T. swinderianus

Bathyergidae [Family]Bathyergus [Genus]

B. janetta [Species]B. suillus

Cryptomys [Genus]C. bocagei [Species]C. damarensisC. foxiC. hottentotusC. mechowiC. ochraceocinereusC. zechi

Georychus [Genus]G. capensis [Species]

Heliophobius [Genus]H. argenteocinereus

Heterocephalus [Genus]H. glaber [Species]

Hystricidae [Family]Atherurus [Genus]

A. africanus [Species]A. macrourus

Hystrix [Genus]H. africaeaustralis [Species]H. brachyuraH. crassispinisH. cristataH. indicaH. javanicaH. pumilaH. sumatrae

Trichys [Genus]T. fasciculata [Species]

Erethizontidae [Family]Coendou [Genus]

C. bicolor [Species]C. koopmaniC. prehensilis

C. rothschildiEchinoprocta [Genus]

E. rufescens [Species]Erethizon [Genus]

E. dorsatum [Species]Sphiggurus [Genus]

S. insidiosus [Species]S. mexicanusS. pallidusS. spinosusS. vestitusS. villosus

Chinchillidae [Family]Chinchilla [Genus]

C. brevicaudata [Species]C. lanigera

Lagidium [Genus]L. peruanum [Species]L. viscaciaL. wolffsohni

Lagostomus [Genus]L. maximus [Species]

Dinomyidae [Family]Dinomys [Genus]

D. branickii [Species]

Caviidae [Family]Cavia [Genus]

C. aperea [Species]C. fulgidaC. magnaC. porcellusC. tschudii

Dolichotis [Genus]D. patagonum [Species]D. salinicola

Galea [Genus]G. flavidens [Species]G. spixii

Kerodon [Genus]K. rupestris [Species]

Microcavia [Genus]M. australis [Species]M. niataM. shiptoni

Hydrochaeridae [Family]Hydrochaeris [Genus]

H. hydrochaeris [Species]

Dasyproctidae [Family]Dasyprocta [Genus]

D. azarae [Species]D. coibaeD. cristataD. fuliginosaD. guamaraD. kalinowskiiD. leporinaD. mexicana

D. prymnolophaD. punctataD. ruatanica

Myoprocta [Genus]M. acouchy [Species]M. exilis

Agoutidae [Family]Agouti [Genus]

A. paca [Species]A. taczanowskii

Ctenomyidae [Family]Ctenomys [Genus]

C. argentinus [Species]C. australisC. azaraeC. boliviensisC. bonettoiC. brasiliensisC. colburniC. conoveriC. dorsalisC. emilianusC. fraterC. fulvusC. haigiC. knightiC. latroC. leucodonC. lewisiC. magellanicusC. maulinusC. mendocinusC. minutusC. nattereriC. occultusC. opimusC. pearsoniC. perrensisC. peruanusC. pontifexC. porteousiC. saltariusC. sericeusC. sociabilisC. steinbachiC. talarumC. torquatusC. tuconaxC. tucumanusC. validus

Octodontidae [Family]Aconaemys [Genus]

A. fuscus [Species]A. sagei

Octodon [Genus]O. bridgesi [Species]O. degusO. lunatus



AM

MA

LSSP

EC

IES

LIST

Documents

Grzimek animal life encyclopedia volume 12 mammals i