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Locomotor Diversification in New World MonkeysRunning Climbing or Clawing Along Evolutionary Branches.

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THE ANATOMICAL RECORD 294:1991–2012 (2011)
Locomotor Diversification in New World
Monkeys: Running, Climbing, or Clawing
Along Evolutionary Branches
1
DIONISIOS YOULATOS1* AND JEFF MELDRUM2
Department of Zoology, Aristotle University of Thessaloniki, School of Biology,
Thessaloniki, Greece
2
Department of Biological Sciences, Idaho State University, Pocatello, Idaho
ABSTRACT
Modern platyrrhines exhibit a remarkable diversity of locomotor and
postural adaptations, which evolved along multiple trajectories since the
initial immigration to the island continent of South America. We trace
this diversification by reviewing the available paleontological and neontological data for postcranial morphology and ecological adaptation. Fossil
platyrrhines are notably diverse, from the Oligocene Branisella, to the
varied Patagonian early Miocene quadurpedal-leaping and quadrupedalclimbing fossils of disputed affinities, on through the rich middle Miocene
Colombian quadurpedal-leaping forms. More recent taxa exhibit even
more derived positional patterns, from the largest suspensory atelids in
Pleistocene Brazil, to the remarkable Antillean radiation with suspensory
forms and also semiterrestrial species, with postcranial morphology convergent on some Old World monkeys. Field studies of positional behavior
of modern platyrrhines set the framework for a spectrum of locomotor
adaptations. Central within this spectrum is a cluster of medium-sized
species with generalized locomotion (quadrupedal-leaping). At opposite
poles lie the more derived conditions: large-bodied species exhibiting locomotor specializations for climbing-suspension; small-bodied species exhibiting adaptations for claw climbing and leaping. This behavior-based
spectrum of locomotor diversification is similarly evident in a morphology-based pattern, that is, that produced by the shape of the talus. The
implications of the record of platyrrhine postcranial evolution for the competing hypotheses of platyrrhine phylogenetic patterns, the ‘‘long lineage
hypothesis’’ and the ‘‘stem platyrrhine hypothesis,’’ are considered. Anat
C 2011 Wiley Periodicals, Inc.
Rec, 294:1991–2012, 2011. V
Key words: platyrrhines; locomotion; evolution; fossils; talus
New World Monkeys (NWMs) are a diverse radiation
of anthropoid primates that currently occupy a wide
range of habitats spanning the American continents,
from southern Mexico to Northern Argentina. They represent almost 1/3 of all living primates, with several
extant species discovered and identified quite recently
and others differentiated through more profound taxonomic analyses (see Rosenberger et al., 2009). The present day diversity of NWMs is generally held to be the
result of a single colonization by a group of primitive
anthropoids, which rafted over the Paleogene Atlantic
Ocean from Western Africa aided by paleowinds and currents (Ciochon and Chiarelli, 1980; Hoffstetter, 1980;
Fleagle, 1999; Houle, 1999). If this scenario holds true,
C 2011 WILEY PERIODICALS, INC.
V
NWMs are most likely monophyletic, a conclusion that
has received support from molecular studies, such as
transposable Alu elements (Singer et al., 2003).
Grant sponsor: Aristotle University of Thessaloniki.
*Correspondence to: Dionisios Youlatos, Aristotle University
of Thessaloniki, School of Biology, Department of Zoology, GR54124 Thessaloniki, Greece. Fax: þ302310998269.
E-mail: dyoul@bio.auth.gr
Received 15 September 2011; Accepted 16 September 2011
DOI 10.1002/ar.21508
Published online 1 November 2011 in Wiley Online Library
(wileyonlinelibrary.com).
1992
YOULATOS AND MELDRUM
Alternately, multiple colonization lineages, or events,
would have resulted in paraphyly in NWMs, as suggested by the analysis of antigenic determinants from
selected serum proteins (Bauer and Schreiber, 1997). In
either case, the timing of this event, or events, remains
uncertain, but likely occurred sometime before the late
Eocene, earlier than 37 Ma (Houle, 1999; Kay et al.,
2004; Seiffert et al., 2004). To survive the transoceanic
journey, protoplatyrrhines were likely preadapted to
strong seasonal variations in water availability in their
original (African) environment (Houle, 1999). South
America of that time was characterized by a cooler, seasonal climate, and dominated by a mixture of forests
and vast open grasslands (MacFadden, 2000). This
diverse habitat undoubtedly played a significant role in
platyrrhine diversification and dispersal.
Modern platyrrhines occupy diverse habitats such as
the forests of the great Amazonian basin, the semideciduous Atlantic forests, and the drier savannas, grasslands, or shrub lands that exist either within extensive
forested areas (e.g., Guyanan savannas) or on the
fringes of great forests (e.g., Venezuelan llanos). The exploitation of such varied habitats has resulted in distinct
morphological,
ecological
and
behavioral
adaptations, which are broadly correlated to specific
phylogenetic groups (Ford and Davis, 1992; Rosenberger, 1992; Fleagle and Reed, 1996, 1999; Youlatos,
2004; Rosenberger et al., 2009). The depth of these
lneages is still debated. Rosenberger et al. (2009) and
Rosenberger (2010) advocate the ‘‘long lineage hypothesis’’ (LLH) that modern NWMs are characterized by a
number of long-lived clades and the sufficiently known
fossil taxa are actually early affiliates of these. The
interpretation of some divergence date estimates, based
on molecular clock data, appear to support the LLH
(e.g., Schneider et al., 2001; Opazo et al., 2006;
Schrago, 2007). In contrast, Kay et al. (2008) and Kay
and Fleagle (2010) propose the ‘‘stem platyrrhine hypothesis,’’ concluding that most early Patagonian fossils
bear no relationships to particular modern clades.
Instead, they comprise an earlier radiation, now largely
extinct, and filled niches analogous to the ones occupied
by modern platyrrhines, which are presumed to be the
latest in a series of radiations. Kay and Fleagle (2010)
point out that different methodologies produce varying
results from the same data, that is Opazo et al. (2006),
and that alternate divergence times lend support to the
stem playrrhine hypothesis.
Modern platyrrhines form groups with rather evident
and distinct adaptations that have been well-studied
behaviorally (e.g., Garber, 1992; Janson and Boinski,
1992; Kinzey, 1992; Rosenberger, 1992; Strier, 1992) and
morphologically (e.g., Erikson, 1963; Hershkovitz, 1977;
Fleagle and Meldrum, 1988; Ford and Davis, 2009). In
this article we will adhere to the revised phylogeny of
Kay et al. (2008), that is the Pitheciidae consist of the
Pitheciinae (Cacajao, Pithecia, Chiropotes) and Callicebus; the Cebidae consist of the Cebinae ([Cebus, Saimiri]
and Aotus} and the Callitrichinae; the Atelidae are
Alouatta, Ateles, Barchyteles, and Lagothrix. This is not
to say that alternate phylogenies are without merit.
However, the subtleties of distinctions are beyond the
scope of this review of postcranial and locomotor
diversification.
Pitheciids are medium-sized forest canopy dwellers,
which move mainly quadrupedally, on intermediate
length limbs, with variable rates of suspension (especially hindlimb suspension) and leaping, and feed on
hard or unripe fruit, as well as seeds, insects and leaves
(Kinzey, 1992). Cebines are medium-sized dwellers of
many forest types and all forest strata, which forage
both on fruit and invertebrate and vertebrate prey via
more active and manipulative behaviors, moving along
with quadrupedalism and leaping (Janson and Boinski,
1992). Callitrichines are small, mainly predacious dwellers of diverse forest types and strata, which base their
diets on arthropods and gums using quadrupedalism,
leaping and clawed scansorial locomotion in variable
degrees (Garber, 1992). Finally, atelids are the largest
NWMs dwelling in the upper canopy layers, depend
mainly on fruit and leaves and employ more climb/clambering and suspensory patterns of locomotion, on relatively lengthened limbs, via the aid of their prehensile
tails (Rosenberger and Strier, 1989; Strier, 1992).
The successful exploitation of these divergent niches
requires positional behaviors that enable food foraging,
manipulation, and ingestion, access to potential mates
and escape from potential predators (see e.g., Garber,
2007). Therefore, the study of primate locomotion is fundamental to understanding their adaptive diversity. The
objective of this review is to summarize locomotor patterns for both fossil and modern NWMs, deciphering correlated patterns of adaptive radiation. While the fossil
record of NWMs, especially with regard to postcranial
remains, is relatively scarce, growing interest in the
extant taxa of NWMs over the past decades has yielded
detailed numerous quantitative reports of their anatomy
and positional behavior. A lack of significant contributions for certain groups, past and present, is evident, as
well as the aforementioned lack of concensus on phylogenetic relationships between fossil and modern taxa. By
bringing together this information now, we hope to stimulate the recovery of more fossils, compell additional
study of the diverse moderns, and provide a fresh framework for asking questions.
OLDEST PLATYRRHINES
Branisella
The oldest records of NWMs in the Americas are Branisella boliviana and Szalatavus attricuspis from the
late Oligocene, more precisely the Deseadan South
American Land Mammal Age (SALMA) 26 Ma (Rosenberger et al., 1991c; Fleagle, 1999; Tejedor, 2008; Rosenberger et al., 2009). These earliest undoubted New
World anthropoid fossils consist mainly of dental and
fragmentary mandibular and cranial elements that have
been unearthed from the locality of Salla, Bolivia (Takai
and Anaya, 1996; Takai et al., 2000). The phylogenetic
relations of Branisella and Szalatavus are still debated.
Some authors, based on specific dental characters, suggest that the latter may be a junior synonym of the former and that they are both related to the rather derived
modern callitrichines (Takai et al., 2000). Alternatively,
these early forms are considered to bear no differential
affiliation to particular modern NWMs and do not establish the morphology of the modern platyrrhine morphotype (Fleagle and Tejedor, 2002). Branisella is 10
million years younger than the estimated age of invasion
LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES
of proto-platyrrhines to South America (Kay et al., 2004,
2008). This gap is vexing since caviomorph rodents,
which are considered likely coimmigrants with platyrrhines, have been unearthed in earlier strata (e.g.,
McFadden, 1990; Rosenberger et al., 2009).
No postcranial fossils attributed to Branisella have
been recovered, providing no direct evidence of their
adaptations for positional behaviors. However, one of the
most notable features of the dentition of Branisella is
the high-crowned lower teeth and the heavy wear of
their cusps that may indicate a diet of very abrasive
food, such as silica-rich leaves or grasses (Takai et al.,
2000; Kay et al., 2001). On this basis some have inferred
a significant commitment to terrestriality, or at least an
understory habit in relatively open woodland where dental resistance to abrasives would have been an important selective factor. The paleo environment of Salla is
described as semiarid, where mainly high-crowned nonprimate mammalian grazers roamed (McFadden, 1990).
This might suit the profile of proto-platyrrhines as suggested by Houle (1999), that is, adapted to strong seasonal variations in water availability in their original
(African) environment. However, given the small body
size of 1,000 g, it is unlikely that terrestrial specializations played a significant role in the positional behavior
of Branisella. Any further inferences about its positional
behavior, in the absence of postcranial fossils, must
remain highly speculative.
THE SOUTHERN CONE: AN EARLY
RADIATION?
Dolichocebus
The oldest NWM fossil with referred postcranial elements is Dolichocebus gaimanensis from the Sarmiento
formation, Chubut Province, Argentina (Table 1). The
fossil, known from an almost complete but badly crushed
cranium, several isolated teeth, mandibular fragments
and a talus, dates from the early Miocene, Colhuehuapian SALMA at 20 Ma (Meldrum, 1990; Fleagle and
Tejedor, 2002; Kay et al., 2008). The phylogenetic affinities of this species have given rise to very divergent
views reflecting differing interpretations of platyrrhine
evolutionary radiations (Kay et al., 2008; Kay and Fleagle, 2010; Rosenberger, 2010). One view, based mainly
on a number of apparent cranial and postcranial synapomorphies, argues that the fossil is an early member of
the lineage leading to modern Saimiri (Reeser, 1984;
Gebo and Simons, 1987; Rosenberger, 1992; Tejedor,
2008; Rosenberger et al., 2009; Rosenberger, 2010). An
alternative view, relying most recently on a large craniodental parsimony analysis, characterizes this fossil and
several others (see below), as stem platyrrhines, as
noted above (Meldrum, 1993; Kay et al., 2008; Hodgson
et al., 2009; Kay and Fleagle, 2010).
The sole postcranial element that has been attributed
to D. gaimanensis is a well-preserved talus (Fig. 1)
which appears to bear the closest morphological affinity
to Saimiri, Cebus, and Callicebus but looks remarkably
primitive in its lack of most conspicuous platyrrhine features (Reeser, 1984; Gebo and Simons, 1987; Ford,
1990a; Meldrum, 1990). Its morphology indicates a generalized function with a preponderance of frequent arboreal quadrupedal activities, and specializations for
increased leaping (Gebo and Simons, 1987; Ford, 1990a;
1993
Meldrum, 1993). A generalized positional pattern such
as this would have enabled the medium-sized Dolichocebus (1,500 g: Kay et al., 2008) to exploit a particularly
diversified seasonal mosaic habitat, which may have
typified the southern cone of South America during this
period (Rosenberger et al., 2009).
Southwards, the Pinturas Formation in the northwest
of Santa Cruz Province, Argentina, has yielded a relatively diverse collection of fossil NWMs (Fleagle and
Tejedor, 2002; Tejedor, 2008). They date from the early
Santacrucian SALMA with an age estimate of 17.5–16.5
Ma (Fleagle and Tejedor, 2002; Rosenberger et al., 2009).
Two genera are described, Soriacebus and Carlocebus,
which both include referred postcranial elements (Table
1). Their morphology has provoked interesting debates
over the phylogeny of early platyrrhines.
Soriacebus
Soriacebus, with an estimated body weight of 1,800 g,
is characterized by an anterior dentition and a deep
mandibular ramus, which resemble those of living Pitheciinae. It was initially described as having resemblances
to Callitrichinae and Pitheciinae (Luchterhand et al.,
1986) and then argued to be an early member of the latter group (Rosenberger et al., 1990; Rosenberger, 1992;
Tejedor, 2000, 2008). However, its posterior teeth are distinct and other studies again called into question pitheciine affinities, and supported the placement of this
genus with others in a stem platyrrhine group including
Dolichocebus (Kay, 1990; Kay et al., 2008; Kay and Fleagle, 2010) among others.
The single talus (Fig. 2) attributed to S. amenghinorum most resembles those of Pithecia and Alouatta (Meldrum, 1990). Functionally, the low, broad, and
moderately wedged trochlea and the short neck partly
covered by a distal extension of the trochlea all indicate
extensive talocrural movements in multiple planes
(Ford, 1988, 1990a; Meldrum, 1990). Therefore, this morphology would be suggestive of arboreal quadrupedal
activities with frequent climbing/leaping and even suspensory activities, similar to extant Pithecia (Fleagle
and Meldrum, 1988). This repertoire also correlates with
body size and the reconstructed diet, which is frugivory,
likely specializing on unripe and woody fruit, but without any specialized seed-predator behavior (Rosenberger,
1992; Meldrum and Kay, 1997b; Rosenberger et al.,
2009). Whether the similarities in talar morphology
between S. ameghinorum and pitheciines indicate phylogenetic affinity or homoplasy, as with aspects of the dentition, remains uncertain.
A smaller species of this genus, S. adrianae, has an
estimated body weight of 800–900 g (Fleagle, 1990).
Younger than S. ameghinorum, it differs only in a few
subtle dental traits. A partial calcaneus was recovered
from a locality rich in dental remains of S. adrianae and
is of appropriate size to be provisionally allocated to this
species (Meldrum, 1993). The fossil preserves a very narrow anterior calcaneal facet that stops short of the distal
end of the calcaneus. This condition has been associated
with an alternating tarsus possessing limited mobility,
especially in eversion and plantarflexion (Dagosto,
1988), likely associated with more quadrupedal and
clinging postures.
3.5 Ka
Holocene
6.7 Ka
Minas Gerais, Brazil
Toca de Boa Vosta, Bahia, Brazil
Cueva del mono fosil, Cueva alta, Cuba
Long Mile Cave, Jamaica
Skeleton cave, Jamaica
Several sites on Hispaniola
U, F, T
H, C, F, A
H, U, C, F
A
A, S, U
A
A
H, U, R, F
A
A
A
S, H, R, U, Mc, V, P, C,
F, T, Fi, A, Ca, Ta, Mt
A
A
H, U, F, T, A, C
H, R, U, Mc, C, F, T, Fi,
A, Ca, Ta, Mt
H, U, F, A, Ca, Ta
Postcranial
elements
2,000–5,000
10,000
2,000–5,000
25,000
1,000
850
850
20,000
1,500
2,500
1,800
?
2,700
?
1,500
2,000
2,200
BW (g)
AQW, CL
ATQW
CL, SUS
CL, SUS
AQW
AQW, L
AQW, L
CL, SUS
AQW, L
AQW, CL
AQW, CL
AQW, L
AQW, L
AQW
AQW, L
AQW, L
AQW, L
positional
behavior
Abbreviations are used for postcranial elements (A: talus, C: os coxae, Ca: calcaneus, F: femur, Fi: fibula, H: humerus, MC: metacarpals, MT: metatarsals, P: phalanges, R: radius, S: scapula, T: Tibia, Ta: distal tarsals, U: ulna, V: vertebrae) and for inferred positional behavior (AQW: arboreal quadrupedal walk/run, ATQW:
arboreal and terrestrial quadrupedal walk/run, CL: climb and clamber, L: horizontal leaping, SUS: suspensory and brachiation).
Antillothrix
Paralouatta varonai
Xenothrix
20 Ka
13.5–11.8 Ma
13.5-11.8 Ma
13.5–11.8 Ma
20 Ka
Aotus dindensis
Laventiana
Neosaimiri
Caipora
Protopithecus
Sarmiento, Chubut, Argentina
Pinturas, Santa Cruz, Argentina
Pinturas, Santa Cruz, Argentina
Alto Rio Cisnes, Chile
Santa Cruz, Santa Cruz, Argentina
Domo de Zaza, Lagunitas, Cuba
Colon Cura, Neuquen, Argentina
La Venta, Madgalena Valley, Colombia
La Venta, Madgalena Valley, Colombia
20.0 Ma
17.5–16.5 Ma
17.5–16.5 Ma
16.5 Ma
16.4 Ma
14.7–18.5 Ma
15.8 Ma
13.5-11.8 Ma
13.5–11.8 Ma
Dolichocebus
Carlocebus
Soriacebus
Rio Cisnes talus
Homunculus
Paralouatta marianae
Proteropithecia
Nuciruptor
Cebupithecia
La Venta, Madgalena Valley, Colombia
La Venta, Madgalena Valley, Colombia
La Venta, Madgalena Valley, Colombia
Toca de Boa Vosta, Bahia, Brazil
Locality
Age
Fossil
TABLE 1. Fossil New World monkeys with known postcranial remains
1994
YOULATOS AND MELDRUM
LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES
1995
Fig. 1. Left talus (MACN-CH 362) attributed to Dolichocebus gaimanensis, as seen in dorsal (A), proximal (B), medial (C), plantar (D), distal (E), and lateral views (F). Scale bar equals 0.5 cm.
Carlocebus
The other NWM from Pinturas is the larger (2,600
g) Carlocebus. Adaptively, the shearing crests of its
molars suggest frugivorous habits (Fleagle and Tejedor,
2002). The genus is quite different from Soriacebus, and
the more generalized morphology of its teeth suggest
similarities to the Callicebus clade (Fleagle and Tejedor,
2002; Tejedor, 2008). Alternately, such morphology could
be considered homoplasic or primitive and it is possible
that the genus also belongs to an earlier platyrrhine
radiation, more closely related to Dolichocebus (Kay
et al., 2008; Rosenberger, 2010).
1996
YOULATOS AND MELDRUM
verging proximally. There was apparently a strong distal
tibiofibular syndesmosis extending 15 mm along the distal tibial shaft, indicating a more stable talocrural joint
associated with rapid quadrupedal running and/or leaping. A partial calcaneus is also referred to this genus.
The posterior articular facet is quite long with a low
angle to the long axis of the calcaneus. The anterior
facet is very broad and extends to the distal end of the
calcaneus. These features are associated with either
leaping or suspensory climbing behaviors or a combination of the two (Ford, 1990a).
These behavioral patterns are also suggested by the
morphology of the fragmented scapula and ulna. The
piriform shape of the glenohumeral facet and the angles
of the spine with the axillary border and that with the
glenoid indicate quadrupedal behavior with enhanced
forelimb use, such as climbing and clambering. In addition, the height of the coronoid process, the reduced
width of the sigmoid notch, and the moderate olecranon
indicate an ulna that works mainly in controlled flexed
stances similar to those encountered during climbing
and climbing activities (Anapol and Fleagle, 1988).
The similarities in the positional behavior of both
Soriacebus and Carlocebus, which employ quadrupedal
activities along with climbing/clambering behaviors,
appear consistent with their reconstructed frugivorous
diets and suited to the paleoenvironmental evidence.
Pinturas was very likely a mixed habitat, dominated by
tropical forests, along with partly forested and watered
areas, as well as even drier areas where dune formation
could have been feasible (Bown and Larriestra, 1990).
SEEDS OF EARLY DIVERSIFICATION
Fig. 2. Tali of Pinturas primates. A–D: Referred to Carlocebus cf.
carmenensis. E referred to Soriacebus ameghinorum.
Postcranially, Carlocebus is known from four wellpreserved tali (Fig. 2) (Meldrum, 1990), distal tibia and
partial calcaneus (Meldrum, 1993) and a fragmentary
scapula and ulna (Anapol and Fleagle, 1988). None of
this material has direct association with craniodental
specimens. The general morphoplogy of the tali approximates that of Callitrichinae and small Cebinae. More
precisely, they share a moderately low and broad trochlea, a very broad, slightly medially directed talar neck,
an oval head in distal view, and a broad shallow posterior calcaneal facet, while the dorsal surface of the trochlea extends onto the talar neck to form a very deep
cavity for the tibia. These features rather suggest a mixture of quadrupedal activities with some moderate leaping behavior probably from vertical postures (Meldrum,
1990). In addition, this repertoire could have been supplemented by relatively ample and varied talocrural
movements, frequently associated with clambering.
An isolated distal fragment of a tibia articulates conformably with the aforementioned tali. The shaft is similar in robusticty to Homunculus. It broadens due to an
expansion of the distolateral border, supporting a broad
fibular incisure bounded by well-developed crests con-
Slightly north and westwards in the southern cone,
lies the Chilean site of Alto Rio Cisnes, which has
yielded a single primate talus that is currently unassigned and dates to the Friasian SALMA 16.4 Ma
(Tejedor, 2003, 2008—Table 1). Generally, the talus bears
some similarities to that of Callicebus and to those tali
referred to the Miocene Carlocebus, but is smaller,
nearer the size of Pithecia. Functionally, the moderately
high talar body with the parallel-sided rims, the relatively long neck, and the morphology of the tibial stops
and that of the proximal and distal calcaneal facets indicate predominantly arboreal quadrupedal behavior with
associated leaping (Gebo and Simons, 1987; Meldrum,
1990). The relationship between the fauna of this site
and Santacrucian faunas is not yet well understood
(Tejedor, 2003). If the evidence confirms that the fauna
from Rio Cisnes is closer in age to the Santacrucian
fauna, then the platyrrhine radiation would have been
more extensive during that period than previously
recognized.
Homuncuclus
South of the Pinturas site, another fossil platyrrhine
has been unearthed from several sites (Rio Gallegos,
Corrigüen Aike, Monte Observacion) of Santacrucian
age, 16.4 Ma (Tejedor and Rosenberger, 2008). Homunculus patagonicus is a medium-sized NWM (2,700 g)
known from partial skulls, mandibular fragments, teeth,
and long bones (Bluntschli, 1913, 1931; Meldrum, 1993;
Tejedor and Rosenberger, 2008). The overall morphology
LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES
1997
Fig. 3. Speculative reconstruction of the skeleton of Homunculus patagonicus. Darkened areas indicate
the associated elements of specimen MACN-A 635. Scale bar equals 5.0 cm.
of the species is reminiscent of Aotus and Callicebus,
and would thus suggest phylogenetic relationships
within the clade of Cebidae or Pitheciidae (Fleagle and
Tejedor, 2002; Tejedor and Rosenberger, 2008). The dentition is rather primitive (Tejedor, 1997, 2008) and the
more advanced morphologies seen in Proteropithecia and
later Pitheciinae (e.g., Nuciruptor, Cebupithecia) could
have evolved out of a Homunculus-like dentition (Tejedor
and Rosenberger, 2008). Functionally, the incisors and
premolars indicate hard-fruit eating, while the relatively
large cheek teeth suggest an important component of
hard fruits and leaves in its diet (Fleagle and Tejedor,
2002; Tejedor and Rosenberger, 2008; Rosenberger et al.,
2009). A varied diet probably suits the reconstruction of
the paleoenvironments as seasonal habitat with more
marginal conditions than a tropical forest, probably
resembling the gallery forests along rivers with exten-
sive areas of savannas (Bown and Fleagle, 1993; Fleagle
and Tejedor, 2002; Tejedor and Rosenberger, 2008; Rosenberger et al, 2009).
Limb proportions of Homunculus are similar to modern quadrupedal platyrrhines, such as Aotus and Callicebus (Meldrum, 1993; Tejedor and Rosenberger, 2008).
The humerus displays a number of features that suggest
climbing behavior, in agreement with the proportionately robust curved radius (Fig. 3). The capitulum is
spherical and quite ‘‘unrolled’’ relative to the long axis of
the humeral shaft, providing a greater range of flexion
and extension (Napier and Davis, 1959; Meldrum et al.,
1990). The lateral epicondyle is relatively large (Ford,
1990a), the trochlea is cylindrical and the medial epicondyle has little dorsal angle (Fleagle and Meldrum, 1988).
In the robust femur, the great degree of extension of
the femoral head and the distally placed fovea are both
1998
YOULATOS AND MELDRUM
features of habitually adducted hindlimbs. The greater
trochanter is very broad and rugous and overhangs the
femoral shaft anteriorly, providing expanded attachment
of the vastus lateralis muscle, an extensor of the knee.
The ridge of bone on the posterior surface of the proximal femoral neck, and the particularly deep patellar
groove, seem to promote rapid for-aft movements of the
thigh, necessary during leaping activities (Ford, 1988,
1990a; Meldrum, 1993). Therefore, this medium-sized
monkey exhibited a mosaic of locomotor behavior that
included quadrupedal walking and leaping, combined
with forelimb-assisted climbing.
Proteropithecia
In northwest Patagonia, in the Province of Neuquen,
the Collon Cura formation has yielded Proteropithecia
neuquenensis, a medium-sized (1,600 g) platyrrhine
known from isolated teeth and a talus (Kay et al., 1998).
The site is considerably younger, dating from 15.8 Ma,
and the associated fauna is slightly different from the
above mentioned Santacrucian, probably from the Colloncuran SALMA (South American Land Mammal Age).
The compressed and procumbent lower incisors and the
shallow basins and crenulated enamel of the lowcrowned molars indicate strong affinities with Pitheciinae, and Proteropithecia is considered as a basal member of the group. Adaptively, Proteropithecia has a molar
structure consistent with fruit- or nut-eating, while its
incisors rather suggest seed-eating in much the same
manner as extant pitheciins.
The talus shows overall resemblances to Aotus and
Callicebus. In general, the oval head, the moderate
neck, the shallow, narrow, and well-delineated dorsal tibial stop, the high and moderately wedged trochlea, and
the extended anterior proximal calcaneal facet are features that are frequently associated with relative stability and enhanced movements to the sagittal plane (Ford,
1988; Meldrum, 1990). Similar functions usually occur
during arboreal quadrupedal activities and moderate
leaping activities (Kay et al., 1998).
Nuciruptor
The La Venta region in the Magdalena Valley, Colombia, is the richest fossiliferous Cenozoic localitiy in
northern South America. From that region, Nuciruptor
rubricae is a medium-sized (2,000 g) fossil monkey that
is represented by a mandible and associated teeth (Meldrum and Kay, 1997), and possibly a referable isolated
talus. The age of the fossil is estimated at 13.5–11.8
Ma. The morphology of the mandibular corpus and the
procumbent and moderately elongate lower incisors and
low-crowned molar indicate that it is more derived than
Callicebus but more primitive than extant and most
other extinct pitheciines (Meldrum and Kay, 1997). It
appears to exhibit precisely those intial adaptations of
the dentition predicted for the earliest Pitheciinae, that
is incisors specialized for opening hard fruit and cheek
teeth able to masticate hard seeds (Kinzey, 1992; Meldrum and Kay, 1997).
An isolated talus has been excavated in El Cardon
Red Beds, a locality immediately adjacent to that of
Nuciruptor. The talus is well preserved with superficial
erosion of the head, posterior tubercles and calcaneal
facets and its size falls within the expected range of this
form. Although, allocation of this specimen is not yet settled, the relatively narrow head and neck and the more
rounded lateral rim of the trochlea would be suggestive
of talocrural movements along the sagittal plane, usually
associated with quadrupedal activities with some leaping
behaviors (Ford, 1988, 1990a; Meldrum and Kay, 1997).
Cebupithecia
Another fossil member of the Pitheciinae, which is
well represented in La Venta, is Cebupithecia sarmientoi. In effect, Cebupithecia, a medium-sized monkey
(1,800 g), is one of the most complete fossil platyrrhines ever found other than the subfossils from the
Caribbean and eastern Brazil, with associated cranial,
mandibular, dental remains, as well as a partial skelton
(Fig. 4; Stirton, 1951; Stirton and Savage, 1951; Davis,
1987; Meldrum and Kay, 1990; Meldrum and Lemelin,
1991; Meldrum, 1993; Hartwig and Meldrum, 2002). The
dentition is clearly synapomorphic with the living Pitheciinae, displaying procumbent upper incisors, large projecting canines that are triangular in cross-section, and
quadrate molars with poorly developed cusps and crests.
On the other hand, premolars appear to be less specialized than in modern forms, and finally the bunodonty
and shallow hypoflexids and raised talonids appear even
more primitive (Meldrum and Kay, 1997). Thus, Cebupithecia appears to be more derived than Nuciruptor in
the direction of living Pitheciinae, with specializations
for opening hard fruit and seed predation. Its cheek
teeth were also able to masticate hard seeds in a similar
manner to extant pitheciins (Meldrum and Kay, 1997).
Postcranially, Cebupithecia appears to lack most apomorphic traits of modern Pitheciinae (Fleagle and Meldrum, 1988; Ford, 1990a; Hartwig and Meldrum, 2002).
Its limb proportions fall within the range of monkeys
that are mainly quadrupedal and use moderate amounts
of leaping, such as the cebines and Callicebus (Meldrum
and Lemelin, 1991; Hartwig and Meldrum, 2002). The
humerus is characterized by a large lateral epicondyle, a
sharp trochleo-capitular ridge and a narrow and deep
biccipital groove. These features are frequently associated with controlled movements at the sagittal plane as
during quadrupedal activities (Ford, 1988; Meldrum
et al., 1990). The femur shows a marked posterior ridge
at the femoral neck and the head extends on the superior part of the neck, while the trochlea is high and well
demarcated, features that are usually associated with
leaping habits (Davis, 1987; Ford, 1990a; Meldrum,
1993). The distal tibia shows a markedly concave trochlear surface coupled with large inferior projections of the
anterior and posterior trochlear margin. These traits are
associated with a strongly curved and deeply grooved
astragalar trochlea with sharp medial and lateral crests
and a distal deep extension on the talar neck. They suggest a relatively stable ankle joint adapted for quick
pivots as during leaping (Ford, 1990a). Therefore, Cebupithecia appears to have been a medium-sized quadrupedal monkey with increased rates of leaping behavior
(Hartwig and Meldrum, 2002), probably not as frequently exhibited as in modern P. pithecia but more
likely comparable with the other members of the
subfamily.
1999
LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES
Fig. 4. Reconstruction of the composite skeletal anatomy of Cebupithecia sarmientoi. Darkened areas
indicate preserved portions of the skeleton. Scale bar equals 5.0 cm.
TABLE 2. Percentages of major locomotor modes of extant Pitheciidae (QWR, arboreal quadrupedal
walk, bound, run; CL, clamber, vertical climb; L, leap, drop, hop; S, bridge and suspensory locomotion)
Species
Pitheciinae
Pithecia pithecia
Pithecia pithecia
Pithecia monachus
Chiropotes satanas
Chiropotes satanas
Cacajao calvus
Callicebinae
Callicebus cupreus
Callicebus brunneus
Callicebus torquatus
Site
QWR
CL
L
S
Lago Guri, Venezuela
Raleighvallen-Voltzberg, Surinam
Yasuni, Ecuador
Lago Guri, Venezuela
Raleighvallen-Voltzberg, Surinam
Lake Teiu, Brazil
25.6
25
46.8
41.2
80
39.9
21.8
5
22.9
20.4
2
25.2
52.6
70
28.4
36.2
18
33.8
_
_
1.9
2.2
_
1.1
Yasuni, Ecuador
Manu, Peru
Estacion Biologica Callicebus, Peru
54.1
49.3
66.9
26.7
12.4
9.2
17.7
38.3
23.9
1.5
_
_
Extant Pitheciinae
Modern Pitheciinae exhibit a regular repertoire where
both quadrupedal activities and leaping behavior are the
dominant positional categories (Table 2). Among them,
Pithecia appears to be the most saltatory, and more particularly P. pithecia, where almost half of its repertoire
is represented by different forms of horizontal leaps and
hops (Fleagle and Mittermeier, 1980; Walker and Ayres,
1996). This is further evident in the postcranial morphology of the species, with functional traits that favor
stability, restricted mobility to the sagittal plane and resistance to high loads (Fleagle and Meldrum, 1988;
Ford, 1988, 1990). In contrast, P. monachus seems to be
more quadrupedal (Youlatos, 1999), and this is reflected
in its postcranial morphology as well (Meldrum and
Lemelin, 1991; Meldrum and Kay, 1997), underscoring
the postcranial and positional flexibility of the genus
(Walker, 1993). Cacajao also appears to use leaps rather
frequently, but quadrupedal activities involving both
walking, climbing, and clambering are more dominant
(Walker and Ayres, 1996). This is also true for Chiropotes
(Fleagle and Mittermeier, 1980; Walker and Ayres, 1996).
Study of the postcranial morphology of this genus has
revealed functional traits that are associated with frequent above branch quadrupedal walking and running,
and some suspensory postures (Fleagle and Meldrum,
1988).
The other member of this family, Callicebus, which
represents the basal member of this clade, is basically
quadrupedal with variable, but generally moderate,
rates of leaping behavior (Table 2—Youlatos, 1999; Lawler et al., 2006).
A noteworthy positional behavior of the larger Pitheciinae is hindlimb suspension, involving extreme plantarflexion and inversion of the ankle, and bracing with
the tail in Chiropotes (Fig. 5—Fleagle and Meldrum,
1988; Meldrum, 1998). This reflects the occasional
2000
YOULATOS AND MELDRUM
in order to comprehend other trends of ecological morphology within this radiation.
ACTIVE FORAGERS
The Miocene paleocommunity of La Venta also include
several fossils representing the Cebinae, for which, however, few postcranial remains are known. These include
the well-represented genera Neosaimiri and Laventiana
(Hartwig and Meldrum, 2002; Tejedor, 2008). In addition, we also consider here Aotus dindensis, if night
monkeys actually form an integral part of the Cebidae
(e.g., Schneider et al., 1993, 1996; Horovitz et al., 1998;
Opazo et al., 2006; Kay et al., 2008), and not of the Pitheciidae (e.g., Ford, 1988; Rosenberger, 1992, 2010; Tejedor, 2008).
Neosaimiri
Fig. 5. Chiropotes satanas demonstrating hind-limb suspension
with tail bracing.
climbing and suspensory behaviors reflected in the knee
and ankle, and confirm their intermediate position
between the medium-sized generalized Cebinae and the
large-bodied suspensory Atelidae (Meldrum, 1990). Considering the reconstructed positional behavior of fossil
Pitheciinae with those behaviors for extant forms, we
observe a consistent pattern of quadrupedal walking–
running–bounding behavior with some variable component of leaping and hopping activities. All fossil forms
tend to exhibit a pattern resembling Callicebus and Chiropotes positional behaviors, quadrupedalism accompanied by some leaping. If Callicebus represents in some
form the postcranial prototype of ancestral platyrrhines
in its positional behavior (Ford, 1988), then all these
forms do not appear to have changed much since the
inception of the pitheciine radiation. Within this radiation, only Pithecia, and more particularly, P. pithecia (as
there are limited data for other species), departs far
from this blueprint. Cacajao also differs, since it evolved
in Amazonian flooded forests with quite discontinuous
canopies (Walker and Ayres, 1996). Additional data on
the positional behavior of other pitheciins are required
Neosaimiri fieldsi is a relatively small platyrrhine
(850 g) from the middle Miocene strata of La Venta,
with obvious affinities to modern Saimiri. This form is
known from several mandibles, many isolated teeth, as
well as an array of postcranial material (Meldrum et al.,
1990; Takai, 1994; Nakatsukasa et al., 1997). The dentition resembles closely Saimiri in the shape and proportions of the molars and crowns of other teeth (Takai,
1994), which seemed to support the proposal set out by
Rosenberger et al. (1991a) for synonomy within Saimiri.
However, several differences in the upper incisors, premolars and the third molar stand out as either autapomorphies, or synapomorphies with Cebus (Takai, 1994;
Tejedor, 2008). Furthermore, Kay and Meldrum (1997)
on the basis of dental and mandibular morphology advocated recognition of Neosaimiri, and it is to this position
we subscribe.
In terms of postcranial morphology, Neosaimiri, as
reviewed by Nakatsukasa et al. (1997), is characterized
by more rugose muscular markings indicating a more
heavily built monkey than its modern relative. In addition, it possesses a high humeral head, a distinct distal
humeral articular surface, a long olecranon process, a
very robust femoral neck, a narrow and deep femoral
patellar groove, a smaller anterior process of the distal
tibia, an absence of a distal surface extension on the anterior tibial shaft, an absence of an anterior midtrochlear depression of the talus, and a short distal
calcaneus relative to the calcaneal tuberosity. This suite
of distinguishing features indicates a dominant forelimb
in quadrupedal progression, a less stabilized upper ankle
joint, and a shorter power arm for plantar flexion. On
the basis of such functions, Neosaimiri would have been
an arboreal quadruped employing frequent horizontal
leaps across gaps in a forested environment.
Laventiana
Laventiana annectens is a taxon very closely related to
Saimiri (Rosenberger and Setoguchi, 1991) and is often
considered as a junior synomym of Neosaimiri (Takai,
1994; Meldrum and Kay, 1997) or congener of Neosaimiri (Kay and Meldrum, 1997). In La Venta, it is represented by a rather complete mandible (Rosenberger
et al., 1991c), a talus (Gebo et al., 1990), and a distal
tibia (Meldrum, 1993). Its molars exhibit a buccal
LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES
2001
nberger, 1987). It was represented originally by a mandible, fragmentary maxilla, and possibly an isolated talus,
but other material has since been added (Takai et al.,
2001). The morphology of the dentition is very similar to
modern Aotus, with slight differences in the incisors and
the less elevated premolar trigonids.
The general morphology of the talus has been compared with that of Aotus and Callicebus (Gebo et al.,
1990). Alternately, comparisons have been made to the
talar morphology of the Callitrichinae (Meldrum, 1993).
Functionally, the large head, the wide and short neck,
the moderate height of the square-shaped trochlea, the
comparably shallow groove, the rounded medial trochlear crest, and the more obliquely facing tibial malleolar
cup are a combination of features that enable arboreal
quadrupedal movements of the foot with no indications
for extensive climbing or leaping (Gebo et al., 1990; Meldrum, 1993).
Extant Cebinae
Fig. 6. Distal tibia and talus of IGM 250436 (A) and IGM-KU 8803
(B) referred to Laventianna annectens, compared with corresponding
elements of Saimiri sciureus (C), Scale bar equals 1.0 mm.
cingulid and a distinct postentoconid notch, proposed as
a significant autapomorphy, but variably present in Neosaimiri and Saimiri.
The overall morphology of the talus is most similar to
living Cebinae (Fig. 6). It bears a moderately long talar
neck, a high and relatively short and wide talar body,
and a narrow talar head (Gebo et al., 1990). The distal
tibia is also most similar to Saimiri. Of particular note
is the indication of a well-developed syndesmosis of the
distal tibiofibular joint. The posterior surface of the tibia
is quite flat and the lateral border is marked by a pronounced ridge, along which the fibula would be
appressed, as in Saimiri and several other platyrrhines
including Aotus, Callithrix, Cebuella, and Pithecia. Only
Saimiri commonly displays the distinctive combination
of mediolateral widening and posterior flattening of the
distal tibial shaft (Meldrum, 1993). This morphology
appears to facilitate quadrupedal activities with high
rates of leaping behavior within an arboreal context.
Aotus
Aotus dindensis is relatively small-bodied (1,000 g)
and dates from 13.5 to 11.8 Ma (Setoguchi and Rose-
There is a strong bias in the study of positional behavior of capuchin and squirrel monkeys over owl monkeys.
Thus, there are no detailed data on the locomotion and
postures of Aotus; not surprisingly, as it is mainly nocturnal. Anecdotal descriptions and predictions from postcranial traits suggest a mainly quadrupedal primate
with moderate leaping activities (Wright, 1989). This is
also supported by postcranial similarities with Callicebus (Ford, 1988), which exhibits such positional patterns. If this is true, there appears to be little change
within this clade since the Miocene, as A. dindensis
from La Venta, is reconstructed to exhibit similar
behaviors.
On the other hand, data on three Saimiri species are
available and all show primarily quadrupedalism, with
variable rates of leaping behavior (Table 3). S. sciureus
seems to be the more saltatorial of the studied species
(Fleagle and Mitteremeier, 1980; Youlatos, 1999). S. boliviensis also uses considerable leaping, but is mainly
quadrupedal (Fontaine, 1990), while S. oerstedii exhibits
more frequent quadrupedalism than other species of
squirrel monkeys (Boinski, 1989). This positional profile
seems to agree with the predacious frugivory of squirrel
monkeys that range in many forest types exploiting all
forest strata (e.g., Janson and Boinski, 1992; Rosenberger, 1992). However, these reported variations may
result from differing sampling methodologies or habitat
differences. If both fossil relatives of Saimiri from the
Miocene, Neosaimiri and Laventiana, are reconstructed
as quadrupedal leapers, then they perhaps most approximate S. sciureus in positional patterns, and coincidentally, the extant range of the latter covers the La Venta
site in Colombia. Thus there appears to be no significant
changes in locomotor behavior since the Miocene within
this clade, as within the Aotus lineage.
Concerning Cebus, modern species appear to be rather
consistent in their patterns (Table 3). The four species
for which data are available indicate increased quadrupedal activities, coupled with variably significant rates
of leaping and variably moderate climbing/clambering
(Fleagle and Mittermeier, 1980; Gebo, 1992; Youlatos,
1998; 1999; Garber and Rehg, 1999; Wright, 2007;
Bezanson, 2009). These behaviors seem to suit the
adaptive profile of this generalist genus as a particularly
2002
YOULATOS AND MELDRUM
TABLE 3. Percentages of major locomotor modes of extant Cebidae: the Cebinae (QWR, arboreal
quadrupedal walk, bound, run; CL, clamber, vertical climb; L, leap, drop, hop; S, bridge and suspensory
locomotion)
Species
Saimiri oerstedii
Saimiri sciureus
Saimiri sciureus
Saimiri boliviensis
Cebus capucinus
Cebus capucinus
Cebus capucinus
Cebus albifrons
Cebus apella
Cebus apella
Cebus apella
Cebus olivaceus
Cebus olivaceus
Site
QWR
CL
L
S
Corcovado, Costa Rica
Yasuni, Ecuador
Raleighvallen-Voltzberg, Surinam
Monkey Jungle, U.S.A.
Santa Rosa, Costa Rica
La Suerte, Costa Rica
La Suerte, Costa Rica
Yasuni, Ecuador
Nouragues, French Guiana
Iwokrama, Guyana
Raleighvallen-Voltzberg, Surinam
Nouragues, French Guiana
Iwokrama, Guyana
88.1
45.1
55
73
55
60.8
78.1
48.5
33.9
53
84
32.5
50
4.5
24.2
3
5
26
9.9
13.2
17.7
29.2
12
5
30.8
11
7.4
25.4
42
20
15
25.9
5.0
27.3
23.6
26
10
26.7
32
_
5.3
_
2
4
3.4
3.7
6.5
13.3
9
1
10.0
7
TABLE 4. Percentages of major locomotor modes of extant Cebidae: the Callitrichinae (QWR, arboreal
quadrupedal walk, bound, run; CL, clamber, vertical climb; L, leap, drop, hop; CC, clawed locomotion)
Species
Saguinus fuscicollis
Saguinus fuscicollis
Saguinus tripartitus
Saguinus labiatus
Saguinus geoffroyi
Saguinus midas
Saguinus midas
Saguinus mystax
Saguinus mystax
Leontopithecus chrysomelas
Leontopithecus chrysomelas
Leontopithecus rosalia
Callimico goeldii
Cebuella pygmaea
Callithrix jacchus
Site
QWR
CL
L
CC
Catuaba, Brazil
Rio Blanco, Peru
Yasuni, Ecuador
Catuaba, Brazil
Barro Colorado, Panama
Nouragues, French Guiana
Raleighvallen-Voltzberg, Surinam
Rio Blanco, Peru
Padre Isla, Peru
London Zoo, UK
Edinburgh Zoo, UK
Washington Zoo, USA
Catuaba, Brazil
Yasuni, Ecuador
Rio de Janeiro, Brazil
38
47.6
40.3
49
43.3
32.5
76
51.6
61.5
51.3
60.2
44
18
27.1
32
6
12.4
10.4
9
7.4
28.7
_
12.0
6.3
0.9
1.5
15
4
5.8
13
38
32.5
33.7
37
41.5
26.5
24
30.9
27.4
31.9
23.2
23
62
24.4
23
18
6.3
15.6
5
7.7
12.1
_
4.3
4.8
15.9
15.1
15
16
42.7
32
agile and destructive omnivore which exploits all forest
strata, ground included, in a remarkable variety of habitats, resulting in nearly one of the most expanded geographical range among all NWMs (Janson and Boinski,
1992; Rosenberger, 1992). There are no pertinent fossils
with associated postcranial elements in order to directly
assess evolutionary trends within this clade. It is, however, safe to infer that these medium-sized taxa have
preserved a largely generalized positional behavior.
‘‘DWARVES AND CLAWS’’
Fossils such as Mohanamico, Patasola, Micodon, and
Lagonomico, from the middle Miocene La Venta locality,
have been related to the callitrichine radiation, although
debates about the exact phylogenetic relationships of some
of them (e.g., Mohanamico and Lagonomico) have not been
fully resolved yet (Rosenberger et al., 1990; Kay, 1994; Kay
and Meldrum, 1997; Rosenberger, 2002; Tejedor, 2008). This
radiation is characterized by shared derived features that
are related to their small size and concern understory,
trunk, and ground use, large and vertical branch use, squirrel-like locomotion using laterally compressed claw-like
nails, and dependence on exudates and arthropods (Ford,
1980; Garber, 1992; Garber et al., 1996). These forms are
known solely from cranial, mandibular, and dental material
with no associated postcranial elements thus far recovered.
Extant Callitrichinae
Neontological evidence of behavior and foraging patterns suggest different evolutionary patterns within the
callitrichines. Molecular systematists, whose cladistic
model is followed here, place Saguinus as as the most
basal member of this clade (e.g., Wildman et al., 2009
and references cited therein). Several species of this genus intensively use quadrupedal walking and bounding
coupled with high rates of leaping, which basically consist of horizontal leaps between terminal branches (Table 4; Garber, 1980, 1991; Garber and Preutz, 1995;
Youlatos, 1999; Garber and Leigh, 2001; Youlatos and
Gasc, 2001). These positional patterns indicate that tamarins still exploit the small-branch milieu to a great
degree while being one of the most ecologically generalized of the large-branch feeders. Their lesser dependence
on gums, by comparison with marmosets, is also correlative with the generally low rates of claw-climbing and
clinging on large vertical supports (Table 4).
The callimico/marmoset radiation was the subject of a
recent extensive study (Ford et al., 2009). Callimico is
LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES
very specialized postcranially, especially in the hind
limbs and ankle joint, which are designed to facilitate
increased leaping by providing the necessary mechanical
advantage and required stability for load resistance
(Ford, 1988; Garber and Leigh, 2001; Davis, 2002;
Garber et al.; 2005, 2009). Behaviorally, callimicos exhibit particularly high rates of leaping, most of which
are vertical leaps (Garber et al.; 2005, 2009), while quadrupedalism, climbing and clawed locomotion are used in
a lesser degree (Garber and Leigh, 2001). These patterns
appear to be ecologically associated with the exploitation
of the lower forest strata with abundant vertical supports, where they frequently forage for arthropods and
collect fruit and fungi (Porter and Garber, 2004).
The marmosets, Cebuella and Callitrhix, are by far
the most ecologically specialized callitrichines; they
exploit large vertical branches in relation to their tree
gouging habits and year-round exudate feeding (Garber,
1992). This is complimented by their locomotor patterns
and associated morphology (Table 4; Davis, 2002; Ford
and Davis, 2009). Cebuella exhibits very high rates of
claw-climbing and clinging on large vertical supports as
well as frequent leaping, including high rates of vertical
leaps (Youlatos, 1999, 2009). Unfortunately, there are no
detailed data on the locomotion of Callithrix, apart from
a study in the Jardim Botanico of Rio de Janeiro, where
C. jacchus emphasized clawed locomotion, used similar
rates of quadrupedal walking and bounding, as well as
rather frequent leaps, of which a significant proportion
were short (Zaluar et al., 2010).
On the other hand, Leontopithecus, is quite specialized
in its own way, having evolved in the different forests of
Mata Atlantica (e.g., Hershkovitz, 1977; Garber, 1992;
Rosenberger et al., 2009): the long and slender upper
forelimbs with especially elongated digits III and IV, the
claw-like nails, and the enlarged incisors indicate an adept manipulative forager for both non-mobile prey and
fruit, as well as seasonal dependence on exudates gleaning (Garber, 1992). Unfortunately, there are no data for
Leontopithecus in the wild, but the few studies in zoos
suggest reliance on quadrupedal activities coupled with
leaping behavior (Stafford et al., 1994; Karantanis,
2010). Similar positional patterns would facilitate and
suit the intensive manipulative exploitation of the discontinuous canopy of all forest levels that lion tamarins
generally exploit.
These data indicate different positional strategies
across the different clades of the Callitrichinae. The
widespread combination of quadrupedalism and leaping
suggests this as the pattern of the common ancestor of
the group, most likely shared by the other members of
the Cebidae. In effect, leaping behavior is present in all
callitrichine clades, but extensive use of vertical leaping
is only common in Callimico and marmosets. Quadrupedalism is significantly reduced in Callimico and
Cebuella, most likely for different reasons. Finally,
clawed climbing and clinging, although used in variable
rates across the subfamily, tends to be particularly
important in Callitrhix and Cebuella, genera highly
dependent on exudate feeding.
2003
ecological features, particularly adapted to below-branch
suspensory behaviors made possible by such features as
fully prehensile tails (e.g., Erikson, 1963; Rosenberger
and Strier, 1989; Strier, 1992). Their early fossil record
is relatively scant compared to other clades. The middle
Miocene Stirtonia from La Venta locality (13.5–11.8 Ma),
Colombia (Kay et al., 1987) is the earliest representative
of this clade, followed by the late Miocene Solimoea from
Solimoes formation (9–6.8 Ma) Acre, Brazil (Kay and
Cozzuol, 2006). There are no postcranial elements representing these early atelid forms. In stark contrast,
younger examples from the late Quaternary consist of
two remarkably complete skeletons of Pleistocene atelids
from Brazil: Protopithecus brasiliensis and Caipora bambuiorum. Their age is 20,000 BP (see Rosenberger
et al., 2009).
Protopithecus
Protopithecus brasiliensis is the largest fossil NWM
(25,000 g) and was discovered in cave deposits in
Minas Gerais and Toca da Boa Vista, Bahia (Hartwig
and Cartelle, 1996). The fossil is known by a virtually
complete skull and skeleton and bears a unique mixture
of traits, including several derived characters shared by
all atelids. The skull shows many morphological similarities to Alouatta that could be ulitmately related to the
presence of an enlarged hyoid bone, but it lacks the
usual specializations for folivory found in the dentition
of howler monkeys (Hartwig and Cartelle, 1996).
Actually, it is very likely that Protopithecus was primarily a frugivore unlike Alouatta, which is highly folivorous (Rosenberger et al., 2009).
The postcranial skeleton of Protopithecus is much
more robust than in other Atelidae, probably due to its
large size. It is most similar to the suspensory Atelinae
(i.e., Ateles and Brachyteles), with traits indicatve of
‘‘brachiating’’ adaptations (Hartwig and Cartelle, 1996),
as opposed to Alouatta, which is more quadrupedal. This
is evident in the high intermembral index, low and wide
humeral trochlea, short ulnar olecranon process, and the
shape of the radial head (Hartwig and Cartelle, 1996).
This combination of cranial vs postcranial features poses
a dilemma for determining its phylogentic relationships
within the family. Hartwig and Cartelle (1996) proposed
that Protopithecus is the sister taxon to Alouatta, while
Fleagle (1999) argued that it is related to the Atelinae.
Jones (2008) likewise proposed two possible outcomes,
based on character trends related to brachiation within
this group. In her view, if Protopithecus is the sistertaxon of Alouatta, there was less change towards an
energy-maximizing strategy in the stem atelin lineage,
the last common ancestor of atelins is less Ateles-like,
and the energy-maximizing strategy would have evolved
in parallel in the Protopithecus, Ateles, and Brachyteles
terminal lineages. In contrast, if Protopithecus is the sister taxon of the Atelinae, there are many more parallelisms along the individual evolutionary branches (Jones,
2008).
Caipora
HEAVY WEIGHT CLIMBERS
The members of the Atelidae are the largest NWMs
and share a set of unique morphological, behavioral and
Caipora bambuiorum is another large NWM (20,000
g) recovered from Toca da Boa Vista, Bahia, and is represented by a second nearly complete skull and skeleton
2004
YOULATOS AND MELDRUM
TABLE 5. Percentages of major locomotor modes of extant Atelidae (QWR, arboreal quadrupedal walk,
bound, run; CL, clamber, vertical climb; L, leap, drop, hop; S, bridge and suspensory locomotion)s
Species
Alouatta caraya
Alouatta caraya
Alouatta paliatta
Alouatta paliatta
Alouatta seniculus
Alouatta seniculus
Alouatta seniculus
Alouatta seniculus
Alouatta seniculus
Ateles geoffroyi
Ateles geoffroyi
Ateles geoffroyi
Ateles paniscus
Ateles paniscus
Ateles belzebuth
Lagothrix lagotricha
Lagothrix lagotricha
Site
QWR
CL
L
S
ENSC, Alegrete, Brazil
Estancia Casa Branca, Brazil
La Suerte, Costa Rica
La Pacifica, Costa Rica
Raleighvallen-Voltzberg, Surinam
Nouragues, French Guiana
Yasuni, Ecuador
Tiputini Biodiversity Station, Ecuador
Fundo Pecuario Masaguaral, Venezuela
Barro Colorado, Panama
Barro Colorado. Panama
Tikal, Guatemala
Raleighvallen-Voltzberg, Surinam
Nouragues, French Guiana
Yasuni, Ecuador
Yasuni, Ecuador
Colombia
41.5
66.4
81.7
47
80
37.3
50.9
30.1
32.8
22.0
51.1
52
25.4
20.1
20.8
28.9
41.8
29.3
18.6
7.9
37
16
43.9
28.0
57.6
57.1
24.2
6.1
19
17.0
28.1
37.9
44.5
38.8
16.8
2.7
3.2
4
4
2.8
2.4
1.7
5.7
10.9
23.5
1
4.2
2.6
2.8
3.9
10.8
12.5
12.3
7.1
13
_
16.0
18.4
10.6
4.2
30.3
10.9
29
47.2
43.0
35.8
22.7
8.6
(Cartelle and Hartwig, 1996). Caipora appears to be
most similar to Ateles in cranial morphology, with a
large, rounded braincase and the quadrate, bunodont,
low-cusped molars.
The postcranium is very robust, probably due to its
large size, but the overall morphology is reminiscent of
the suspensory Atelinae and exhibits brachiating locomotor adaptations (Cartelle and Hartwig, 1996). This is
apparent in the high intermebral index, the large globular humeral head, the short olecranon process, the round
radial head and its ulnar facet, and the overall morphology of the metacarpals and metatarsals (Cartelle and
Hartwig, 1996; Jones, 2008). It is still unknown how
these fossil forms attained similar sizes in the Brazilian
forests, where they were recovered (Rosenberger et al.,
2009). The morphology of these recent fossil forms,
which are so closely related to the modern taxa, are certain to shed a bright light on the evolution of positional
behavior in Atelidae once the material is extensively
studied.
Extant Atelidae
Alouatta encompasses the smallest, as well as some of
the largest, species among the atelids. Howler monkeys
appear to have differentiated earlier than the other
forms and their locomotion is characterized by a preponderance of quadrupedalism. This involves both horizontal or inclined quadrupedal walking and clambering,
limited forelimb suspension, and especially tail-assisted
hindlimb suspension during feeding postures (Table 5;
Fleagle and Mittermeier, 1980; Schön Ybarra and Schön,
1987; Gebo, 1992; Bicca Marques and Calegaro Marques,
1998; Youlatos and Gasc, 2001; Youlatos, 2004; Prates
and Bicca Marques, 2008; Bezanson, 2009; Guillot,
2009). Of the studied species, A. seniculus appears to be
the one that exhibits more suspensory and much more
clambering/climbing activities (Table 5). These distinctions may be related to the varied habitats that this
wide-ranging species exploits.
The remaining three extant genera show a gradient of
increasing degrees of suspensory locomotion, with two
caveats: (a) there are limited data on the positional
behavior of Brachyteles, although anecdotal observations
coupled with an array of major forelimb traits, indicate
increased forelimb suspension similar to the welldescribed tail-arm brachiation of Ateles (Rosenberger
and Strier, 1989; Strier, 1992; Jones, 2008); and, (b) performance of suspended locomotion may be quite different
among the genera, as was documented by Cant et al.
(2003) for Lagothrix and Ateles (see also Lockwood,
1999). As the Atelinae evolved, they apparently became
larger in body mass and more suspensory in order to forage more efficiently and cover more distances in search
of sparsely dispersed food sources (Erikson, 1963; Jones,
2008). Tail-assited forelimb suspension is a remarkable
locomotor specialization that greatly facilitates canopy
travel by these large platyrrhines. Ateles is considered
the sister taxon of Lagothrix and Brachyteles (Meireles
et al., 1999; but see Collins, 2004), and apparently differentiated rapidly from the stem atelin group by pursuing
this forelimb-dominated suspensory locomotion and postures (Table 5; Mittermeier, 1978; Cant, 1986; Fontaine,
1990; Youlatos, 2002; Cant et al., 2001; 2003). Subtle differences in locomotion among the species of spider monkeys do exist (e.g., A. paniscus is the most suspenory
species while A. geoffroyi the least; Table 5), but it is difficult to assess any correlations with habitat or phylogenetic/eco-morphological parameters (Youlatos, 2008).
If Brachyteles and Lagothrix are indeed sister-taxa, it
suggests that the Ateles-like forelimb-dominated suspensory locomotion evolved in parallel in Brachyteles, in the
distinct Mata Atlantica, while Lagothrix assumed a different regime of frugivory-animalivory, coupled with a
different locomotor profile involving relatively high rates
of quadrupedalism and climbing/clambering activities
(Table 5; Defler, 1999; Cant et al., 2001). This is also
reflected in the postcranium of this genus, which differs
significantly from that of more suspensory Ateles and
Brachyteles (Erikson, 1963; Jones, 2008).
ISLAND DISPERSALS
Currently there are no nonhuman primates living on
the Caribbean islands. However, at least four different
genera have been unearthed from Pleistocene to Holocene strata of three different islands: Paralouatta from
Cuba, Antillothrix and Insulacebus from Hispaniola, and
LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES
Xenothrix from Jamaica (Cooke et al., 2011). The colonization of these islands by primates is potentially set
prior to the middle Miocene, due to a single talus apparently of that age from Cuba (see Iturralde Vinent and
MacPhee, 1999; MacPhee and Horovitz, 2002; Rosenberger et al., 2009). Colonization would have taken
place either via overwater dispersal, probably by rafting
(Ford, 1986; 1990b) or over a large, short-lived landbridge which connected mainland South America, Cuba,
Hispaniola, Puerto Rico, and the Lesser Antilles (Iturralde Vinent and MacPhee, 1999). Whether there was a
single primate colonization event (Horovitz and MacPhee, 1999; MacPhee and Horovitz, 2002), or multiple
(Rosenberger; 2002; Rosenberger et al., 2011) remains
uncertain. In either case, these forms underwent remarkable specialization, leading to some rather unique
endemic forms for which the phylogenetic relationships
remain contested. Some authors propose that all these
fossils form a monophyletic group which is the sister
taxon of Callicebus (Horovitz and MacPhee, 1999; MacPhee and Horovitz, 2002), while others advocate a more
complex biogeography: a pitheciine or Aotus affinity for
Xenothrix (Rosenberger, 1977; Tejedor, 2008), cebine
affinities for Antillothrix (MacPhee and Woods, 1982;
Rosenberger et al, 2011), and alouattine associations for
Paralouatta (Rivero and Arredondo, 1991; Rosenberger,
2002).
Paralouatta
The earliest primate fossil in the Greater Antilles is
Paralouatta marianae from the Cuban Miocene (14.68–
18.5 Ma) site of Doma de Zaza, known from a single talus (MacPhee et al., 2003). The specimen is characterized by a nonwedged trochlea, a long, slightly deviated
neck, a large head, and wide and extended calcaneal facets, suggesting mid-tarsal mobility that is usually associated with arboreal quadrupedal habits (MacPhee and
Meldrum, 2006). The geological evidence, and the presence of some marine fauna, indicates that the site lay
along the banks of the sea where several depositional
environments were present (MacPhee et al., 2003).
Paralouatta varonai, from the Holocene of Cuba is the
largest monkey (9,000–10,000 g) from the Antilles, as
large as any living platyrrhine. It is known from a wellpreserved skull, several mandibles, isolated teeth and
numerous postcranial elements (Horovitz and MacPhee,
1999; MacPhee and Horovitz, 2002; MacPhee and Meldrum, 2006). The skull exhibits a lack of cranial flexion,
the face projects upward with somewhat large orbits,
and the braincase is long and low, relatively large with
strong temporal and nuchal crests (Horovitz and MacPhee, 1999). The canine is very small and the cheek
teeth are crested and wear down in a conspicuously flat
fashion, indicating thick enamel (Horovitz and MacPhee,
1999; Rosenberger et al., 2009).
The suite of postcranial characters of Paralouatta is
not seen in other platyrrhines, but it exhibits intriguing
resemblences to certain so-called semiterrestrial Old
World monkeys. These traits favor limb movements relatively restricted to the sagittal plane, some resistance to
high reaction forces and overall stability of the joints.
Morphologies reflecting this in the fossil include the retroflexed medial epicondyle, the narrow trochlea and the
deep olecranon fossa in the humerus, the robust and
2005
straight ulna with a narrow proximal sigmoid notch that
does not flare laterally, the short-necked radius with a
proximal biccipital tubrosity, the marked and relatively
deep patella groove of the femur, the massive tibial
medial malleolus with an extended distal fibular facet,
the nonwedged talar trochlea and the short, straight
and relatively robust metapodials and phalanges (MacPhee and Meldrum, 2006).
Xenothrix
Xenothrix was a Pleistocene, medium to large-sized
primate (2,000–5,000 g) known from several cranial,
dental and postcranial elements found in six different
caves in Jamaica. The relatively short length of the humerus, wide and shallow biccipital groove, comparably
broad and distolaterally extensive capitulum, and the
moderately prominent trochlear lips indicate ample
quadrupedal movements in an arboreal habitat (MacPhee and Fleagle, 1991; MacPhee and Meldrum, 2006).
Similar adaptations are also evident in the ulna, with a
relatively short olecranon, a proximally wide sigmoid
facet and well-defined radial notch. In contrast, humeral
features such as the deep olecranon fossa and short, and
posteriorly directed medial epicondyle indicate more restricted quadrupedal activities, but these can also be
related to the relatively large size of the animal (MacPhee and Fleagle, 1991; MacPhee and Meldrum, 2006).
In the femur, the size and conformation of the greater
and lesser trochanters, the short, anteriorly convex diaphysis, exceptionally robust shaft, large and anteroposteriorly compressed distal epiphysis, shallow and wide
patellar groove, and asymmetry of the condyles indicate
controlled movements in various planes, suggesting cautious clambering activities (Ford, 1990a,b; MacPhee and
Fleagle, 1991; MacPhee and Meldrum, 2006). This is
also consistent with tibial morphology with large and
wide tibial plateau, prominence of the tibial tuberosity,
and the depth of evident muscle scars that suggest
powerful extension and flexion of the leg at the knee
(MacPhee and Fleagle, 1991).
Antillothrix
Antillothrix bernensis was a medium to large-sized
primate (2,000–5,000 g) recovered from several Pleistocene sites in Hispaniola. Two relatively complete skulls
have been allocated to the species, as well as some teeth,
isolated postcranial fragments, and a partial skeleto,
with its skull, presenting long bones, ribs, and vertebrae
(MacPhee and Horovitz, 2002; Tejedor, 2008; Rosenberger et al., 2011; Kay et al., 2011). Rosenberger (2002)
and Rosenberger et al. (2011) conclude affinities to
extant Cebinae. Others have proposed close relationship
to the Cuban Paralouatta, which together constitute the
sister group to Xenothrix (Horovitz and MacPhee, 1999;
MacPhee and Horovitz, 2002). A second newly discovered skull has been interpreted as a stem platyrrhine,
unrelated to any of the living families of NWMs (Kay
et al., 2011).
Several points of interest have been observed on the
isolated postcranials. The tibia displays a central position for a rather deep fibular facet, anterior and posterior trochlear borders extending inferiorly equally, and a
narrowed medial malleolus, all of which are suggestive
2006
YOULATOS AND MELDRUM
of sagittally oriented limb movements, that is, rapid arboreal quadrupedalism and leaping (Ford, 1986, 1990a;
MacPhee and Meldrum, 2006). Kay et al. (2011) note an
undescribed distal humerus fragment associated with
teeth attributed to Antillothrix resembling that of a typical platyrrhine arboreal quadruped. On the other hand,
recently described associated femur and ulna are anatomically distinctive, suggesting quadrupedal and climbing/clambering habits (Rosenberger et al., 2011). On the
basis of cranial shape of one recently recovered skull,
others have proposed a locomotor pattern probably similar to modern Alouatta (Kay et al., 2011).
ADAPTIVE RADIATIONS AND THE
DIVERSIFICATION OF LOCOMOTOR
PATTERNS IN PLATYRRHINES
The above review of the locomotor behaviors reconstructed for fossil platyrrhines and those of modern
taxa, reveals a remarkable diversity among NWMs. This
diversity appears to be differentially distributed among
well-defined divergent clades of extant genera, but with
possible examples of convergence in some fossil taxa.
Behaviorally, it can be interpreted in two ways: one concerns the postcranial adaptations correlated with body
size and substrate grain, both relative and absolute, that
promoted specific locomotor patterns within well-established lineages; the other concerns the way these
locomotor patterns promote niche partitioning of food
resources within specific assemblages through space and
time. However, these two views are not mutually exclusive (Rosenberger et al., 2009). Locomotion is one of the
principal links between morphology, ecology, and phylogeny and has been shaped through microhabitat utilization within specific contexts.
Assuming platyrrhine monophyly, we might ask what
was the original blueprint that gave rise to this notable
pattern of locomotor diversity encountered today among
the varied Central/South American habitats. On the basis of a comprehensive analysis of the postcranium of
both extant and fossil platyrrhines, Ford (1988, 1990a)
concluded that the ancestral platyrrhine was a small to
medium-sized (1,000 g) arboreal quadruped, which
emphasized quadrupedal running and walking, principally on horizontal branches, and included a significant
component of leaping in its locomotor repertoire. Ford
proposed Aotus as the most useful living model on the
basis of its postcranial traits. This is somehow ironic, in
the sense that there are no detailed quantitative observations, only anecdotal information on the locomotor
repertoire of owl monkeys. On the other hand, the postcranium of Callicebus is virtually equivalent to Aotus,
and this genus, as well as Saimiri, manifests similar
locomotor behaviors: frequent above branch quadrupedalism, substantial use of horizontal supports, and considerable leaping in variable rates. The same holds true
for the closely related Cebus, which frequently employs
similar locomotion, but it is somewhat larger in body
mass and more specialized in exploiting divergent
microhabitats by utilizing more destructive foraging
techniques. The generalized locomotor repertoire utilized by medium-sized platyrrhines has also been proposed, on the basis of assessing the available
postcranial elements, as a pattern relevant to the primitive anthropoid condition (e.g., Gebo and Dagosto,
2004). The essence of these behavioral reconstructions
reflect the correlations of locomotor behavior of small to
medium-sized platyrrhines (1,000 g) to substrate
grain and texture presented in the landmark work of
Fleagle and Mittermeier (1980).
A Principal Components Analysis (PCA) of the logtransformed percentages of the distinct locomotor modes
(quadrupedalism, climb/clamber, leap, suspensory, and
clawed locomotion) reveals an interesting pattern of locomotor variation among extant platyrrhines (Fig. 7).
Each axis contributed differentially to the separation of
the locomotor groups, particularly separating the more
specialized forms along respective axes. Medium-sized
platyrrhines characterized by a mixture of quadrupedalism and leaping are clustered around the intersection of
the axes. This cluster includes Saimiri, Cebus and Callicebus species. Large-bodied climbers/suspenders were
separated from above-branch locomotors on Factor 1,
which accounted for 44.7% (Factor 1 loadings of 0.827
and 0.830, respectively). The large bodied folivore-frugivores exhibit increased climbing and suspensory abilities and can readily exlploit the high canopies of mainly
rich, as well as poorer, forests (Strier, 1992). On the
other hand, the claw-climbing and leaping groups were
separated along Factor 2, which accounted for 29.1% of
explained variance, (loadings of 0.578 and 0.467, respectively). These are small-bodied insectivore-gummivores,
using claw-climbing, clinging and vertical leaping in the
understories of diverse types of forested habitats
(Garber, 1992). Some taxa, such as the Pitheciinae Chiropotes and Cacajao, and the Callitrichinae Saguinus
and Leontopithecus, overlap considerably with the central cluster, reflecting the less specialized nature of their
locomotor repertoires. Even Alouatta tended towards the
central cluster of ‘‘generalists.’’
This grouping pattern is not entirely evident, as some
sets of genera are quite dispersed on the plot, but this
may be an artifact of the original data, which was compiled from many separate studies. Problems of comparability across studies with differing localities and
methodologies have been acknowledged repeatedly in
the past. These inconsistencies of particulars understandably introduce variation that will not correlate
closely with broader generalizations made here. However, a comprehensive analysis of a selected anatomical
region, the ankle (i.e., talus), which is frequently recovered in the platyrrhine fossil record, revealed a strikingly similar pattern to the behavioral data (Meldrum,
1990). This was based on eleven dimensions and a multivariate analysis of the fundamental proportions of the
talus of 300 specimens of platyrrhine genera, excluding
only Brachyteles and Callimico. The pattern of variation
in this instance revealed four distinguishable groupings:
a central cluster of small-to-medium-bodied Aotus, Callicebus, Saimiri, and finally Cebus, exhibiting quadrupedal running and leaping; towards one pole, the smallbodied Callitrichinae, exhibiting claw-assisted scansorial
and clinging positional behaviors; towards the other
pole, the Pitheciinae, first the more quadrupedal Cacajao and Chiropotes, who also exhibit hindlimb suspension and foot reversal, followed by Pithecia; finally largebodied Alouatta and the other Atelidae at the extreme,
exhibiting climbing/clambering and suspensory behaviors, with increased tail-assited suspension in the latter
(Fig. 8).
LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES
2007
Fig. 7. Plot of modern platyrrhine genera on the first two axes of the Principal Component Analysis,
based on log-transformed percentages of grouped locomotor modes (quadrupedalism, climb/clamber,
suspensory, leap and claw-climb).
The inferred placement, on either plot (Figs. 7 and 8),
of the fossil species with known postcrania permitting
locomotor reconstruction, would exhibit a narrower spectrum of variation, with many extinct taxa falling within
the range of the central cloud of species, among quadrupedal leapers and quadrupedal/climbers. By contrast,
the younger large-bodied Caipora and Protopithecus
would align with the more suspensory extant Atelinae.
However, these locomotor patterns do not form exclusive
units, classified on a strictly phylogenetic basis. They
demonstrate adaptive strategies to specific habitats, at
times convergent, that are shared by more than one
sympatric or syntopic species (Fleagle and Reed, 1996,
1999).
Until the recovery of postcranial elements for the earliest platyrrhine fossil, Branisella, little can be said with
certainty about its locomotor behavior, other than perhaps a likely correlation to its body size and the locomotor behavior of similar-sized extant playrrhines, that is,
arboreal quadrupedal running and leaping. This may be
a moot point in the search for the ancestral platyrrhine
condition, if Branisella is a member of an ancient radiation of stem platyrrhines, which bears no apparent affinities to modern taxa (e.g., Rosenberger et al., 1991;
Takai et al., 2000; Kay et al., 2008). In that case, the
model proposed by Ford (1988), based on the study of
the locomotor diversity of extant platyrrhines, would
point to the ancestral morphology of the last common
ancestor of extant platyrrhine genera, rather than the
earliest and presumed ancestor of all platyrrhines, fossil,
and living.
The early Miocene fossils considered here, Dolichocebus, Soriacebus, Carlocebus, Homunculus (and Tremacebus, not known postcranially) from Patagonia, likely
represent a distinct ancient radiation (Kay et al., 2008;
Kay and Fleagle, 2010), in our view. The oldest of these,
Dolichocebus, shows the generalized mixture of quadrupedal activities with leaping behavior, which most
closely approximates Ford’s morphotype reconstruction.
If Dolichocebus is indeed a primitive member of the Saimiri lineage (Tejedor, 2008; Rosenberger et al., 2009), its
generalized locomotor reconstruction may be the bridge
2008
YOULATOS AND MELDRUM
Fig. 8. Three-dimension Principal Coordinates ordination of extant platyrrhine genera computed from
generic means of log transformed ratios. The minimum spanning tree is projected onto the horizontal plan
(see Meldrum, 1990).
between the early Miocene radiation and the diversity of
extant genera. Otherwise its postcranial generalization
would be merely a primitive retention for a small to medium-sized platyrrhine. On the other hand, Soriacebus
and Carlocebus seem to be postcranially more derived,
exhibiting mixed quadrupedal and climbing/clambering,
and even some suspensory habits, especially in Soriacebus (Meldrum, 1990). These adaptations, which very
likely enabled them to differentially utilize the ancient
forests and exploit the available fruit sources, seem to
parallel the evolution of locomotor patterns in Pitheciinae and Callicebus, where some authors align these fossils (e.g., Rosenberger, 2002; Tejedor, 2008; Rosenberger
et al., 2009). Thus, these platyrrhines may represent
early members of the pitheciid clade, or they represent
early forms that were adapted to analogous niches in
the early Miocene southern forests, convergent on the
pitheciid condition. By contrast, the dental pitheciine
Proteropithecia with its associated talus, as well as the
isolated talus from Chile, show no postcranial similarity
or convergence on the derived pitheciine condition,
rather morphologies correlated with generalized quadrupedalism and leaping, correlated with medium to small
body size, as in Callicebus for example (Kay et al.,
1998). The meager postcranial remains of these taxa do
not offer a clear resolution to the question of synapomorphy or homoplasy at this time. A pattern of convergent
niche partitioning might also be suggested by other
recovered fossil platyrrhines, such as the Callicebus-like
frugivore/folivore and quadrupedal leaper Homunculus,
whose inferred locomotion aligns with that of the titi
monkey’s generalized positional repertoire.
Even Antillothrix, the Pleistocene Hispaniolan fossil,
is now considered as a remnant of an early platyrrhine
radiation, probably similar to that of the early taxa discussed above (Rosenberger et al., 2011; Kay et al., 2011).
This is particularly interesting since this fossil seems to
exhibit a derived morphology correlated with quadrupedalism, climbing/clambering, and possibly even suspensory habits (Rosenberger et al., 2011; Kay et al., 2011).
This behavior could be a novel adaptation to niche partitioning in an isolated insular habitat, just as was the
peculiar semiterrestriality of Paralouatta in Cuba, and
the kinkajou-like suspension of Xenothrix in Jamaica
(McPhee and Fleagle, 1991). Alternatively, it could have
been retention of positional abilities of an earlier radiation similar to the early Miocene Argentinean fossils.
However, the overall plasticity of positional behavior
(e.g., Garber and Preutz, 1995) lends support to the former hypothesis.
In the middle Miocene, the rich paleo-community of
La Venta has been extensively studied (e.g., Hartwig
and Meldrum, 2002). The three sets of Nuciruptor and
Cebupithecia, Neosaimiri, and Laventiana, plus Aotus
dindensis, seem to represent three distinct adaptive
clades. The first favored hard or unripe fruit and seed
LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES
eating accessed by quadrupedalism and leaping; the second, an insectivorous/frugivorous diet acquired by
increased bouts of quadrupedal walk/run and leaping;
and the third, a frugivore/insectivore frequently using
quadrupedal walking/running and leaping behavior.
These adaptations seem very comparable to the ones
observed in modern counterparts of their respective
clades, such as Pithecia, Saimiri, and Aotus, where they
are found syntopically. All these three fossil groups seem
to have retained in some measure the positional adaptations of the earliest platyrrhine—a mixture of quarupedalism and leaping. Among the small- to medium-sized
platyrhrines, modern Cebinae and Aotus especially have
retained this pattern throughout their long evolutionary
history, whereas the Pitheciinae evolved towards two different patterns: relatively longer limbs and increased
suspensory behavior, and in the case of Pithecia pithecia,
increased clinging and leaping. P. pithecia, evolved to be
one of the most saltatorial modern platyrrhines (e.g.,
Fleagle and Meldrum, 1988).The sister taxa Cacajao and
Chiropotes adhere to a more quadrupedal strategy,
including a variable but significant amount of leaping,
which is performed in a different manner from that
encountered in Pithecia (Walker and Ayres, 1996), and
below-branch behavior, especially hindlimb suspension
(Fleagle and Meldrum; 1988; Meldrum et al., 1997; Meldrum, 1998).
Atelidae and Callitrichinae, the two most derived
groups that were mentioned earlier, have been the subject of extensive studies, and the fact that they are characterized by either very few, but highly derived fossil
members like the Protopithecus and Caipora in the
atelid lineage, or fossils of less certain affinities with no
preseserved postcranial elements, as in the callitrichine
lineage, leaves little to discuss.
The Callitrichinae stand out because there are comparably few field studies on the locomotion and postures of
several extant genera, such as Leontopithecus, Mico,
Callibella, and Callithrix. Because of their derived postcrania (Ford, 1988; Davis, 2002; Ford and Davis, 2009),
these genera are expected to be rather specialized in
their positional behavior, but recent studies have shown
significant plasticity in other marmosets (e.g., Porter
and Garber, 2004; Youlatos, 2009). The diversity of adaptations in these forms could be equivalent to that
observed in Saguinus (e.g., Garber, 1992, 2007).
In contrast, the Atelidae seem to have been oversampled in the wild. Alouatta, the most basal member of
the group is relatively well known. Some species have
been well studied in a variety of habitats and do show
some diversity around a well-established locomotor pattern characterized by quadrupedal walking, clambering,
climbing, and tail-hind limb suspension. However, as
Alouatta is one of the few platyrrhines that is so widespread across the Americas, from dry tropical forests in
southern Mexico to temperate forests in northern Argentina, more studies are required to understand the potential behavioral flexibility of this platyrrhine. Only Cebus
shows a similar degree of adaptive plasticity. Further
studies will also shed light on the adaptive significance
of tail-assisted-hind limb suspension in relation to
diverse micro-habitat parameters. Two of the more
derived members of the group, Ateles and Lagothrix, are
now well known from the field, but the lack of systematic quatitative data for Brachyteles, as a tail-arm bra-
2009
chiating folivore/frugivore inhabiting the Mata Atlantica
of southeastern Brazil, leaves a void in the reconstruction of the evolution of suspensory behavior and its relation to frugivory and energy maximization within this
large-bodied clade. Nevertheless, field data on the locomotor ecology of more Ateles species are still required, in
order to obtain a complete image of the adaptive significance of tail-forelimb suspension in atelid evolution.
We are far from completing the evolutionary history of
platyrrhines. The recovery of new and more complete
fossils is enriching the paleontological record, while
additional field studies are adding to an understanding
of the adaptive significance and general plasticity of
locomotor and postural diversity of extant taxa. The
growing platyrrhine postcranial fossil record has
witnessed significant additions since last reviewed by
Meldrum (1993). Novel hypotheses synthesizing the
framework of platyrrhine origins and phylogenetic diversification have been proposed in recent years, focusing
discussions on both morphologies and methodologies.
Hopefully these will lead to clarification of the nature of
the proto-platyrrhine immigration to the Western Hemisphere and subsequent pattern of platyrrhine diversification. Although the evolution of locomotor diversity
offers many insights into the adative radiation among
platyrrhines, it offers no definitive resolution to competing hypotheses of platyrrhine phylogeny.
ACKNOWLEDGEMENTS
The authors are particularly grateful to Alfie Rosenberger, who invited them to participate in this project.
His continuous encouragement and editorial guidance
helped us complete this review, which likewise rests
upon the contributions of mentors, colleagues, museum
curartors, and funders, too numerous to mention singly.
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