IRCFREPTILES&AMPHIBIANS•21(3):93–95•SEP2014

Body-inversion in the Cuban Racer, Cubophis cantherigerus cantherigerus (Dipsadidae):

Death-feigning or Warning Signal?Tomás M. Rodríguez-Cabrera1, Javier Torres2, and Ruben Marrero Romero3

1JardínBotánicodeCienfuegos,PepitoTey,Cienfuegos,CP59290,Cuba(tomasmichel.rodriguez@gmail.com)2DepartamentodeBiologíaAnimalyHumana,FacultaddeBiología,UniversidaddelaHabana,LaHabana,CP10400,Cuba(javiertorres@fbio.uh.cu)

3DivisióndeZoologíadeVertebrados,InstitutodeEcologíaySistemática,LaHabana,CP11900,Cuba(rubens@ecologia.cu)

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IRCF REPTILES & AMPHIBIANS • VOL15, NO 4 • DEC 2008 189TABLE OF CONTENTS

T A B L E O F C O N T E N T S

F E A T U R E A R T I C L E S

Chasing Bullsnakes (Pituophis catenifer sayi) in Wisconsin: On the Road to Understanding the Ecology and Conservation of the Midwest’s Giant Serpent ...................... Joshua M. Kapfer 190

The Shared History of Treeboas (Corallus grenadensis) and Humans on Grenada: A Hypothetical Excursion ............................................................................................................................Robert W. Henderson 198

R E S E A R C H A R T I C L E S

The Texas Horned Lizard in Central and Western Texas ....................... Emily Henry, Jason Brewer, Krista Mougey, and Gad Perry 204 The Knight Anole (Anolis equestris) in Florida

.............................................Brian J. Camposano, Kenneth L. Krysko, Kevin M. Enge, Ellen M. Donlan, and Michael Granatosky 212

C O N S E R V A T I O N A L E R T

World’s Mammals in Crisis ............................................................................................................................................................. 220 More Than Mammals ...................................................................................................................................................................... 223 The “Dow Jones Index” of Biodiversity ........................................................................................................................................... 225

H U S B A N D R Y

Captive Care of the Central Netted Dragon ....................................................................................................... Shannon Plummer 226

P R O F I L E

Kraig Adler: A Lifetime Promoting Herpetology ................................................................................................ Michael L. Treglia 234

C O M M E N T A R Y

The Turtles Have Been Watching Me ........................................................................................................................ Eric Gangloff 238

B O O K R E V I E W

Threatened Amphibians of the World edited by S.N. Stuart, M. Hoffmann, J.S. Chanson, N.A. Cox, R. Berridge, P. Ramani, and B.E. Young .............................................................................................................. Robert Powell 243

CONSERVATION RESEARCH REPORTS: Summaries of Published Conservation Research Reports ................................. 245 NATURAL HISTORY RESEARCH REPORTS: Summaries of Published Reports on Natural History ................................. 247 NEWBRIEFS ...................................................................................................................................................................................... 248 EDITORIAL INFORMATION ..................................................................................................................................................... 251 FOCUS ON CONSERVATION: A Project You Can Support ............................................................................................... 252

Front Cover. Shannon Plummer.Totat et velleseque audant mo estibus inveliquo velique rerchil erspienimus, quos accullabo. Ilibus aut dolor apicto invere pe dolum fugiatis maionsequat eumque moditia erere nonsedis ma sectiatur ma derrovitae voluptam, as quos accullabo.

Back Cover. Michael KernTotat et velleseque audant mo

estibus inveliquo velique rerchil erspienimus, quos accullabo. Ilibus

aut dolor apicto invere pe dolum fugiatis maionsequat eumque

moditia erere nonsedis ma sectia-tur ma derrovitae voluptam, as

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Predationisamongthemainselectivepressuresthatdrivebiologicalevolution(e.g.,Futuyma2013).Snakesarefre-

quentpreyofothervertebrates.Toavoidpredation,theyhavedevelopedawidevarietyofdefensivebehaviors(seeGreene1994forareview).Anti-predationbehaviorsreportedforWestIndiancolubroidsincludeimmobility,tail-waving,con-cealment,locomotorescape,anteriorbody-raisinganddor-soventralcobra-likeneck-flattening,gaping,strike-feigning,biting,balling,cloacaldischarge,meal-disgorging,andrapidbodyrotationwhencaptured(seeHendersonandPowell2009forareview). Theseanti-predationbehaviorsarerelativelysimpleandgeneralizedformostsnakes(e.g.,Mattison1995),butafewspeciescandisplaymorecomplexpatterns,includingdeath-feigning.Thisisastateofexternalunresponsivenesstotactilestimulation,exhibitedasalast-resortanti-predationtacticforanindividualunabletoevadecapturebyapredator(e.g.,Greene1994,Caro2005,Gregory2008).Death-feigningcanincludebody-inversion,kinetic(or“erratic”)display,tonicimmobility,limp-mouthgape,tongue-hanging,eyerotation,autohemorrhaging,cloacaldischarge,andevenbradycardia(e.g.,Heterodon platirhinos;seePlatt1969,Gehlbach1970,McDonald1974).Body-inversionusuallyoccursinassocia-tionwithdeath-feigning(e.g.,Platt1969,Gehlbach1970),butGreene(1994)consideredthemindependentbehaviors(althoughheemphasizedthattheyfrequentlyappearincom-bination).Consistentwiththeseparationofbothbehaviors,awarningfunctionhasalsobeensuggestedforbody-inversion,particularlyforcertaindeath-feigningcolubroidswithstrik-inglymarkedventerssuchasHeterodon nasicus, Natrix natrix, and Diadophis punctatus(HeusserandSchlumpf1962). Death-feigning has beenwidely documented in thefamilies Colubridae, Dipsadidae, Natricidae, Elapidae,Leptotyphlopidae, andTropidophiidae (for a review seeGreene1994).However,neitherdeath-feigningsensu lato nor

body-inversion sensu strictohaveeverbeenreportedforanyWestIndiansnakes.Hereinwereportbody-inversionbehav-iorintheCubanRacer,Cubophis cantherigerus cantherigerus (Bibron1840),fromwesternCuba,anddiscussitspossiblerelationshiptodeath-feigningorwarningsignal.

Fig. 1.ACubanRacer(Cubophis c. cantherigerus)fromtheJardínBotánicoNacionaldeCubaexhibitingacobra-likedefensiveposture.PhotographbyNancydelaC.Llevat.

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On6January2012,at1500h,weobservedaCubanRacer (ca. 120 cm total length) pursuing aCubanTreeFrog (Osteopilus septentrionalis,Hylidae) in a bromeliad(Tillandsia valenzuelana)onatreeca.3.5maboveground

levelattheJardínBotánicoNacionaldeCuba(23°00’00”N,82°20’50”W;Datum:NAD27forCuba),ArroyoNaranjo,LaHabanaProvince,Cuba.Thefrogjumpedtothegroundandthesnakerapidlyfollowed.Onceontheground,fourphotographerssurroundedthesnake.Abouttwominutesafterthephotographersstartedtheirwork,thesnakeadoptedthecobra-likedefensiveposturetypicalofthisspeciesandotheralsophiines (Fig.1; seealsoHendersonandPowell2009).Eachtimethesnakeattemptedtoescapeitwasinter-ceptedbyoneofthephotographers,butnevertouched.Aftereightminutesofcontinuousharassmentthesnakelowereditshead(Fig.2)andsuddenlyrolledonitsbackandadoptedaninvertedsemicoiledposture,withtheheadbentslightlyupward(Fig.3).Thesnakeremainedinvertedforlessthanoneminutebefore reverting to thenormalposition andresumingthecobra-likedefensivepostureforaboutfivemoreminutes,afterwhichitwasallowedtoescape.Thesnakewasnotsubjectedtoanyadditionaldisturbanceduringthetimeitremained inverted. Weconsiderthisbehaviorasaparticularcaseofdeath-feigning,lesselaboratethanthestereotypedbehaviorsobservedincontinentalspeciesofthegeneraHeterodon, Masticophis, Diadophis, and Natrix (e.g.,Platt 1969,Gehlbach1970,

IRCFREPTILES&AMPHIBIANS•21(3):93–95•SEP2014RODRIGUEZ-CABRERAETAL.

Fig. 3.Thesamesnakeinaninvertedposition.PhotographbyRaimundoLópez-Silvero.

Fig. 2.The sameCubanRacer lowering itshead in transition toaninvertedposture.PhotographbyRobertoCruz.

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RODRIGUEZ-CABRERAETAL. IRCFREPTILES&AMPHIBIANS•21(3):93–95•SEP2014

Greene1994).Theindividualdescribedhereindidnotgape,extenditstongue,ordischargeitsscentglands,anditrapidlyrevertedtoanormalposture.However,wecannotidentifyanapparentadvantageother than those related todeath-feigning.Removalofcues(e.g.,movement)thatelicitprey-killingbehaviorinapotentialvertebratepredatorseemsrea-sonenoughtoadoptdeath-feigning,sinceitmightprovideananimalwithsubsequentopportunitiesforescape(Alcock1975,Gregory2008).Theanti-predationfunctionofdeath-feigningmaylieindirectinterferencewiththepredator’sabil-itytoconsumetheprey(Honmaetal.2006).However,itmayalsodependonthepredatornotimmediatelyconsumingimmobileprey,therebygivingthepotentialpreyawindowofopportunitytoescapeifthepredatorisevenmomentarilyinattentiveordistracted(Gregory2008). Analternativeexplanationforthisbehaviorisasawarn-ingsignal,butthisindividuallackedaposematiccolorationonitsventralregion(whichistheruleforitsconspecifics,butseebelow).AninvertedpositioncouldbeassumedbytheCubanRacerafterprolongedharassmentwithoutdirectaggression,andasalast-resorttacticafterfailureofotheranti-predationmecha-nisms(e.g.,locomotorescapeorthecobra-likeposture).Death-feigninginotherspecies(e.g.,H. platirhinos and Naja haje)alsocomesattheendofarepertoireofotherdefensivebehaviors,includingintimidationandodorproduction(Mattison1995). Despitethelackofaposematiccolorationintheindivid-ualdescribedabove,SchwartzandHenderson(1991)men-tioned one pattern of C. cantherigerus thatincludesposteriorventralscales“sometimesentirelyred,usuallydarkwithmoreorlessbold,redoryellowblotching.”TheseniorauthorhasobservedindividualsofC. c. cantherigerus and C. c. schwartzi withposteriorblackandredventralmarkings. Some indi-vidualsofC. c. pepeifromeasternCubapossessbluethroatsandbicoloredbellies(SchwartzandThomas1960).SomespecimensfromthePenínsuladeGuanahacabibeshaveven-tralscaleswithyellowventralmarkings(J.Torres,pers.obs.). Furthermore, C. cantherigerus is known to haveDuvernoy’sglandsandavenomousbite(Neill1954,JaumeandGarrido1980),whichsupporttheideathatstrikingven-

tralcolorationandbody-inversioncouldserveasawarningsignal.However,additionalobservationsarerequiredtocor-roboratebody-inversioninthisspeciesandtoelucidatetrig-gering factors and function.

AcknowledgementsRaimundoLópez-Silvero,NancydelaC.Llevat,andRobertoCruzprovidedvaluable information.Wecalculated timeframesforeachbehaviorfromtheirphotographicsequences.

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