Proc. Natl. Acad. Sci. USAVol. 93, pp. 6405-6409, June 1996Evolution

A new extinct primate among the Pleistocene megafauna ofBahia, Brazil

(New World monkeys/paleontology/Atelinae)

CASTOR CARTELLE* AND WALTER CARL HARTWIGt*Instituto de Geociencias, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil; and tDepartment of Anthropology, George WashingtonUniversity, Washington, DC 20052

Communicated by F. Clark Howell, University of California, Berkeley, CA, February 12 1996 (received for review November 1, 1995)

ABSTRACT A nearly complete skeleton of a robust-bodied New World monkey that resembles living spider mon-keys was recovered from undisturbed Pleistocene deposits inthe Brazilian state of Bahia. The skeleton displays the highlyspecialized postcranial pattern typical of spider and woollyspider monkeys and shares cranial similarities to the spidermonkey exclusively. It is generically distinct on the basis of itsrobustness (>20 kg) and on the shape of its braincase. Thisnew genus indicates that New World monkeys nearly twice thesize of those living today were part of the mammalian biomassof southern Amazonia in the late Pleistocene. The discovery ofthis specimen expands the known adaptive diversity of NewWorld monkeys and demonstrates that they underwent bodysize expansion in the terminal Pleistocene, as did many othertypes of mammals.

Anthropoid primates colonized South America in the earlypart of the Tertiary (>30 million years ago) and radiatedwidely throughout the neotropics. Sixteen New World mon-key genera survive today, all of which are arboreal andrelatively small-bodied compared with most Old Worldanthropoids. Four living genera (Alouatta, Ateles, Brachy-teles, and Lagothrix) are closely related to one another andare distinct among New World monkeys for their relativelylarge body size (6-12 kg), suspensory postures, and prehen-sile tails (1-3). They are usually classified in a separatesubfamily, Atelinae, within which the howler monkey (Al-ouatta) is considered less closely related to the other threethan they are to each other (2). Ateles and Brachyteles arefurther distinguished by a specialized postcranial adaptationto a brachiating mode of locomotion, in which the forelimbsare relatively elongated (3). The Pleistocene skeleton de-scribed here resembles the spider monkey (Ateles) more thanit does any other living genus. However, this skeleton isunusually robust, and its neurocranium is more roundedcompared with any living or extinct ateline.

DEPOSITIONAL CONTEXT

The fossil skeleton was discovered in 1992 in Toca da BoaVista, a cave in the Brazilian state of Bahia (Fig. 1). Theskeleton was found in an undisturbed deposit in a chamber thatalso contained other Pleistocene fossils and a nearly completeskeleton of a second large platyrrhine referred to ProtopithecusLund, 1838 (4-5). Toca da Boa Vista is an extensive limestonetravertine with over 100 km of interfingering galleries. The fossilswere recovered in a chamber along the northeastern wall of thecave several hundred meters from the principal entrance. The

Table 1. Mammals discovered in Toca da Boa Vista

Order Species

Chiroptera Mormoops megalophyllaPteronotus parnelliChrotopterus auritusLoncophylla mordaxDesmodus rotundus+Desmodus draculaeEptesicus brasiliensisTadarida brasiliensis

Edentata + Nothrotherium maquinense+ Scelidodon cuvieriMyrmecophaga tridactylaEuphractus sexcistus

Rodentia Coendou prehensilisArtiodactyla Tayassu tajacu

Lama guanicoeMazama gouazoubira

Carnivora Cerdocyon thous+ Protocyon troglodytes+Arctotherium brasilienseProcyon cancrivorusConepatus semistriatusFelis pardalisFelis tigrinaFelis yagouaroundiFelis concolor+ Smilodon populator

Primates + Protopithecus brasiliensis+ Caipora bambuiorum

The plus sign indicates extinct species.

relative completeness of several fossil skeletons in this chambersuggests that the sediments were in primary depositional contextat the time of discovery.

Systematics. The order is Primates (Linnaeus, 1758); thesuborder is Haplorhini (Pocock, 1918); the infraorder isPlatyrrhini (E. Geoffroy, 1812); the subfamily is Atelinae(Gray, 1825); the tribe is Atelini (Gray, 1825); the genus isCaipora; and the species is Caipora bambuiorum.Type Specimen. IGC-UFMG 05 (Instituto de Geociencias -

Universidade Federal de Minas Gerais) is a nearly completeskeleton of a late-stage subadult, including cranium, mandible,axial skeleton including caudal vertebrae, incomplete scapulaeand pelvis, upper and lower limb long bones, carpals, tarsals,metacarpals, metatarsals, and numerous phalanges.Age and Locality. Toca da Boa Vista is located at 40o51'39R W

longitude and 10°09'36" S latitude at an altitude of 600 m abovemean sea level. No radiometric dates are available from thedeposits, but other mammalian taxa found in the same sedimen-tary context represent a mix of living and extinct Pleistocenespecies (Table 1). Pending a more precise radiometric assessment,

6405

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+ 8°420

State of Bahia

+ 8°38°

FIG. 1. The location of Toca da Boa Vista in the northern part of the state of Bahia, Brazil, is shown.

A

V e1cm 1cm

FIG. 2. Anterior (A), lateral (B), and posterior (C) views of the cranium of IGC-UFMG 05, type specimen of Caipora bambuiorum.

Table 2. Cranial measurements for Caipora and the four genera of living ateline New World monkeys

Caipora (1) Ateles (92) Brachyteles (11) Lagothrix (73) Alouatta (25)NCL 94.1 77.9 86.6 73.7 61.2

68.5-84.4 79.8-91.7 67.0-81.2 54.9-68.8NCB 75.4 60.8 61.9 58.6 51.0

54.9-65.7 57.7-65.1 - 53.8-63.1 47.3-56.2TSL 131.5 114.1 114.8 104.9 107.6

104.0-122.0 100.0-122.0 97.2-114.6 96.3-121.4BAS-NAS 77.2 63.3 68.2 63.1 64.9

55.4-71.9 58.2-74.4 57.9-70.0 57.6-78.2PL 40.6 34.4 38.7 31.6 39.9

29.9-40.7 34.2-44.1 26.2-37.4 34.7-59.9BOB 63.3 55.6 57.3 54.0 52.3

49.9-64.2 52.0-61.2 47.9-59.0 47.2-60.7

NCL, neurocranial length; NCB, neurocranial breadth; TSL, total skull length; BAS-NAS, basion-nasion; PL, palate length;BOB, biorbital breadth. Sample sizes are in parentheses. All measurements are in millimeters.

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4.32 4.44 4.56 4.68 4.80Cranial Size Composite

4.4

4.3 -

42k

TE;4.1hP:

. 4.0

Z 3.9 V

3.84.20 4.32 4.44 4.56

B _* _~

It

EI

X

c.

Q

4.68 4.80

Cranial Size Composite

0.5

0.4 -

0.3 L

0.1 L

.4-

4.20 4.32 4.44 4.56 4.68Cranial Size Composite

FIG. 3. Log-log plots of cranial dimensions on overall cranial size [(total skull length + basicranial length + facial length + basion-nasion)/4]for living atelines and Caipora. The ellipse represents 90% of the variation in the Ateles, Brachyteles and Lagothrix sample. Neurocranial length(A) and breadth (B) of Caipora have opposite relative relationships to the distribution of living species, such that a measure of their differential(C) demonstrates a more spherical neurocranium than is typical in living atelines.

A B

FIG. 4. Drawings of the palate(A) and mandible (B) of Caipora

1 cm bambuiorum, in occlusal view.

Table 3. Postcranial measurements for Caipora and the four genera of living ateline NewWorld monkeys

Caipora (1) Ateles (31) Brachyteles (3) Lagothrix (17) Alouatta (25)FHD 22.9 17.9 18.2 15.0 13.4

15.8-20.2 16.9-19.8 14.0-15.7 11.8-15.9FL 216* 205.6 202.0 166.4 154.2

190.5-226.0 186.5-212.0 157.5-176.5 139.0-171.0BCB 38.5 31.8 29.0 27.1 23.9

29.1-34.9 28.0-30.9 24.2-29.3 21.4-26.7HHD 25.1 20.5 19.8 20.1 19.8

17.8-24.1 18.2-21.6 18.6-22.2 16.9-23.1HL 222.0 207.3 208.7 - 166.2 145.9

184.5-225.5 192.0-223.0 154.5-177.0 129.0-165.0BIEPI 37.7 30.9 30.0 28.0 26.6

28.5-33.2 26.7-33.0 25.6-30.0 22.5-30.8I-I 1.06* 1.05 1.07 0.98 0.95

1.01-1.07 1.05-1.08 0.96-1.00 0.92-0.98FV 70 ml 40 ml 20 ml 20 ml

FHD, femoral head diameter; FL, femoral length; BCB, femoral bicondylar breadth; HHD, humeralhead diameter; HL, humeral length; BIEPI, humeral biepicondylar breadth; I-I, intermembral index(forelimb length/hindlimb length); FV, femoral volume (measured by water displacement in a graduatedcylinder). Sample sizes are in parentheses. All measurements are in millimeters except where indicated.*Measurements that reflect incomplete growth of the fossil.

4.60

4.48 k

'Z )J'I IVAor7

A A teles, Wyy BrachivteheS- L-agothliv.r Al99ittilit/ Z A

;

c)

C

C.)z

4.36 F

4.24 H

4.12 K

4.00;4.20 4.80

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FIG. 5. Selected postcranial elements of Caipora bambuiorum. (A) Anteriorview of left humeri of (left to right)Atelespaniscus, C. bambuiorum,Lagothrix lagotricha, and Alouatta belzebul. (B) Right and left ulnae of C. bambuiorum. (C) Incomplete left innominate of C. bambuiorum. (D)Anterior view of right femur of (left to right) Ateles paniscus, C. bambuiorum, Lagothrix lagotricha, and Alouatta belzebul. (E) Reconstructed leftfoot of C. bambuiorum.

an age of late Pleistocene/early Holocene (ca. 10,000 B.P.) isassigned based on this faunal correlation.

Etymology. Caipora (ky-por-ah), after Caipora, a creature ofnative South American folklore described by Peter Wilhelm

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Lund, a Danish naturalist and father of Brazilian paleontology, in1836: "the district here mentioned is even yet inhabited by a verylarge ape, to which the Indians have given the name Caypore,which signifies the dweller in the wood" (ref. 6, see p. 315);bambuiorum, after Bambui + -orum, in recognition of GrupoBambui de Pesquisas Espeleologicas of Belo Horizonte, thespeleological team that discovered the fossils in Toca da BoaVista in 1992.

Diagnosis. Large-bodied (>20 kg) New World monkey char-acterized by a robust postcranium, spherical and capacious neu-rocranium, a projecting premaxilla, bunodont dentition, and a highforelimb/hindlimb length ratio. It is distinguished from non-atelines by its large size and postcranial adaptation to suspensionand brachiation. Compared with atelines (Alouatta, Ateles,Brachyteles, and Lagothrix), it is distinguished fromAlouatta by theabove-mentioned characters, its neurocranial shape and size, andin lacking cranial modifications for an enlarged hyo-laryngealapparatus (i.e., a flat, caudally directed nuchal plane and anextended basicranium). It is distinguished from Lagothrix andAteles by its postcranial robustness, the rounded shape of itsneurocranium, and in having a relatively more projecting premax-illa. It is further distinguished from Brachyteles in lacking molarshearing crests. It is distinguished from Protopithecus by having aless robust postcranium, particularly in the areas of gluteal andforelimb flexion musculature, and a larger, more rounded neuro-cranium. Species diagnosis, C. bambuiorum: as for genus.

DESCRIPTIONThe neurocranium of Caipora is large and globose (Fig. 2). Thebraincase ascends above the supraorbital rim, and the maximumbreadth is found high on the parietals, giving the neurocraniuma more rounded contour than is typical of New World monkeys.Its neurocranial length and, in particular, its neurocranial breadthexceed that of any known platyrrhine (Table 2). A comparison ofthese dimensions relative to overall cranial size demonstrates thatthe neurocranium of Caipora is more spherical than the neuro-crania of other New World monkeys (Fig. 3). The temporal linesare faint and pass parallel to one another along the supero-lateralaspect of the neurocranium. The facial skeleton displays a gracilecircum-orbital region and ovoid orbits that are similar to Ateles.All cranial sutures are closed, and both upper and lower thirdmolars are fully occluded and worn.The mandible and dentition bear the most striking resem-

blance to Ateles (Fig. 4). Premolar and molar cusp configu-ration is remarkably similar to Ateles and Lagothrix. Upperand lower molars are quadrate, and the occlusal morphology isbunodont and relatively undeveloped, as inAteles. The lower thirdmolar is set in the corpus of the mandible, not along the base ofthe ascending ramus as in Alouatta and Brachyteles. Length andbreadth tooth dimensions in Caipora are not significantly greaterthan those in large Ateles individuals.The postcranial skeleton, although not yet fully grown, is

more robust than that of any living New World monkey(Table 3). Limb proportions and articular morphology re-flect the same suite of adaptations to suspensory posture andbrachiating locomotion that characterizes spider and woollyspider monkeys (Fig. 5). Signatures of this unusual below-branch habitus include extremely long upper limbs, mobilegleno-humeral articular morphology, metacarpals subequalin length to metatarsals, and relatively robust proximalcaudal vertebrae (3, 7-8). Caipora displays a sphericalhumeral head, straight humeral shaft, relatively short ulnarolecranon process, and radial articular facet flush with theshaft of the ulna. These features and its intermembral indexare all characteristic of brachiating New World monkeys.

DISCUSSIONIt is difficult to estimate the body weight of Caipora accurately.Postcranial elements are considerably more robust, but not

significantly longer, than their complements in living atelines(Table 3 and Fig. 5). Based on a formula for calculating bodymass in primates from articular dimensions {logio(femoralhead volume) = 1.196[logio(body mass)] + 2.234} (9), thisCaipora individual probably weighed 20.5 kilograms. Thisweight is approximately 75% 'greater than the highest weightsreported for living atelines (10).The late Pleistocene paleoenvironment of this region of

Bahia may have been similar to current conditions, withhillside forests to the north and along river margins to thesouth, and level terrain covered by low vegetation (rasteira), asandy, soil-poor sedimentary complex. Pleistocene mammalsfrom other caves in the region include such taxa as Toxodon,Eremotherium, and Haplomastodon, suggesting that the area atthat time period provided sufficient grazing cover to supportmegaherbivores. The forest cover, however, appears to havebeen more prominent and diversified than it is today, insofaras it supported the larger biomass ofNew World monkeys suchas Caipora bambuiorum.With the exception of Caipora and Protopithecus (4, 11),

Pleistocene New World monkeys are known primarily fromisland deposits in the Caribbean (12-13). The insular Pleisto-cene platyrrhines are difficult to integrate into the evolution-ary history of living genera and in some cases display unusualpostcranial morphologies (14). Caipora, by contrast, is clearlyrelated to a distinct lineage of living New World monkeys, theatelines. Its body size and apparent phylogenetic affinity tospider monkeys make it a remarkable addition to the adaptivediversity of neotropical primates. It further demonstrates thatplatyrrhines were a part of the megafauna characteristic of theterminal Pleistocene in South America (15).

The fossils of Toca da Boa Vista were discovered by the membersof Grupo Bambui de Pesquisas Espeleologicas of Belo Horizonte. Wewould especially like to thank Mauro A. Chagas Ferreira and RodrigoLopes F. for help in the field and Humberto do Espirito Santo for theartwork. John Fleagle and Alfred Rosenberger facilitated our collab-oration and provided many helpful suggestions. Assistance and helpfuladvice was also offered by William Jungers, Dan Gebo, and MiguelSchon Ybarra. We thank S. Franco, L. Oliviera, and G. Wilson Nunanof the Museu Nacional in Rio de Janeiro; R. Thorington of theNational Museum of Natural History; B. Patterson of the FieldMuseum of Natural History; and R. D. E. MacPhee of the AmericanMuseum of Natural History for access to comparative specimens.Laboratory and photographic support was provided by PontificiaUniversidade Catolica de Minas Gerais and Universidade Federal deMinas Gerais. This research was supported by a grant from the LSBLeakey Foundation.

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3. Erickson, G. E. (1963) Symp. Zool. Soc. London 10, 135-164.4. Cartelle, C. (1993) Neotropical Primates 1, 8.5. Cartelle, C. & Ferreira, M. A. C. (1994) Acta Geol. Leopold. 17,

411-414.6. Lund, P. W. (1840) Charles. Mag. Nat. Hist., Vol. 4.7. German, R. M. (1982) Am. J. Phys. Anthropol. 58, 453-459.8. Meldrum, D. J. & Lemelin, P. (1991)Am. J. Primatol. 25, 69-89.9. Ruff, C. B. (1990) in Body Size in Mammalian Paleobiology:

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