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Home , Atelinae, Caipora (monkey), Howler monkey, New World monkey, Protopithecus, Scelidodon

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

A new extinct among the megafauna of Bahia, ( monkeys/paleontology/) CASTOR CARTELLE* AND WALTER CARL HARTWIGt *Instituto de Geociencias, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil; and tDepartment of Anthropology, George Washington University, 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- Table 1. discovered in Toca da Boa Vista bodied New World that resembles living spider mon- Order keys was recovered from undisturbed Pleistocene deposits in the Brazilian state of Bahia. The skeleton displays the highly Chiroptera Mormoops megalophylla specialized postcranial pattern typical of spider and woolly Pteronotus parnelli spider monkeys and shares cranial similarities to the spider Chrotopterus auritus monkey exclusively. It is generically distinct on the basis of its Loncophylla mordax robustness (>20 kg) and on the shape of its braincase. This Desmodus rotundus new indicates that New World monkeys nearly twice the +Desmodus draculae size of those living today were part of the mammalian biomass Eptesicus brasiliensis of southern Amazonia in the . The discovery of Tadarida brasiliensis this specimen expands the known adaptive diversity of New Edentata + maquinense World monkeys and demonstrates that they underwent body + Scelidodon cuvieri size expansion in the terminal Pleistocene, as did many other Myrmecophaga tridactyla types of mammals. Euphractus sexcistus Rodentia Coendou prehensilis Artiodactyla Tayassu tajacu Anthropoid colonized in the early Lama guanicoe part of the Tertiary (>30 million years ago) and radiated Mazama gouazoubira widely throughout the neotropics. Sixteen New World mon- Carnivora Cerdocyon thous key genera survive today, all of which are arboreal and + Protocyon troglodytes relatively small-bodied compared with most Old World + brasiliense anthropoids. Four living genera (Alouatta, Ateles, Brachy- Procyon cancrivorus teles, and Lagothrix) are closely related to one another and Conepatus semistriatus are distinct among New World monkeys for their relatively Felis pardalis large body size (6-12 kg), suspensory postures, and prehen- Felis tigrina sile tails (1-3). They are usually classified in a separate Felis yagouaroundi subfamily, Atelinae, within which the (Al- Felis concolor ouatta) is considered less closely related to the other three + populator than they are to each other (2). Ateles and Brachyteles are Primates + brasiliensis further distinguished by a specialized postcranial adaptation + bambuiorum to a brachiating mode of locomotion, in which the forelimbs are relatively elongated (3). The Pleistocene skeleton de- The plus sign indicates extinct species. scribed here resembles the (Ateles) more than relative completeness of several fossil skeletons in this chamber it does any other living genus. However, this skeleton is suggests that the sediments were in primary depositional context unusually robust, and its neurocranium is more rounded at the time of discovery. compared with any living or extinct ateline. Systematics. The order is Primates (Linnaeus, 1758); the suborder is (Pocock, 1918); the infraorder is Platyrrhini (E. Geoffroy, 1812); the subfamily is Atelinae DEPOSITIONAL CONTEXT (Gray, 1825); the tribe is Atelini (Gray, 1825); the genus is The fossil skeleton was discovered in 1992 in Toca da Boa Caipora; and the species is Caipora bambuiorum. Vista, a cave in the Brazilian state of Bahia (Fig. 1). The Type Specimen. IGC-UFMG 05 (Instituto de Geociencias - skeleton was found in an undisturbed deposit in a chamber that Universidade Federal de Minas Gerais) is a nearly complete also contained other Pleistocene fossils and a nearly complete skeleton of a late-stage subadult, including cranium, mandible, skeleton of a second large platyrrhine referred to Protopithecus axial skeleton including caudal vertebrae, incomplete scapulae Lund, 1838 (4-5). Toca da Boa Vista is an extensive limestone and pelvis, upper and lower limb long bones, carpals, tarsals, travertine with over 100 km of interfingering galleries. The fossils metacarpals, metatarsals, and numerous phalanges. were recovered in a chamber along the northeastern wall of the Age and Locality. Toca da Boa Vista is located at 40o51'39R W cave several hundred meters from the principal entrance. The longitude and 10°09'36" S latitude at an altitude of 600 m above mean sea level. No radiometric dates are available from the The publication costs of this article were defrayed in part by page charge deposits, but other mammalian taxa found in the same sedimen- payment. This article must therefore be hereby marked "advertisement" in tary context represent a mix of living and extinct Pleistocene accordance with 18 U.S.C. §1734 solely to indicate this fact. species (Table 1). Pending a more precise radiometric assessment, 6405 Downloaded by guest on September 29, 2021 6406 Evolution: Cartelle and Hartwig Proc. Natl. Acad. Sci. USA 93 (1996)

+ 8° + 8° 420 38° State of Bahia

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

V e 1cm 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 54.9-68.8 NCB 75.4 60.8 61.9 58.6 51.0 54.9-65.7 57.7-65.1 - 53.8-63.1 47.3-56.2 TSL 131.5 114.1 114.8 104.9 107.6 104.0-122.0 100.0-122.0 97.2-114.6 96.3-121.4 BAS-NAS 77.2 63.3 68.2 63.1 64.9 55.4-71.9 58.2-74.4 57.9-70.0 57.6-78.2 PL 40.6 34.4 38.7 31.6 39.9 29.9-40.7 34.2-44.1 26.2-37.4 34.7-59.9 BOB 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. Downloaded by guest on September 29, 2021 Evolution: Cartelle and Hartwig Proc. Natl. Acad. Sci. USA 93 (1996) 6407

4.60 4.4 0.5 'Z )J'I IV B _ * Aor 7 _~ 4.48 k A A teles, W 4.3 - 0.4 - yy BrachivteheS EI - L-agothliv. X c) 42k c. 4.36 F r Al99ittilit/ ZA I It 0.3 L TP: C E;4.1h --7' .4- 4.24 H ; . 4.0 C.) z 4.12 K Z 0.1 L 3.9 V Q

4.00; 3.8 4.20 4.32 4.44 4.56 4.68 4.80 4.20 4.32 4.44 4.56 4.68 4.80 4.20 4.32 4.44 4.56 4.68 4.80 Cranial Size Composite Cranial Size Composite Cranial 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 New World 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 11.8-15.9 FL 216* 205.6 202.0 166.4 154.2 190.5-226.0 186.5-212.0 157.5-176.5 139.0-171.0 BCB 38.5 31.8 29.0 27.1 23.9 29.1-34.9 28.0-30.9 24.2-29.3 21.4-26.7 HHD 25.1 20.5 19.8 20.1 19.8 17.8-24.1 18.2-21.6 18.6-22.2 16.9-23.1 HL 222.0 207.3 208.7 - 166.2 145.9 184.5-225.5 192.0-223.0 154.5-177.0 129.0-165.0 BIEPI 37.7 30.9 30.0 28.0 26.6 28.5-33.2 26.7-33.0 25.6-30.0 22.5-30.8 I-I 1.06* 1.05 1.07 0.98 0.95 1.01-1.07 1.05-1.08 0.96-1.00 0.92-0.98 FV 70 ml 40 ml 20 ml 20 ml FHD, femoral head diameter; FL, femoral length; BCB, femoral bicondylar breadth; HHD, humeral head 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 graduated cylinder). Sample sizes are in parentheses. All measurements are in millimeters except where indicated. *Measurements that reflect incomplete growth of the fossil. Downloaded by guest on September 29, 2021 6408 Evolution: Cartelle and Hartwig Proc. Natl. Acad. Sci. USA 93 (1996)

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 left foot of C. bambuiorum.

an age of late Pleistocene/early (ca. 10,000 B.P.) is Etymology. Caipora (ky-por-ah), after Caipora, a creature of assigned based on this faunal correlation. native South American folklore described by Peter Wilhelm Downloaded by guest on September 29, 2021 Evolution: Cartelle and Hartwig Proc. Natl. Acad. Sci. USA 93 (1996) 6409 Lund, a Danish naturalist and father ofBrazilian paleontology, in significantly longer, than their complements in living atelines 1836: "the district here mentioned is even yet inhabited by a very (Table 3 and Fig. 5). Based on a formula for calculating body large , to which the Indians have given the name Caypore, mass in primates from articular dimensions {logio(femoral which signifies the dweller in the wood" (ref. 6, see p. 315); head volume) = 1.196[logio(body mass)] + 2.234} (9), this bambuiorum, after Bambui + -orum, in recognition of Grupo Caipora individual probably weighed 20.5 kilograms. This Bambui de Pesquisas Espeleologicas of Belo Horizonte, the weight is approximately 75% 'greater than the highest weights speleological team that discovered the fossils in Toca da Boa reported for living atelines (10). Vista in 1992. The late Pleistocene paleoenvironment of this region of Diagnosis. Large-bodied (>20 kg) char- Bahia may have been similar to current conditions, with acterized by a robust postcranium, spherical and capacious neu- hillside forests to the north and along river margins to the rocranium, a projecting premaxilla, bunodont , and a high south, and level terrain covered by low vegetation (rasteira), a forelimb/hindlimb length ratio. It is distinguished from non- sandy, soil-poor sedimentary complex. Pleistocene mammals atelines by its large size and postcranial adaptation to suspension from other caves in the region include such taxa as Toxodon, and brachiation. Compared with atelines (Alouatta, Ateles, , and Haplomastodon, suggesting that the area at Brachyteles, and Lagothrix), it is distinguished fromAlouatta by the that time period provided sufficient grazing cover to support above-mentioned characters, its neurocranial shape and size, and megaherbivores. The forest cover, however, appears to have in lacking cranial modifications for an enlarged hyo-laryngeal been more prominent and diversified than it is today, insofar apparatus (i.e., a flat, caudally directed nuchal plane and an as it supported the larger biomass of New World monkeys such extended basicranium). It is distinguished from Lagothrix and as Caipora bambuiorum. Ateles by its postcranial robustness, the rounded shape of its With the exception of Caipora and Protopithecus (4, 11), neurocranium, and in having a relatively more projecting premax- Pleistocene New World monkeys are known primarily from illa. It is further distinguished from Brachyteles in lacking molar island deposits in the (12-13). The insular Pleisto- shearing crests. It is distinguished from Protopithecus by having a cene platyrrhines are difficult to integrate into the evolution- less robust postcranium, particularly in the areas of gluteal and ary history of living genera and in some cases display unusual forelimb flexion musculature, and a larger, more rounded neuro- postcranial morphologies (14). Caipora, by contrast, is clearly cranium. Species diagnosis, C. bambuiorum: as for genus. related to a distinct lineage of living New World monkeys, the atelines. Its body size and apparent phylogenetic affinity to DESCRIPTION spider monkeys make it a remarkable addition to the adaptive The neurocranium of Caipora is large and globose (Fig. 2). The diversity of neotropical primates. It further demonstrates that braincase ascends above the supraorbital rim, and the maximum platyrrhines were a part of the megafauna characteristic of the breadth is found high on the parietals, giving the neurocranium terminal Pleistocene in South America (15). a more rounded contour than is typical of New World monkeys. Its neurocranial length and, in particular, its neurocranial breadth The fossils of Toca da Boa Vista were discovered by the members exceed that of any known platyrrhine (Table 2). A comparison of of Grupo Bambui de Pesquisas Espeleologicas of Belo Horizonte. We these dimensions relative to overall cranial size demonstrates that would especially like to thank Mauro A. Chagas Ferreira and Rodrigo the neurocranium of Caipora is more spherical than the neuro- Lopes F. for help in the field and Humberto do Espirito Santo for the crania of other New World monkeys (Fig. 3). The temporal artwork. John Fleagle and Alfred Rosenberger facilitated our collab- lines oration and provided many helpful suggestions. Assistance and helpful are faint and pass parallel to one another along the supero-lateral advice was also offered by William Jungers, Dan Gebo, and Miguel aspect of the neurocranium. The facial skeleton displays a gracile Schon Ybarra. We thank S. Franco, L. Oliviera, and G. Wilson Nunan circum-orbital region and ovoid orbits that are similar to Ateles. of the Museu Nacional in Rio de Janeiro; R. Thorington of the All cranial sutures are closed, and both upper and lower third National Museum of Natural History; B. Patterson of the Field molars are fully occluded and worn. Museum of Natural History; and R. D. E. MacPhee of the American The mandible and dentition bear the most striking resem- Museum of Natural History for access to comparative specimens. blance to Ateles (Fig. 4). Premolar and molar cusp configu- Laboratory and photographic support was provided by Pontificia ration is remarkably similar to Ateles and Lagothrix. Upper Universidade Catolica de Minas Gerais and Universidade Federal de and lower molars are quadrate, and the occlusal morphology is Minas Gerais. This research was supported by a grant from the LSB bunodont and relatively undeveloped, as inAteles. The lower third Leakey Foundation. molar is set in the corpus of the mandible, not along the base of 1. Fleagle, J. G. (1988) PrimateAdaptation and Evolution (Academ- the ascending ramus as in Alouatta and Brachyteles. Length and ic, San Diego), pp. 129-135. breadth tooth dimensions in Caipora are not significantly greater 2. Rosenberger, A. L. & Strier, K B. (1989) J. Hum. Evol. 18, than those in large Ateles individuals. 717-750. The postcranial skeleton, although not yet fully grown, is 3. Erickson, G. E. (1963) Symp. Zool. Soc. London 10, 135-164. more robust than that of any living New World monkey 4. Cartelle, C. (1993) Neotropical Primates 1, 8. (Table 3). Limb proportions and articular morphology re- 5. Cartelle, C. & Ferreira, M. A. C. (1994) Acta Geol. Leopold. 17, flect the same suite of adaptations to suspensory posture and 411-414. brachiating locomotion that characterizes spider and woolly 6. Lund, P. W. (1840) Charles. Mag. Nat. Hist., Vol. 4. 7. German, R. M. (1982) Am. J. Phys. Anthropol. 58, 453-459. spider monkeys (Fig. 5). Signatures of this unusual below- 8. Meldrum, D. J. & Lemelin, P. (1991)Am. J. Primatol. 25, 69-89. branch habitus include extremely long upper limbs, mobile 9. Ruff, C. B. (1990) in Body Size in Mammalian Paleobiology: gleno-humeral articular morphology, metacarpals subequal Estimation- and Biological Implications, eds. Damuth, J. & in length to metatarsals, and relatively robust proximal MacFadden, B. J. (Cambridge Univ. Press, Cambridge, U. K.), caudal vertebrae (3, 7-8). Caipora displays a spherical pp. 119-150. humeral head, straight humeral shaft, relatively short ulnar 10. Peres, C. A. (1994) J. Hum. Evol. 26, 245-249. olecranon process, and radial articular facet flush with the 11. Hartwig, W. C. (1995) J. Hum. Evol. 28, 189-195. shaft of the ulna. These features and its intermembral index 12. Ford, S. M. (1990) J. Hum. Evol. 19, 237-254. are all 13. Williams, E. E. & Koopman, K F. (1952) Am. Mus. Novit. 1546, characteristic of brachiating New World monkeys. 1-16. 14. MacPhee, R. D. E. & Fleagle, J. G. (1991) Bull Am. Mus. Nat. DISCUSSION Hist. 206, 287-321. 15. Anderson, E. (1984) in Quaternary : A Prehistoric It is difficult to estimate the body weight of Caipora accurately. Revolution, eds. Martin, P. S. & Klein, R. G. (Univ. of Arizona Postcranial elements are considerably more robust, but not Press, Tucson), pp. 40-89. Downloaded by guest on September 29, 2021