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Reconstructing the Locomotor Repertoire of Protopithecus brasiliensis. II. Forelimb Morphology

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THE ANATOMICAL RECORD 294:2048–2063 (2011)
Reconstructing the Locomotor
Repertoire of Protopithecus brasiliensis.
II. Forelimb Morphology
The Graduate Center, Department of Anthropology, City University of New York,
New York Consortium in Evolutionary Primatology (NYCEP), New York, New York
The majority of previous publications have suggested that the largebodied subfossil Protopithecus brasiliensis was a suspensory ateline with
a locomotor repertoire similar to that of extant Ateles and Brachyteles.
This is unexpected, as the cranial morphology of Protopithecus is very
similar to Alouatta, a genus usually classified as a deliberate quadrupedal
climber. Complicating matters further, as Protopithecus is twice as large
as Ateles and Brachyteles, its ability to be as suspensory as those two genera is suspect and a terrestrial component of the locomotor repertoire has
also been hypothesized. The forelimbs of Protopithecus, while relatively
elongated as would be expected in a suspensory animal, are also quite robust and show several adaptations for climbing. To test these hypotheses
about the fossil locomotor repertoire, three-dimensional geometric morphometric techniques were used to quantify the shapes of the fossil distal
humerus and proximal ulna and then compare them to a broad sample of
extant primates with varying body sizes and locomotor patterns. Results
indicate that Protopithecus is similar to Ateles and Brachyteles in terms
of its forelimb joint surface morphology; however, the overall locomotor
repertoire of the fossil is reconstructed as more flexible to include forelimb suspension, climbing, and potentially some terrestrial ground use.
The combination of suspensory locomotion and quadrupedal climbing supported here indicates the beginnings of the evolutionary transition from a
more acrobatic style of locomotion in the last common ancestor of alouattins and atelins to the current pattern of howler locomotion. Anat Rec,
C 2011 Wiley Periodicals, Inc.
294:2048–2063, 2011. V
Key words: Protopithecus; locomotor reconstruction; forelimb
morphology; 3DGM; platyrrhine evolution
From the time of its discovery in 1836, Protopithecus
brasiliensis has been associated with the extant suspensory atelines Ateles and Brachyteles (Lund, 1838; Winge,
1895). The first fragmentary specimens to be recovered
from the Lagoa Santa (LS) caves in Minas Gerais, Brazil, a left proximal femur and a right distal humerus,
were largely ignored for over 100 years after being
described as a giant Brachyteles and assumed to be
nearly identical to that genus (Hartwig, 1995a). It was
not until the mid-1990s, when a nearly complete skeleton of Protopithecus was discovered in the Toca da Boa
Vista (TBV) caves in the neighboring state of Bahia,
that the scientific mystery of this taxon was fully appreC 2011 WILEY PERIODICALS, INC.
ciated. The full skeleton seems to combine traits found
in two genera that are usually seen as belonging to opposite ends of the ateline adaptive spectrum; its skull
shares several derived characters with Alouatta while
Grant sponsor: National Science Foundation Doctoral
Dissertation Improvement Grant; Grant number: 0925704.
*Correspondence to: Lauren B. Halenar, The Graduate Center,
Department of Anthropology, City University of New York, 365 Fifth
Avenue, New York, NY 10016. E-mail:
Received 15 September 2011; Accepted 16 September 2011
DOI 10.1002/ar.21499
Published online 1 November 2011 in Wiley Online Library
Flat, faces
Wide, shallow
Long, curved
Not projecting
Faces laterally
Wide, shallow
Recessed, gutteral
Large, medially
Spherical, posteriorly
Broad, cylindrical,
low edges
Long, straight,
Large, round,
medially directed
Equal to or lower
the headb
Narrow, deep
At least halfway down
the shaft
Long, slender,
Large, faces
Narrow, long
Large, medially
Spherical, ‘‘unrolled’’
High degree of
Greater faces
Relatively long
Inflated, capitular
Narrow, cylindrical
Medially directed
Below the head
Clinging and leaping
Long and retroflexed
Narrow, lateral
articular facets
Outset, subdivided
Deep, lateral wall
articular surface
Narrow, strong
Flattened distally
Posteriorly directed
Strong medial
Oval, posteriorly
Project proximally
above head
Quarter to a third
of the way down
the shaft
Compiled from Gebo (1993), Larson (1993), Meldrum (1993), Rose (1993), MacPhee and Meldrum (2006), Jones (2008), and personal observation.
The descriptions in bold describe the relevant morphology in Protopithecus.
Coronoid process
Radial facet
Proximal ulna
Olecranon process
Trochlear notch
Zona conoidea
Brachioradialis flange
Olecranon fossa
Broad, distolaterally
Wide, conical,
prominent edges
Oval, posteriorly
Project proximally
above head
Broad, shallow
Broad, v-shaped,
quarter of the
way down the
Short, bowed slightly
in anterior view
Distal humerus
Medial epicondyle
Humeral shaft
Bicipital groove
Deltoid tuberosity
Proximal humerus
TABLE 1. Qualitative descriptions of aspects of forelimb morphology known to vary with locomotor pattern in extant primatesa
its teeth and postcranial skeleton are more similar to
Ateles (Hartwig and Cartelle, 1996). Along with its large
body size that has been estimated at 23–25 kg, twice the
size of any living New World monkey (Hartwig, 1995b;
Hartwig and Cartelle, 1996; Halenar, 2011), this mosaic
of traits has made interpreting the paleobiology of
Protopithecus and its impact on reconstructing the
evolutionary history of the ateline primates a challenge
that few have attempted to address.
Locomotor behavior is one facet of Protopithecus paleobiology that has remained enigmatic. The original suggestion of ateline-like suspensory locomotion, which was
mostly based on limb proportions (Hartwig and Cartelle,
1996), has been challenged by another hypothesis pointing to the large body size of Protopithecus as evidence
for a ‘‘high degree’’ of terrestrial behavior (Heymann,
1998). More recently, several quantitative traits in the
Protopithecus postcranial skeleton have been shown to
group it with other ‘‘brachiating’’ primates (Jones, 2008);
however, because of the fragmentary nature of the fossil
joint surfaces used to calculate some of the key indices,
these results should be viewed with caution. Different
methodology will be used here in an attempt to test the
various hypotheses that have been proposed so far for
the locomotor repertoire of Protopithecus. Detailed qualitative descriptions of the humerus, radius, and ulna will
be given first. Then three-dimensional geometric morphometric (3DGM) techniques are used to capture the
shape of the distal humerus and proximal ulna and to
quantify aspects of their morphology that are known to
vary in predictable ways with locomotor patterns in
extant primate taxa. Principal components analyses
(PCA) are used to visualize the major axes of shape variation within the sample. The species, or group of species,
to which the fossil is most similar is used as an analog
for reconstructing its locomotor repertoire. Results of
these analyses are discussed in relation to the overall
evolutionary trajectory of the alouattin tribe and the
sequence of changes leading from the ateline last common ancestor to modern Alouatta.
Table 1 was constructed as an aid in comparing the
Protopithecus forelimb with forelimb morphology known
to vary predictably amongst taxa of different locomotor
patterns. The qualitative data compiled here present a
muddled picture with few truly diagnostic characters, as
the same features appear under different types of locomotion and characters found in Protopithecus fall under
several different behavioral categories. However, it is
still instructive to examine each element of the fossil on
its own in more detail.
Unfortunately, the scapula of Protopithecus is very
fragmentary and does not preserve any functional information. Similarly, the proximal humerus, especially
parts of the head that would make clear its size, shape,
and orientation, is only present on the right side and is
not well preserved (Fig. 1). However, the bicipital groove
and size of the tubercles can be seen; the groove is relatively narrow and deep and the tubercles sit below the
level of the head, as in suspensory primates (Larson,
1993). The shaft of the humerus is straight and relatively long but is also quite robust as would be expected
in an animal of its body size. Distally, the specimens
Fig. 1. Humerus of Protopithecus. Note the narrow, deep bicipital
groove and low tubercles on the proximal end and the large brachioradialis flange on the distal end of the Toca da Boa Vista specimen
(left). The specimen from Lagoa Santa (right) is smaller and lacks the
protruding brachioradialis flange, but otherwise is similar in joint morphology to the TBV specimen. Scale bar ¼ 1 cm.
from LS and TBV differ from one another in their size
and robusticity (Fig. 1); this is especially apparent in the
width of the entire joint and prominent brachioradialis
flange of the TBV specimen. These are some of the features pointed out by Hartwig and Cartelle (1996) that
suggest climbing as an important part of the locomotor
repertoire for this specimen. The LS specimen is similar
in shape to the larger TBV specimen, and its smaller
size could indicate a relatively high level of sexual
dimorphism for Protopithecus; other atelines, especially
Alouatta, are also sexually dimorphic (Ford, 1994). If the
TBV specimen represents a larger male individual, a
well-developed brachioradialis flange would be expected
as the flexor muscles that attach there would also be
larger for hoisting its heavier body through the trees
and pulling itself up on branches. The medial epicondyle
on both specimens is large and projects medially as in
arboreal quadrupedal primates; it is not retroflexed as in
terrestrial Old World monkeys. Neither do the fossils
Fig. 2. Partial proximal radius of Protopithecus. Scale bar ¼ 1 cm.
Fig. 4. Composite ray of Protopithecus. Lines on the proximal phalanx show the dimensions necessary for calculating the included angle
of curvature, which on this specimen was approximately 60 degrees.
Scale bar ¼ 1 cm.
Fig. 3. Proximal ulna of Protopithecus in anterior (left) and lateral
view (right). Note the relatively prominent and straight olecranon process, the inset radial notch, and the relative overall width of the trochlear notch. Scale bar ¼ 1 cm.
exhibit the extreme distal projection of the medial edge
of the trochlea like those terrestrial primates (Rose,
1988, 1993). Protopithecus also does not have an entepicondylar foramen, a feature that has been lost in atelines but is frequently seen in other platyrrhines such as
Cebus, Aotus, and Pithecia (Gebo, 1993).
The radius of Protopithecus is not complete (Fig. 2);
only the proximal end is present and the head is heavily
worn and covered in calcite deposits. Without the entire
shaft it is hard to judge important characteristics of the
radial head and tuberosity related to their orientation.
The radial tuberosity, however, is relatively large and
the head seems to be oval in shape, but the circumference is incomplete. A more circular radial head is a characteristic of suspensory primates (Rose, 1993). The
proximal ulna also does not have any of the classical features indicative of terrestrial locomotion in Old World
monkeys (Fig. 3). More like an arboreal climber, the radial facet is inset against the shaft of the bone and faces
anterolaterally as opposed to the outset condition seen
in a terrestrial primate (Gebo, 1993; Rose, 1993). The
TABLE 2. Taxa and number of individuals included in the comparative samplea
Male body weightb
Proximal ulna
Locomotor repertoire
AQ, terrestrial,
Arboreal climbing
and clinging
Upside-down below
branch suspension
AQ, leaping
AQ, leaping
AQ, leaping
AQ, climbing, PHT
AQ, climbing, PHT
AQ, suspensory, PHT
AQ, suspensory, PHT
AQ, leaping
AQ, terrestrial
AQ, leaping
AQ, leaping, swimming
AQ, climbing, terrestrial
Brachiation, climbing
AQ, suspensory, terrestrial
Distal humerus
Abbreviations: VCL ¼ vertical clinging and leaping; AQ ¼ arboreal quadrupedalism; PHT ¼ prehensile tail.
The ‘‘?’’ indicate that the locomotor repertoire for those two fossil taxa is unknown/under investigation.
Data from Rosenberger and Strier (1989), Cartelle and Hartwig (1996), Fleagle (1999), Jungers et al. (2002), Di Fiore and
Campbell (2007), and Halenar (2011).
Only male body weights are listed for comparative purposes as both TBV Protopithecus and Caipora have been suggested
to be males.
Fig. 5. Three-dimensional landmarks collected to describe the shape of the distal humerus (A) and
proximal ulna (B). Landmarks are shown on the TBV Protopithecus and are connected as a reference for
the wireframes in the following PCA figures. Scale bars ¼ 1 cm.
olecranon process is not retroflexed; the superior surface
is angled slightly posteriorly but the whole process is
prominent and oriented proximally, much like in Ateles.
However, other aspects of the joint surface are not similar to the Ateles condition. For example, the distal facet
of the trochlear notch is much smaller and less convex.
Also, the coronoid process is slightly more projecting and
oriented at a shallower angle. As in the humerus, the
ulna exhibits a combination of traits usually seen only
in either suspensory taxa like the atelins or taxa that
are more generalized arboreal climbers like Alouatta.
Moving down to the distal end of the forelimb, degree
of phalangeal curvature is also strongly correlated with
substrate preference: arboreal taxa show much more
curved phalanges than terrestrial taxa (Susman et al.,
1984; Hamrick et al., 1995; Jungers et al., 1997). Qualitative inspection of the Protopithecus phalanges suggests
that they are curved as in arboreal primates (Fig. 4). In
fact, the included angle of curvature (Stern et al., 1995)
for one proximal phalanx of Protopithecus is approximately 60 degrees; this is in the high end of the range of
values reported for Ateles and Hylobates but below the
range of Pongo (Jungers et al., 1997). The phalanges
also have relatively strong and distally placed flexor
sheath ridges, indicating strong grasping abilities (Almécija et al., 2007, 2009). Unfortunately, it is unclear
whether the phalanges in the sample are from the hands
or the feet. Also, there are no relevant metacarpals preserved to determine whether Protopithecus had a vestigial pollex, a hallmark of both Ateles and Brachyteles
(Biegert, 1963; Erikson, 1963; Jouffroy et al., 1991;
Tague, 1997).
Although some single aspects of the joints might
appear similar to nonplatyrrhine taxa, there is no suite
of characters seen in the Protopithecus forelimb that
would suggest extreme locomotor specializations like
those seen in leaping or slow climbing strepsirhines or
terrestrial Old World monkeys. As has been observed in
other parts of the skeleton, the forelimb combines traits
possessed by extant primates that practice both belowbranch forelimb suspension and arboreal climbing.
These qualitative aspects of the Protopithecus forelimb
will be quantified using landmark-based 3DGM
TABLE 3. Anatomical landmark definitions
Distal humerusa
Proximal ulna
A comparative sample of living primates was used consisting of adult male and female wild-shot individuals
from collections at the American Museum of Natural
History (AMNH) in New York, the National Museum of
Natural History (NMNH) in Washington, DC, and the
Museu Nacional (MN), Rio de Janeiro, Brazil (Table 2).
This set of taxa was chosen to represent a diverse array
of body sizes, locomotor patterns, and phylogenetic affinities, extending the comparative framework used in previous studies of the Protopithecus postcranial remains.
The fossil material includes the original Protopithecus
distal humerus discovered in the LS caves, which is now
housed in the Universitets Zoologisk Museum in Copenhagen, Denmark; the nearly complete Protopithecus
skeleton from TBV, curated in the Museu de Ciências
Naturais at the Pontificia Universidade Católica de
Minas Gerais in Belo Horizonte, Brazil; the nearly complete skeleton of Caipora bambuiorum, discovered at the
Most lateral point
Most medial point
Most lateral point on the capitulum
Most medial point on the capitulum
Most superiolateral point on the
trochlea (excluding the capitulum)
Most inferiomedial point on the
trochlea (excluding the capitulum)
Most superior point on the medial
Most inferior point on the medial
Most superior point on the lateral
Most inferior point on the lateral
Most superior point of the olecranon
Most inferiomedial point of the
olecranon fossa
Most inferiolateral point of the
olecranon fossa
Deepest point of the olecranon fossa
Most medial point on the trochlea
Most lateral point on the trochlea
Tip of the medial epicondyle
Most proximal point of the olecranon
Most medial point on the maximum
constriction of the olecranon process
Most lateral point on the maximum
constriction of the olecranon process
Most posterior point on the olecranon
Most anteriomedial point on the
olecranon process
Most aneriolateral point on the
olecranon process
Most medial point on the ‘‘wing’’ of
the proximal articular facet
Most lateral point on the ‘‘wing’’ of
the proximal articular facet
Most anterior point on the proximal
border of the proximal articular
Most distomedial point of the
proximal articular facet
Most distolateral point of the
proximal articular facet
Deepest point in the midline of the
trochlear notch
Most posteriomedial point of the
distal articular facet
Most anterior point of the distal
articular facet
Most anterior point of the radial facet
Most posterior point of the radial
Most proximal point of the radial
Most distal point of the radial facet
Deepest point in the radial facet
The anterior and posterior landmarks on the distal
humerus were digitized together without changing the orientation of the specimen.
Fig. 6. PCA results for the distal humerus of the entire comparative
sample. The taxa are arrayed across PC1 (26% total variance) based
on the width of the joint, which is affected by the length and orientation of the medial epicondyle and height and depth of olecranon
fossa. PC2 (14% total variance) shows the variation based on the
height of the epicondyles. The wireframes show the morphology in the
nearest cluster of a right humerus in anterior view (see Fig. 5A for reference). Bottom left Protopithecus ¼ TBV; top right ¼ LS.
same time and in the same cave as the TBV Protopithecus material (Cartelle and Hartwig, 1996); and several
subfossil lemur specimens curated in the AMNH (Archaeolemur sp.: AMNH30042-B-10; Paleopropithecus ingens:
AMNH30042-B-1, 30042-A-3, 30042-A-5; Megaladapis
edwardsi: AMNH30042-A-1; plus several uncatalogued
specimens assigned to those genera). The Caipora skeleton is of a subadult individual, but epiphyses of the distal
humerus and proximal ulna are fully fused.
A Microscribe 3DX digitizer was used to collect the
three-dimensional coordinates (x, y, z) of a set of landmarks designed to capture the shapes that are expected
to vary among living taxa of differing locomotor profiles
(Fig. 5; Table 3). Data were collected on the distal humerus and proximal ulna; these elements are well preserved in Protopithecus on at least one side of the body.
As there are few biologically homologous Type I landmarks, such as the meeting point of two sutures, on
postcranial elements, sets of Type II landmarks, those
that are defined by the geometry of the specimens (Bookstein, 1991), were designed specifically for this study.
During data collection, both the distal humerus and the
proximal ulna were positioned in such a way so that
landmarks on all sides of the bone could be digitized
without changing its orientation.
So far, few 3DGM analyses involving postcrania have
been published (e.g., Drapeau, 2008; Harcourt-Smith
et al., 2008) and none of them are focused on platyrrhines. 3DGM techniques, especially generalized
Procrustes analysis (GPA; e.g., O’Higgins and Jones,
1998), are expected to be of particular help in answering
questions about the large-bodied Protopithecus because
it is a size-independent method that scales specimens to
unit centroid size as a way of normalizing body mass differences within a sample. PCA were conducted on the
results of a GPA using the program morphologika2 v2.5
(O’Higgins and Jones, 2006) to visualize the morphological variation within the sample for each skeletal element. Clouds of points representing groups of taxa with
similar locomotor behaviors were thus produced and the
locomotor behavior of the fossil was inferred based on its
position with respect to the comparative sample; for
example, if Protopithecus were to fall in the middle of a
cloud of acrobatic suspensory atelines, this would support the hypothesis that it was using acrobatic suspensory locomotion. This method was chosen over
discriminant function analysis, which was used previously in a quantitative analysis involving Protopithecus
(Jones, 2008), because it does not require the user to
specify a particular locomotor category for each specimen
in the comparative sample. As discussed below, living
primates use a variety of locomotor behaviors that can
leave their mark on the postcranial skeleton and reducing taxa to a single categorical definition might not be
as useful as allowing their variation to fall out naturally
in multidimensional shape space. The inclusion of a fossil in a PCA lets the fossil speak for itself with regard to
its similarities to extant taxa.
Fig. 7. PCA results for the distal humerus of the platyrrhine taxa
only. PC1 (23% total variance) is being driven by the height of the
olecranon fossa and the length of the medial epicondyle. PC2 (14%
total variance) shows the variation in the height of lateral epicondyle
and the orientation of medial epicondyle. The wireframes represent
the morphology in the nearest cluster of a right humerus in anterior
view (see Fig. 5A for reference). Top left Protopithecus ¼ TBV; bottom
right ¼ LS.
PCA were run on several different iterations of the
sample for each element; one including the entire comparative sample, one including only the platyrrhine
taxa, and one on the male species mean landmark configuration for those platyrrhines which was then overlaid with a minimum spanning tree to connect the most
similar shapes. Both the mean landmark configurations
and the minimum spanning trees were calculated using
the PAST software package (Hammer et al., 2001). As
the comparative sample spans a relatively wide range of
body sizes, for each PCA, the first two principal component axes scores were regressed against ln centroid size
of the specimens to test for correlation with body size;
although the size of an animal is certainly related to
how it can move through its habitat and is therefore relevant to the variation in the sample, it is not desirable
for size alone to be driving the grouping patterns on the
axes that represent the majority of that variation.
arate from the more generalized arboreal taxa (Alouatta
and Cebus) and those that add more leaping to their repertoire (Aotus, Pithecia, and Chiropotes). The three fossils, both Protopithecus individuals and Caipora, are
consistently part of this atelin cluster because of their
mediolaterally wide distal humerus and large medially
projecting medial epicondyle. In the full sample PCA,
the TBV humerus is situated closer to the strepsirhine
cluster on PC2 due to the enlarged brachioradialis flange
that it shares with some members of that vertical clinging and leaping group (Fig. 6). When a minimum spanning tree is overlaid connecting the three-dimensional
shapes representing the male mean landmark configuration for each species of platyrrhine in the sample, the
TBV humerus is joined to Brachyteles as is the LS specimen, which is also linked to Lagothrix (Fig. 8). The two
Protopithecus individuals are not linked to each other,
emphasizing the differences between the two specimens
noted in the qualitative description above.
The full sample PCA for the proximal ulna produces
clustering of New World monkeys, Old World monkeys,
and hominoids similar to that seen for the distal humerus (Fig. 9). The strepsirhine group is different in
this case, as the subfossil lemurs are separate from their
extant relatives, Propithecus and Indri; the larger size of
the subfossils and their extremely reduced olecranon
process make them more similar to the living hominoids
in the sample. When the platyrrhines are analyzed separately, the distinctions between the various taxa are
clearer for the proximal ulna than they were for the
A PCA of the entire primate-wide sample for the distal
humerus results in a clear separation of New World
monkeys, Old World monkeys, hominoids, and strepsirhines (Fig. 6). The Old World monkeys are arranged
across PC1 from more arboreal taxa like Colobus on the
left to the more terrestrial baboons on the right, with
the variable macaques spanning both groups. In both
the full sample and platyrrhine-only analyses (Figs. 6
and 7), the suspensory atelins form their own group sep-
Fig. 8. PCA results for the average male distal humerus shape for all platyrrhine species in the sample
overlaid with a minimum spanning tree connecting the most similar shapes in three-dimensional space.
Both Protopithecus specimens are connected to Brachyteles, while not being connected to each other,
emphasizing the differences between the two fossil specimens as described in the text.
Fig. 9. PCA results for the proximal ulna using the entire comparative sample. PC1 (30% total variance) represents the variation in the
height of the olecranon process and the width of the distal facet of
the trochlear notch. Variation along PC2 (13% total variance) is driven
by the orientation of the proximal portion of the trochlear notch and
the radial facet. The wireframes represent the left ulna in anterior view
showing the morphology represented by the nearest cluster (see Fig.
5B for reference).
Fig. 10. PCA results for the proximal ulna of the platyrrhine taxa
only. Morphological variation along PC1 (20% total variance) is driven
by the length and orientation of the distal facet of the trochlear notch.
PC2 (13% total variance) is driven by the height of the olecranon pro-
cess and the overall width of the trochlear notch. The wireframes represent the left ulna in anterior view showing the morphology in the
nearest cluster (see Fig. 5B for reference).
distal humerus (Fig. 10). Again, Protopithecus and Caipora group with the more suspensory atelins, not with
the less agile Alouatta, because of their shorter olecranon
process and wider, more anteriorly facing trochlear notch.
A minimum spanning tree produces the same results as
for the distal humerus, linking Protopithecus with Brachyteles as the extant taxon sharing the most similar
joint surface morphology (Fig. 11). For neither element is
the much larger size of the fossils driving any of the
grouping patterns on either PC1 or PC2; when ln centroid size of each individual in the sample is regressed
against its PC score, R2 values are all less than 0.5.
fleeing predators or feeding. This is especially important
for a fossil like Protopithecus, which presents a mosaic
of traits that could fall under several different, commonly recognized locomotor categories. Another relevant
issue involves work done on comparing ateline ‘‘brachiation’’ to hylobatid ‘‘brachiation.’’ Historically, the term
‘‘semibrachiation’’ has been used for the atelines (Ashton
and Oxnard, 1963, 1964; Napier, 1963; Oxnard, 1963;
Ashton et al., 1965; Napier and Napier, 1967; Rose,
1973); however, there are several problems with this
conceptualization, most notably the fact that further
detailed behavioral studies have shown that the animals
that have been included in this category all move in
very different ways (Stern and Oxnard, 1973; Mittermeier and Fleagle, 1976).
Protopithecus has fallen victim to this terminological
chaos as well and has been lumped together with the
Ateles-style ‘‘brachiators’’ based on possession of a suite
of traits associated with this genus, including long forelimbs relative to hindlimbs, long and straight diaphyses,
mobile shoulder joints, curved phalanges, and (inferentially) a prehensile tail (Hartwig and Cartelle, 1996;
Jones, 2008). However, Hartwig and Cartelle (1996) also
pointed out unique features of the Protopithecus postcranium, such as the well-developed brachioradialis flange
on the distal humerus and the large attachment site for
the gluteus medius muscle on the ilium, that suggest
climbing as an adaptively important part of the locomotor repertoire in addition to suspension. Alouatta has a
large gluteus medius as well as a large gluteus
Broad categories of locomotor behavior, that is, ‘‘quadrupedal,’’ ‘‘arboreal,’’ ‘‘terrestrial,’’ or ‘‘leaper,’’ are not
necessarily useful when it comes to describing the complex behavior of living primates (e.g., Prost, 1965; Stern
and Oxnard, 1973; Hunt et al., 1996). The entire locomotor repertoire of an individual or a species might be different from the locomotor behavior it uses most often on
a daily basis. This creates a situation akin to that surrounding ‘‘fallback foods’’ (e.g., Marshall and Wrangham,
2007) and the ‘‘critical function’’ hypothesis (Rosenberger
and Kinzey, 1976); the morphology preserved in a fossil
of the postcranial skeleton could be reflecting adaptations to the way the animal moves most often while
traveling or, instead, to those parts of the behavioral
profile that could be most important to survival, such as
Fig. 11. PCA results for the average shape of the male proximal ulna shape in the platyrrhine portion
of the comparative sample overlaid with a minimum spanning tree connecting the most similar shapes in
three-dimensional space. Protopithecus is linked with Caipora, most likely due to the larger body size of
the two fossils, as well as with Brachyteles as in the results for the distal humerus.
maximus, both of which are useful in ‘‘antipronograde’’
postures (Stern, 1975). The gluteus maximus and tensor
fasciae femoris of howler monkeys form a muscle mass
in the hip, similar to the deltoid muscle in the shoulder,
that is useful in suspension by the hindlimbs (Stern and
Oxnard, 1973). This positional behavior is used often by
Alouatta during feeding and is seen much more frequently than is the type of suspension by the forelimbs
characteristic of Ateles (Stern, 1971; Gebo, 1992). This
combination of suspensory locomotion and deliberate
quadrupedal climbing in Protopithecus is confirmed
here, both qualitatively and quantitatively.
One of the most mysterious aspects of the evolutionary
history of New World monkeys is the lack of terrestrial
species. To date, no fossil or living South American primate has been described as spending the majority of its
daily activity budget on the ground, as do many Old
World monkeys and lemurs of Madagascar. This is not
for lack of open habitat; there are, and have been for
approximately 25 million years (MacFadden, 1997),
plenty of grasslands in South America that are home to
many diverse mammal species, but no primates. Several
suggestions have been made for why the platyrrhines
are restricted to an arboreal lifestyle: for example, some
argue that the South American forest structure is more
conducive to suspensory behavior with the aid of a prehensile tail (Emmons and Gentry, 1983; Lockwood,
1999), whereas others point to the high predator pressure on the ground for the relatively small-bodied
taxa that are found in the New World (Di Fiore, 2002;
Campbell et al., 2005).
Recently, several fossil platyrrhines have been suggested to have been either terrestrial or ‘‘semiterrestrial’’
(Heymann, 1998; Kay et al., 2002; MacPhee and Meldrum, 2006; Kay, 2010). Semiterrestrial has been defined
as a separate locomotor category for Old World monkeys
that have adaptations for transitioning between the
trees and the ground by climbing and leaping as well as
adaptations for quadrupedal running (Gebo and Sargis,
1994; Anapol et al., 2005). A combination of terrestrial
and arboreal traits such as relatively long distal limb
segments, a long tail, and smaller body size would indicate membership in this group; an example in the Old
World is Cercopithecus aethiops, the vervet monkey
(Anapol et al., 2005). In their study of the Paralouatta
postcranium, MacPhee and Meldrum (2006) compared
several morphological features of the elbow joint, ankle
joint, and digits to the same elements in living New
World and Old World primates of various locomotor patterns. Because of its unique combination of skeletal features, which includes a retroflexed medial epicondyle
and short straight phalanges, Paralouatta’s postcranial
skeleton was suggested to function more like that of a
cercopithecine than any other platyrrhine. Whether this
means that Paralouatta is directly analogous to the vervet monkey as another semiterrestrial species is not
exactly clear. However, it is worth noting that Paralouatta, like Protopithecus, does not seem to be moving
around in its environment in the same was as any
extant ateline.
Spending at least some time on the ground has also
been suggested for the oldest platyrrhine, Branisella
Fig. 12. Ateline portion of Fig. 1 from Heymann (1998). The regression line added through the nonsuspensory taxa, although driven by
the marked contrast between species of two different size classes, still
suggests that the intermembral index of Protopithecus and Caipora is
on trend for their larger body size. Despite having high intermembral
indices in the range of the more suspensory taxa, when their body
size is taken into account, the fossils appear more similar to the
slower, more quadrupedal atelines.
boliviana (Kay et al., 2002). However, this was based on
its high-crowned and heavily worn molars (the assumption being that grit in the terrestrial diet would wear
teeth faster, necessitating higher crowns) combined with
paleoenvironmental reconstruction of a more open habitat, as no postcranial remains are yet known for this
taxon. Similar reasoning has been used to infer ‘‘scansorial’’ behavior from the high-crowned molars of the
newly discovered Argentinian primate Mazzonicebus
almendrae (Kay, 2010). Protopithecus and its Pleistocene
subfossil relative Caipora (Cartelle and Hartwig, 1996;
Hartwig and Cartelle, 1996) provide new morphological
information relevant to this topic. For these taxa, which
are both represented by nearly complete skeletons,
hypotheses about locomotor adaptations can be tested by
looking directly at the joint surfaces themselves, instead
of distant functional systems such as teeth.
Heymann (1998) has proposed a counterhypothesis
stating that Protopithecus and Caipora were not as suspensory as Hartwig and Cartelle (1996) believed and
instead would have practiced a ‘‘high degree’’ of terrestriality. Most of the evidence presented is intended to
counter the pendulum model of brachiation as practiced
by gibbons and siamangs as the main mode of locomotion for the fossils. For example, the intermembral indices of the fossils, when taking into account their
extremely large body size for New World primates, make
them look more similar to chimps or bonobos than to spider monkeys (see Fig. 1 in Heymann, 1998). In fact, if
the ateline portion of that figure is isolated, Protopithecus and Caipora seem to fall on a line with Alouatta and
Lagothrix, the less-acrobatic atelines, whereas Ateles
and Brachyteles are the more specialized suspensory outliers (Fig. 12). Although the intermembral index of Protopithecus, at 104, is within the range of values for
Ateles (Erikson, 1963), this value is more correctly seen
as being in line with expectations for its body size based
on a regression model restricted to the nonspecialized
extant ateline genera. However, this is simply evidence
against suspensory locomotion for the fossil, not for terrestriality. The intermembral index is a gross indicator
of limb proportions and, hence, locomotor capabilities.
However, conclusions about locomotion in fossil taxa
should not be based on this value alone as it can mask
subtler differences in limb structure and behavior among
related taxa.
Just as limb proportions cannot provide a smoking
gun for locomotor capabilities, neither can body size
alone. Many other variables, both intrinsic to the animal-like joint surface morphology and extrinsic-like habitat type and social behavior, can influence how an
animal moves (Remis, 1995). However, in regards to suspensory locomotion, there is some evidence that siamangs, at 10–12 kg, are at the body size limit for
biomechanically efficient brachiation (Preuschoft and
Demes, 1985). Even the largest New World suspensory
taxa, Ateles and Brachyteles, do not exceed more than
about 12 kg (Di Fiore and Campbell, 2007) despite possessing a prehensile tail that provides more support and
weight distribution throughout the canopy. Protopithecus, at an estimated 20–25 kg (Hartwig, 1995b; Hartwig
and Cartelle, 1996; Halenar, 2011), is well above this
Although the limb proportions and large body size of
Protopithecus may indicate a nonsuspensory mode of
locomotion, this does not automatically mean that Protopithecus was terrestrial. The picture is most certainly
more complicated than a strict dichotomy between arboreality and terrestriality. A primate probably cannot be
an efficient brachiator at 20–25 kg; however, this does
not make terrestriality its only other option. Other
large-bodied primates, like orangutans and the truly
giant subfossil ‘‘sloth’’ lemurs, have found other ways to
move around successfully in the trees (e.g., Godfrey and
Jungers, 2003; Thorpe and Crompton, 2006). Heymann
(1998) pointed out that the great apes, while being
designed for brachiating, do not actually brachiate and
that most primates have a flexible locomotor repertoire,
the full range of which might not be represented in their
postcranial morphology. Analogy suggests that, perhaps,
Protopithecus was not completely arboreal or terrestrial
but could be better compared to a versatile great ape,
such as the chimpanzee. This would just be one more
example of convergence between atelines and hominoids
(for a review, see Di Fiore and Campbell, 2007).
Other evidence presented for a high degree of terrestriality in the fossil repertoire is largely reliant on circular logic: for example, if Protopithecus was terrestrial,
its large body size would be a good defense against predators such as jaguars and other large cats. Heymann
(1998) also brings up contradictory statements made by
Cartelle and Hartwig (1996) about the paleoenvironmental reconstructions of the area. They appear to vacillate
between an interpretation of the area as being more
open and similar to the cerrado vegetation that exists in
parts of Bahia and Minas Gerais today while also inferring that the existence of the large-bodied suspensory
primates is evidence for a more closed forest habitat
type. The paleoenvironment in the TBV and LS areas
relevant to Protopithecus is hard to pin down, especially
as the fossils have not been dated directly. Various lines
of evidence suggest mixed habitat types in alternating
wet and dry climates for the region through the late
Pleistocene (Cartelle, 1994; Auler et al., 2004, 2006;
MacFadden, 2005). If the climate was more dry and habitat more open at the time the fossils were extant, the
primates would have had an opportunity to spend more
time on the ground. Even if the habitat was more closed,
Heymann (1998) suggested that the New World forest
structure, with its lack of lianas and more fragile
branches (Emmons and Gentry, 1983), cannot support a
large-bodied suspensory taxon, even one with a prehensile tail. Both of these points, potential for predator
defense and the possible existence of a more open habitat, are valid considerations but do not prove that Protopithecus was terrestrial.
As mentioned above in regards to ‘‘brachiation,’’ the terminology being used here, and elsewhere in the literature, can benefit from clarification. Even though results
presented here do not ally Protopithecus with terrestrial
Old World monkeys like some macaques and baboons,
none have suggested that these extinct animals did not
use the ground at all. Several other ateline species, while
not ‘‘terrestrial’’ in their dominant locomotor pattern, use
the ground in many ways during their daily activities. In
the Atlantic Coastal forest, both Brachyteles and Alouatta
guariba come to the ground, especially in more disturbed
parts of the habitat, to cross cleared patches (Mourthe
et al., 2007). Even Ateles, the most suspensory and highly
reliant on an arboreal habitat, does come to the ground,
most often for reasons related to specialized feeding
behaviors such as drinking water during the dry season
and geophagy at mineral licks (Campbell et al., 2005);
some of these mineral licks are even in small caves (Link
et al., 2011), an interesting point to consider regarding
the taphonomy of the nearly complete Protopithecus skeleton from TBV. The majority of these behaviors are
described in the literature as opportunistic and more
properly called ‘‘ground use,’’ not ‘‘terrestrial locomotion,’’
and as such they may not leave an adaptive signal on a
fossilized postcranial skeleton. There is a difference
between being labeled a terrestrial primate in the manner of an Old World monkey, which is what previous
authors have been suggesting for various fossil platyrrhines, and allowing for ground use as part of a more
flexible locomotor repertoire that could be more correctly
given a different categorization. Perhaps ‘‘semiterrestrial’’
could be used, but as with ‘‘semibrachiation,’’ lumping
taxa into a catchall intermediate category can obscure
distinctions between them and caution should be exercised; a description of a range of possible behaviors may
be preferable to a single categorical label.
Despite the postcranial similarities creating functional
links to Ateles and Brachyteles, Protopithecus is a member of the alouattin tribe, more closely related to extant
Alouatta and fossils such as Stirtonia and Paralouatta
(Hartwig and Cartelle, 1996; Cooke et al., 2007; Rosenberger et al., in review). This designation is mostly
based on cranial synapomorphies seen in the TBV specimen such as the strong temporal lines, posteriorly
directed nuchal plane, large airorynchous face, and a
relatively small brain and foramen magnum. Based on
the results presented here, and considering their similar
Atlantic Coastal forest habitats, an alternate hypothesis
originally proposed by Hartwig (1995b) based on the LS
postcrania could be revived suggesting that Protopithecus is actually more closely related to Brachyteles. There
would be a size decrease and transition to a semifolivorous diet in the subsequent evolution of Protopithecus to-
ward its closest modern relative, whether that is
Alouatta or Brachyteles. However, if Protopithecus is
more closely related to Brachyteles, the cranial morphology shared by Protopithecus and the alouattins would be
convergent, an unlikely scenario given how very derived
the alouattin condition is when compared with the atelins. The inclusion of Protopithecus in the alouattin tribe
as a basal form that retains primitive aspects of its postcranial skeleton from the more suspensory common
ancestor of both alouattins and atelins is a more parsimonious hypothesis that does not necessitate convergence in any part of the skeleton. Positing a mediumsized ateline last common ancestor with a prehensile tail
used during feeding postures and a moderately suspensory mode of locomotion can help explain why the Protopithecus cranium is so similar to Alouatta but the
postcranial skeleton examined here is not. The results
presented here corroborate this description of the ateline
last common ancestor, which was also one of the suggestions made by Jones (2008) in her study of the evolution
of ‘‘brachiation’’ in atelines.
All extant genera in the subfamily have diverged
away from that moderately suspensory common ancestor, with Ateles and Brachyteles becoming more specialized acrobats and Alouatta and Lagothrix becoming less
specialized. For the Alouatta lineage, this evolutionary
transition began with a size increase toward Protopithecus, a large-bodied animal that would need to decrease
its reliance on acrobatic behaviors to preserve energetic
efficiency. Next came a size decrease during which climbing and slow quadrupedalism became even more prevalent as the newly enlarged hyoid bone and an increase
in percent of leaves included in the diet continued to create obstacles to acrobatic movement and enhance the
energy-minimizing strategy that Alouatta follows today
(Rosenberger and Strier, 1989; Fig. 13). The fossil evidence presented here allows a fleshing out of the hypotheses of Schön Ybarra (1976, 1984) regarding the
influence of the enlarged hyoid on possible locomotor
patterns. As sub-basal space decreased with decreasing
body size over evolutionary time, the cranial base was
forced to flatten and elongate to maintain the volume
necessary for the enlarged hyoid. The smaller-bodied
Alouatta ancestor with the newly unbalanced mass in its
throat would have altered its locomotor repertoire
accordingly toward the more slow, cautious quadrupedalism practiced by the extant species.
Protopithecus can thus be described as a taxon that
includes both types of locomotion in its repertoire and is
therefore positioned as transitional between the more
suspensory ateline last common ancestor and the more
quadrupedal alouattins. This means that the actual subfossil material that exists with its Pleistocene date is the
remains of a platyrrhine ‘‘living fossil’’ (Delson and
Rosenberger, 1984). The divergence date for the alouattin lineage obtained from molecular clock studies is
approximately 15.5 Ma, and the extant species of
Alouatta begin their divergence from one another at
approximately 7 Ma (Meireles et al., 1999; Collins and
Dubach, 2000a,b; Collins, 2001; Cortés-Ortiz et al.,
2003). It has been suggested that Protopithecus is part
of a more primitive Miocene radiation (Rosenberger
et al., 2009) and the same could be said of Paralouatta
that is represented by Pleistocene material as well as
the Miocene talus referred to Protopithecus marianae
Fig. 13. Ateline cladogram modified from Jones (2008). The branching pattern and divergence dates for the extant taxa reflect results from
molecular studies (Meireles et al., 1999; Collins and Dubach, 2000a,b;
Collins, 2001; Cortés-Ortiz et al., 2003). Protopithecus provides support
for these evolutionary transitions. Several steps not included in the original figure along the alouattin branch can be added, such as a size
decrease and craniodental changes associated with an increase in folivory and use of howling behaviors. The exact order and timing of those
changes are unknown; however, they must have occurred between the
more primitive alouattin Protopithecus and the appearance of Paralouatta and Stirtonia, fossil taxa from the Miocene which are more similar to extant Alouatta cranial and dental morphology, respectively.
(Rivero and Arredondo, 1991; MacPhee et al., 2003).
Just because we have not yet uncovered older Protopithecus fossils, it does not mean that they were not there.
The lack of specifically Alouatta-like traits in the forelimb reported here further supports a basal position for
Protopithecus; it is unlikely that a late-evolving Pleistocene giant Alouatta would become more suspensory and
not retain Alouatta-like aspects of the postcranium or
alouattins was a more suspensory animal than previously thought (Jones, 2008). This supports the hypothesis that Protopithecus is a primitive alouattin, moving
toward the extant condition in regards to cranial adaptations, but lagging behind in retaining a forelimb more
adapted for suspensory locomotion.
The general qualitative observations made above are
backed up by the quantitative analyses performed here
as the fossils are never grouped with extant primate
leapers or terrestrial quadrupeds. The hypothesis presented by Heymann (1998) suggesting a high degree of
terrestrial locomotion for Protopithecus is refuted by
these results, although using the ground for specialized
feeding behaviors or to cross short open patches in the
habitat is still likely. Nothing in the morphology of these
large monkeys would prohibit ground use. The multiple
links to Brachyteles seen throughout the analyses vindicate the original nineteenth century functional interpretations of Protopithecus as a large member of this genus.
The fossils are never grouped with Alouatta, reinforcing
their mosaic nature and emphasizing the differences
between the Protopithecus cranial and postcranial skeleton (also see Rosenberger et al., in review). However,
there is no need to invoke homoplasy or convergent evolution, as was suggested when the TBV skeleton was
discovered (Hartwig and Cartelle, 1996); newer analyses
suggest that the last common ancestor of atelins and
The author thanks Dr. Castor Cartelle of the Museu
de Ciências Naturais at the Pontificia Universidade
Católica de Minas Gerais in Belo Horizonte, Brazil, and
Dr. Kim Aaris at the Universitets Zoologisk Museum in
Copenhagen, Denmark, for access to the fossil material,
and Eileen Westwig (AMNH), Linda Gordon (NMNH),
and Dr. Leandro Salles (MN) for access to the extant primate collections. The author also thanks Drs. Jeffrey
Laitman, Alfred Rosenberger, and Walter Hartwig for
sponsoring this special issue and allowing her to participate. The author especially thanks Drs. Eric Delson,
Michelle Singleton, Melissa Tallman, and Sergio Almécija for their support and very helpful comments during
the revisions of the manuscript.
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morphology, locomotor, repertoire, protopithecus, forelimb, brasiliensis, reconstruction
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