A complete skeleton of the giant South American primate Propithecus

Abstract

A complete skeleton of a large-bodied New World monkey has been found in Pleistocene cave deposits in the Brazilian state of Bahia. It demonstrates an unprecedented combination of body size, locomotor and cranial morphology. Skeletal features indicate an animal of approximately 25 kg, more than twice the mass of any living South American monkey. We refer the specimen to Protopithecus brasiliensis Lund, 1838, a large Pleistocene primate originally represented by only a proximal femur and distal humerus. The skeleton resembles species of two distinct New World monkey lineages. The cranium is modified for an enlarged vocal sac typical of living howler monkeys, and the postcranium includes suspensory and brachiating components of locomotion as seen in living spider and woolly spider monkeys. This skeleton confirms that adaptive diversity in neotropical primates was greater in the recent past, and that current interpretations of how their distinctive adaptations evolved should be revised.

Full text

Proc. Natl. Acad. Sci. USA
Vol. 93, pp. 6405–6409, June 1996
Evolution
A new extinct primate among the Pleistocene megafauna of
Bahia, Brazil
(New World monkeys
y
paleontology
y
Atelinae)
CASTOR CARTELLE* AND WALTER CARL HARTWIG
†
*Instituto de Geociencias, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil; and
†
Department 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-
bodied New World monkey that resembles living spider mon-
keys was recovered from undisturbed Pleistocene deposits in
the Brazilian state of Bahia. The skeleton displays the highly
specialized postcranial pattern typical of spider and woolly
spider monkeys and shares cranial similarities to the spider
monkey exclusively. It is generically distinct on the basis of its
robustness (>20 kg) and on the shape of its braincase. This
new genus indicates that New World monkeys nearly twice the
size of those living today were part of the mammalian biomass
of southern Amazonia in the late Pleistocene. The discovery of
this specimen expands the known adaptive diversity of New
World monkeys and demonstrates that they underwent body
size expansion in the terminal Pleistocene, as did many other
types of mammals.
Anthropoid primates colonized South America in the early
part of the Tertiary (.30 million years ago) and radiated
widely throughout the neotropics. Sixteen New World mon-
key genera survive today, all of which are arboreal and
relatively small-bodied compared with most Old World
anthropoids. Four living genera (Alouatta, Ateles, Brachy-
teles, and Lagothrix) are closely related to one another and
are distinct among New World monkeys for their relatively
large body size (6–12 kg), suspensory postures, and prehen-
sile tails (1–3). They are usually classified in a separate
subfamily, Atelinae, within which the howler monkey (Al-
ouatta) is considered less closely related to the other three
than they are to each other (2). Ateles and Brachyteles are
further distinguished by a specialized postcranial adaptation
to a brachiating mode of locomotion, in which the forelimbs
are relatively elongated (3). The Pleistocene skeleton de-
scribed here resembles the spider monkey (Ateles) more than
it does any other living genus. However, this skeleton is
unusually robust, and its neurocranium is more rounded
compared with any living or extinct ateline.
DEPOSITIONAL CONTEXT
The fossil skeleton was discovered in 1992 in Toca da Boa
Vista, a cave in the Brazilian state of Bahia (Fig. 1). The
skeleton was found in an undisturbed deposit in a chamber that
also contained other Pleistocene fossils and a nearly complete
skeleton of a second large platyrrhine referred to Protopithecus
Lund, 1838 (4–5). Toca da Boa Vista is an extensive limestone
travertine with over 100 km of interfingering galleries. The fossils
were recovered in a chamber along the northeastern wall of the
cave several hundred meters from the principal entrance. The
relative completeness of several fossil skeletons in this chamber
suggests that the sediments were in primary depositional context
at the time of discovery.
Systematics. The order is Primates (Linnaeus, 1758); the
suborder is Haplorhini (Pocock, 1918); the infraorder is
Platyrrhini (E. Geoffroy, 1812); the subfamily is Atelinae
(Gray, 1825); the tribe is Atelini (Gray, 1825); the genus is
Caipora; and the species is Caipora bambuiorum.
Type Specimen. IGC-UFMG 05 (Instituto de Geociencias -
Universidade Federal de Minas Gerais) is a nearly complete
skeleton of a late-stage subadult, including cranium, mandible,
axial skeleton including caudal vertebrae, incomplete scapulae
and pelvis, upper and lower limb long bones, carpals, tarsals,
metacarpals, metatarsals, and numerous phalanges.
Age and Locality. Toca da Boa Vista is located at 40°519390 W
longitude and 10°099360 S latitude at an altitude of 600 m above
mean sea level. No radiometric dates are available from the
deposits, but other mammalian taxa found in the same sedimen-
tary context represent a mix of living and extinct Pleistocene
species (Table 1). Pending a more precise radiometric assessment,
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Table 1. Mammals discovered in Toca da Boa Vista
Order Species
Chiroptera Mormoops megalophylla
Pteronotus parnelli
Chrotopterus auritus
Loncophylla mordax
Desmodus rotundus
1Desmodus draculae
Eptesicus brasiliensis
Tadarida brasiliensis
Edentata 1 Nothrotherium maquinense
1 Scelidodon cuvieri
Myrmecophaga tridactyla
Euphractus sexcistus
Rodentia Coendou prehensilis
Artiodactyla Tayassu tajacu
Lama guanicoe
Mazama gouazoubira
Carnivora Cerdocyon thous
1 Protocyon troglodytes
1Arctotherium brasiliense
Procyon cancrivorus
Conepatus semistriatus
Felis pardalis
Felis tigrina
Felis yagouaroundi
Felis concolor
1 Smilodon populator
Primates 1 Protopithecus brasiliensis
1 Caipora bambuiorum
The plus sign indicates extinct species.
6405

FIG. 1. The location of Toca da Boa Vista in the northern part of the state of Bahia, Brazil, is shown.
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.
6406 Evolution: Cartelle and Hartwig Proc. Natl. Acad. Sci. USA 93 (1996)

FIG. 3. Log-log plots of cranial dimensions on overall cranial size [(total skull length 1 basicranial length 1 facial length 1 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)ofCaipora 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.
FIG. 4. Drawings of the palate
(A) and mandible (B)ofCaipora
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 lengthyhindlimb 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.
Evolution: Cartelle and Hartwig Proc. Natl. Acad. Sci. USA 93 (1996) 6407

an age of late Pleistoceneyearly Holocene (ca. 10,000 B.P.) is
assigned based on this faunal correlation.
Etymology. Caipora (ky-por-ah), after Caipora, a creature of
native South American folklore described by Peter Wilhelm
FIG. 5. Selected postcranial elements of Caipora bambuiorum.(A) Anterior view of left humeri of (left to right) Ateles paniscus, 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.
6408 Evolution: Cartelle and Hartwig Proc. Natl. Acad. Sci. USA 93 (1996)

Lund, a Danish naturalist and father of Brazilian paleontology, in
1836: ‘‘the district here mentioned is even yet inhabited by a very
large 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 1 -orum, in recognition of Grupo
Bambui de Pesquisas Espeleologicas of Belo Horizonte, the
speleological team that discovered the fossils in Toca da Boa
Vista 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 high
forelimbyhindlimb length ratio. It is distinguished from non-
atelines by its large size and postcranial adaptation to suspension
and brachiation. Compared with atelines (Alouatta, Ateles,
Brachyteles, and Lagothrix), it is distinguished from Alouatta by the
above-mentioned characters, its neurocranial shape and size, and
in lacking cranial modifications for an enlarged hyo-laryngeal
apparatus (i.e., a flat, caudally directed nuchal plane and an
extended basicranium). It is distinguished from Lagothrix and
Ateles by its postcranial robustness, the rounded shape of its
neurocranium, and in having a relatively more projecting premax-
illa. It is further distinguished from Brachyteles in lacking molar
shearing crests. It is distinguished from Protopithecus by having a
less robust postcranium, particularly in the areas of gluteal and
forelimb flexion musculature, and a larger, more rounded neuro-
cranium. Species diagnosis, C. bambuiorum: as for genus.
DESCRIPTION
The neurocranium of Caipora is large and globose (Fig. 2). The
braincase ascends above the supraorbital rim, and the maximum
breadth is found high on the parietals, giving the neurocranium
a more rounded contour than is typical of New World monkeys.
Its neurocranial length and, in particular, its neurocranial breadth
exceed that of any known platyrrhine (Table 2). A comparison of
these dimensions relative to overall cranial size demonstrates that
the neurocranium of Caipora is more spherical than the neuro-
crania of other New World monkeys (Fig. 3). The temporal lines
are faint and pass parallel to one another along the supero-lateral
aspect of the neurocranium. The facial skeleton displays a gracile
circum-orbital region and ovoid orbits that are similar to Ateles.
All cranial sutures are closed, and both upper and lower third
molars 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. Upper
and lower molars are quadrate, and the occlusal morphology is
bunodont and relatively undeveloped, as in Ateles. The lower third
molar is set in the corpus of the mandible, not along the base of
the ascending ramus as in Alouatta and Brachyteles. Length and
breadth tooth dimensions in Caipora are not significantly greater
than 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 and
brachiating locomotion that characterizes spider and woolly
spider monkeys (Fig. 5). Signatures of this unusual below-
branch habitus include extremely long upper limbs, mobile
gleno-humeral articular morphology, metacarpals subequal
in length to metatarsals, and relatively robust proximal
caudal vertebrae (3, 7–8). Caipora displays a spherical
humeral head, straight humeral shaft, relatively short ulnar
olecranon process, and radial articular facet flush with the
shaft of the ulna. These features and its intermembral index
are all characteristic of brachiating New World monkeys.
DISCUSSION
It 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 body
mass in primates from articular dimensions {log
10
(femoral
head volume) 5 1.196[log
10
(body mass)] 1 2.234} (9), this
Caipora individual probably weighed 20.5 kilograms. This
weight is approximately 75% greater than the highest weights
reported for living atelines (10).
The late Pleistocene paleoenvironment of this region of
Bahia may have been similar to current conditions, with
hillside forests to the north and along river margins to the
south, and level terrain covered by low vegetation (rasteira), a
sandy, soil-poor sedimentary complex. Pleistocene mammals
from other caves in the region include such taxa as Toxodon,
Eremotherium, and Haplomastodon, suggesting that the area at
that time period provided sufficient grazing cover to support
megaherbivores. The forest cover, however, appears to have
been more prominent and diversified than it is today, insofar
as it supported the larger biomass of New World monkeys such
as Caipora bambuiorum.
With the exception of Caipora and Protopithecus (4, 11),
Pleistocene New World monkeys are known primarily from
island 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 unusual
postcranial morphologies (14). Caipora, by contrast, is clearly
related to a distinct lineage of living New World monkeys, the
atelines. Its body size and apparent phylogenetic affinity to
spider monkeys make it a remarkable addition to the adaptive
diversity of neotropical primates. It further demonstrates that
platyrrhines were a part of the megafauna characteristic of the
terminal Pleistocene in South America (15).
The fossils of Toca da Boa Vista were discovered by the members
of Grupo Bambui de Pesquisas Espeleologicas of Belo Horizonte. We
would especially like to thank Mauro A. Chagas Ferreira and Rodrigo
Lopes F. for help in the field and Humberto do Espirito Santo for the
artwork. John Fleagle and Alfred Rosenberger facilitated our collab-
oration and provided many helpful suggestions. Assistance and helpful
advice was also offered by William Jungers, Dan Gebo, and Miguel
Scho¨n Ybarra. We thank S. Franco, L. Oliviera, and G. Wilson Nunan
of the Museu Nacional in Rio de Janeiro; R. Thorington of the
National Museum of Natural History; B. Patterson of the Field
Museum of Natural History; and R. D. E. MacPhee of the American
Museum of Natural History for access to comparative specimens.
Laboratory and photographic support was provided by Pontificia
Universidade Catolica de Minas Gerais and Universidade Federal de
Minas Gerais. This research was supported by a grant from the LSB
Leakey Foundation.
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Evolution: Cartelle and Hartwig Proc. Natl. Acad. Sci. USA 93 (1996) 6409