THE ANATOMICAL RECORD 294:1991–2012 (2011)

Locomotor Diversification in New World Monkeys: Running, Climbing, or Clawing Along Evolutionary Branches

1 2 DIONISIOS YOULATOS * AND JEFF MELDRUM 1Department of Zoology, Aristotle University of Thessaloniki, School of Biology, Thessaloniki, Greece 2Department 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 neonto- logical data for postcranial morphology and ecological adaptation. Fossil platyrrhines are notably diverse, from the Oligocene Branisella, to the varied Patagonian early quadurpedal-leaping and quadrupedal- climbing 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 con- vergent 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 loco- motor specializations for climbing-suspension; small-bodied species exhib- iting adaptations for claw climbing and leaping. This behavior-based spectrum of locomotor diversification is similarly evident in a morphol- ogy-based pattern, that is, that produced by the shape of the talus. The implications of the record of platyrrhine postcranial evolution for the com- peting hypotheses of platyrrhine phylogenetic patterns, the ‘‘long lineage hypothesis’’ and the ‘‘stem platyrrhine hypothesis,’’ are considered. Anat Rec, 294:1991–2012, 2011. VC 2011 Wiley Periodicals, Inc.

Key words: platyrrhines; locomotion; evolution; fossils; talus

New World Monkeys (NWMs) are a diverse radiation NWMs are most likely monophyletic, a conclusion that of anthropoid that currently occupy a wide has received support from molecular studies, such as range of habitats spanning the American continents, transposable Alu elements (Singer et al., 2003). from southern Mexico to Northern Argentina. They rep- resent almost 1/3 of all living primates, with several extant species discovered and identified quite recently Grant sponsor: Aristotle University of Thessaloniki. and others differentiated through more profound taxo- *Correspondence to: Dionisios Youlatos, Aristotle University nomic analyses (see Rosenberger et al., 2009). The pres- of Thessaloniki, School of Biology, Department of Zoology, GR- ent day diversity of NWMs is generally held to be the 54124 Thessaloniki, Greece. Fax: þ302310998269. result of a single colonization by a group of primitive E-mail: [email protected] anthropoids, which rafted over the Paleogene Atlantic Received 15 September 2011; Accepted 16 September 2011 Ocean from Western Africa aided by paleowinds and cur- DOI 10.1002/ar.21508 rents (Ciochon and Chiarelli, 1980; Hoffstetter, 1980; Published online 1 November 2011 in Wiley Online Library Fleagle, 1999; Houle, 1999). If this scenario holds true, (wileyonlinelibrary.com).

VC 2011 WILEY PERIODICALS, INC. 1992 YOULATOS AND MELDRUM Alternately, multiple colonization lineages, or events, Pitheciids are medium-sized forest canopy dwellers, would have resulted in paraphyly in NWMs, as sug- which move mainly quadrupedally, on intermediate gested by the analysis of antigenic determinants from length limbs, with variable rates of suspension (espe- selected serum proteins (Bauer and Schreiber, 1997). In cially hindlimb suspension) and leaping, and feed on either case, the timing of this event, or events, remains hard or unripe fruit, as well as seeds, insects and leaves uncertain, but likely occurred sometime before the late (Kinzey, 1992). Cebines are medium-sized dwellers of Eocene, earlier than 37 Ma (Houle, 1999; Kay et al., many forest types and all forest strata, which forage 2004; Seiffert et al., 2004). To survive the transoceanic both on fruit and invertebrate and vertebrate prey via journey, protoplatyrrhines were likely preadapted to more active and manipulative behaviors, moving along strong seasonal variations in water availability in their with quadrupedalism and leaping (Janson and Boinski, original (African) environment (Houle, 1999). South 1992). Callitrichines are small, mainly predacious dwell- America of that time was characterized by a cooler, sea- ers of diverse forest types and strata, which base their sonal climate, and dominated by a mixture of forests diets on arthropods and gums using quadrupedalism, and vast open grasslands (MacFadden, 2000). This leaping and clawed scansorial locomotion in variable diverse habitat undoubtedly played a significant role in degrees (Garber, 1992). Finally, atelids are the largest platyrrhine diversification and dispersal. NWMs dwelling in the upper canopy layers, depend Modern platyrrhines occupy diverse habitats such as mainly on fruit and leaves and employ more climb/clam- the forests of the great Amazonian basin, the semide- bering and suspensory patterns of locomotion, on rela- ciduous Atlantic forests, and the drier savannas, grass- tively lengthened limbs, via the aid of their prehensile lands, or shrub lands that exist either within extensive tails (Rosenberger and Strier, 1989; Strier, 1992). forested areas (e.g., Guyanan savannas) or on the The successful exploitation of these divergent niches fringes of great forests (e.g., Venezuelan llanos). The ex- requires positional behaviors that enable food foraging, ploitation of such varied habitats has resulted in dis- manipulation, and ingestion, access to potential mates tinct morphological, ecological and behavioral and escape from potential predators (see e.g., Garber, adaptations, which are broadly correlated to specific 2007). Therefore, the study of locomotion is fun- phylogenetic groups (Ford and Davis, 1992; Rose- damental to understanding their adaptive diversity. The nberger, 1992; Fleagle and Reed, 1996, 1999; Youlatos, objective of this review is to summarize locomotor pat- 2004; Rosenberger et al., 2009). The depth of these terns for both fossil and modern NWMs, deciphering cor- lneages is still debated. Rosenberger et al. (2009) and related patterns of adaptive radiation. While the fossil Rosenberger (2010) advocate the ‘‘long lineage hypothe- record of NWMs, especially with regard to postcranial sis’’ (LLH) that modern NWMs are characterized by a remains, is relatively scarce, growing interest in the extant taxa of NWMs over the past decades has yielded number of long-lived clades and the sufficiently known detailed numerous quantitative reports of their anatomy fossil taxa are actually early affiliates of these. The and positional behavior. A lack of significant contribu- interpretation of some divergence date estimates, based tions for certain groups, past and present, is evident, as on molecular clock data, appear to support the LLH well as the aforementioned lack of concensus on phyloge- (e.g., Schneider et al., 2001; Opazo et al., 2006; netic relationships between fossil and modern taxa. By Schrago, 2007). In contrast, Kay et al. (2008) and Kay bringing together this information now, we hope to stim- and Fleagle (2010) propose the ‘‘stem platyrrhine hy- ulate the recovery of more fossils, compell additional pothesis,’’ concluding that most early Patagonian fossils study of the diverse moderns, and provide a fresh frame- bear no relationships to particular modern clades. work for asking questions. 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 OLDEST PLATYRRHINES latest in a series of radiations. Kay and Fleagle (2010) Branisella point out that different methodologies produce varying The oldest records of NWMs in the Americas are Bra- results from the same data, that is Opazo et al. (2006), nisella boliviana and Szalatavus attricuspis from the and that alternate divergence times lend support to the late Oligocene, more precisely the Deseadan South stem playrrhine hypothesis. American Land Age (SALMA) 26 Ma (Rose- Modern platyrrhines form groups with rather evident nberger et al., 1991c; Fleagle, 1999; Tejedor, 2008; Rose- and distinct adaptations that have been well-studied nberger et al., 2009). These earliest undoubted New behaviorally (e.g., Garber, 1992; Janson and Boinski, World anthropoid fossils consist mainly of dental and 1992; Kinzey, 1992; Rosenberger, 1992; Strier, 1992) and fragmentary mandibular and cranial elements that have morphologically (e.g., Erikson, 1963; Hershkovitz, 1977; been unearthed from the locality of Salla, Bolivia (Takai Fleagle and Meldrum, 1988; Ford and Davis, 2009). In and Anaya, 1996; Takai et al., 2000). The phylogenetic this article we will adhere to the revised phylogeny of relations of Branisella and Szalatavus are still debated. Kay et al. (2008), that is the Pitheciidae consist of the Some authors, based on specific dental characters, sug- Pitheciinae (Cacajao, Pithecia, Chiropotes) and Callice- gest that the latter may be a junior synonym of the for- bus; the Cebidae consist of the Cebinae ([Cebus, Saimiri] mer and that they are both related to the rather derived and Aotus} and the Callitrichinae; the Atelidae are modern callitrichines (Takai et al., 2000). Alternatively, Alouatta, Ateles, Barchyteles, and Lagothrix. This is not these early forms are considered to bear no differential to say that alternate phylogenies are without merit. affiliation to particular modern NWMs and do not estab- However, the subtleties of distinctions are beyond the lish the morphology of the modern platyrrhine morpho- scope of this review of postcranial and locomotor type (Fleagle and Tejedor, 2002). Branisella is 10 diversification. million years younger than the estimated age of invasion LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES 1993 of proto-platyrrhines to South America (Kay et al., 2004, Meldrum, 1993). A generalized positional pattern such 2008). This gap is vexing since caviomorph rodents, as this would have enabled the medium-sized Dolichoce- which are considered likely coimmigrants with platyr- bus (1,500 g: Kay et al., 2008) to exploit a particularly rhines, have been unearthed in earlier strata (e.g., diversified seasonal mosaic habitat, which may have McFadden, 1990; Rosenberger et al., 2009). typified the southern cone of South America during this No postcranial fossils attributed to Branisella have period (Rosenberger et al., 2009). been recovered, providing no direct evidence of their Southwards, the Pinturas Formation in the northwest adaptations for positional behaviors. However, one of the of Santa Cruz Province, Argentina, has yielded a rela- most notable features of the dentition of Branisella is tively diverse collection of fossil NWMs (Fleagle and the high-crowned lower teeth and the heavy wear of Tejedor, 2002; Tejedor, 2008). They date from the early their cusps that may indicate a diet of very abrasive Santacrucian SALMA with an age estimate of 17.5–16.5 food, such as silica-rich leaves or grasses (Takai et al., Ma (Fleagle and Tejedor, 2002; Rosenberger et al., 2009). 2000; Kay et al., 2001). On this basis some have inferred Two genera are described, Soriacebus and Carlocebus, a significant commitment to terrestriality, or at least an which both include referred postcranial elements (Table understory habit in relatively open woodland where den- 1). Their morphology has provoked interesting debates tal resistance to abrasives would have been an impor- over the phylogeny of early platyrrhines. tant selective factor. The paleo environment of Salla is described as semiarid, where mainly high-crowned non- primate mammalian grazers roamed (McFadden, 1990). Soriacebus This might suit the profile of proto-platyrrhines as sug- gested by Houle (1999), that is, adapted to strong sea- Soriacebus, with an estimated body weight of 1,800 g, sonal variations in water availability in their original is characterized by an anterior dentition and a deep (African) environment. However, given the small body mandibular ramus, which resemble those of living Pithe- size of 1,000 g, it is unlikely that terrestrial specializa- ciinae. It was initially described as having resemblances tions played a significant role in the positional behavior to Callitrichinae and Pitheciinae (Luchterhand et al., of Branisella. Any further inferences about its positional 1986) and then argued to be an early member of the lat- behavior, in the absence of postcranial fossils, must ter group (Rosenberger et al., 1990; Rosenberger, 1992; remain highly speculative. Tejedor, 2000, 2008). However, its posterior teeth are dis- tinct and other studies again called into question pithe- THE SOUTHERN CONE: AN EARLY ciine affinities, and supported the placement of this RADIATION? genus with others in a stem platyrrhine group including Dolichocebus (Kay, 1990; Kay et al., 2008; Kay and Flea- Dolichocebus gle, 2010) among others. The oldest NWM fossil with referred postcranial ele- The single talus (Fig. 2) attributed to S. amenghino- ments is Dolichocebus gaimanensis from the Sarmiento rum most resembles those of Pithecia and Alouatta (Mel- formation, Chubut Province, Argentina (Table 1). The drum, 1990). Functionally, the low, broad, and fossil, known from an almost complete but badly crushed moderately wedged trochlea and the short neck partly cranium, several isolated teeth, mandibular fragments covered by a distal extension of the trochlea all indicate and a talus, dates from the early Miocene, Colhuehua- extensive talocrural movements in multiple planes pian SALMA at 20 Ma (Meldrum, 1990; Fleagle and (Ford, 1988, 1990a; Meldrum, 1990). Therefore, this mor- Tejedor, 2002; Kay et al., 2008). The phylogenetic affin- phology would be suggestive of arboreal quadrupedal ities of this species have given rise to very divergent activities with frequent climbing/leaping and even sus- views reflecting differing interpretations of platyrrhine pensory activities, similar to extant Pithecia (Fleagle evolutionary radiations (Kay et al., 2008; Kay and Flea- and Meldrum, 1988). This repertoire also correlates with gle, 2010; Rosenberger, 2010). One view, based mainly body size and the reconstructed diet, which is frugivory, on a number of apparent cranial and postcranial synapo- likely specializing on unripe and woody fruit, but with- morphies, argues that the fossil is an early member of out any specialized seed-predator behavior (Rosenberger, the lineage leading to modern Saimiri (Reeser, 1984; 1992; Meldrum and Kay, 1997b; Rosenberger et al., Gebo and Simons, 1987; Rosenberger, 1992; Tejedor, 2009). Whether the similarities in talar morphology 2008; Rosenberger et al., 2009; Rosenberger, 2010). An between S. ameghinorum and pitheciines indicate phylo- alternative view, relying most recently on a large cranio- genetic affinity or homoplasy, as with aspects of the den- dental parsimony analysis, characterizes this fossil and tition, remains uncertain. several others (see below), as stem platyrrhines, as A smaller species of this genus, S. adrianae, has an noted above (Meldrum, 1993; Kay et al., 2008; Hodgson estimated body weight of 800–900 g (Fleagle, 1990). et al., 2009; Kay and Fleagle, 2010). Younger than S. ameghinorum, it differs only in a few The sole postcranial element that has been attributed subtle dental traits. A partial calcaneus was recovered to D. gaimanensis is a well-preserved talus (Fig. 1) from a locality rich in dental remains of S. adrianae and which appears to bear the closest morphological affinity is of appropriate size to be provisionally allocated to this to Saimiri, Cebus, and Callicebus but looks remarkably species (Meldrum, 1993). The fossil preserves a very nar- primitive in its lack of most conspicuous platyrrhine fea- row anterior calcaneal facet that stops short of the distal tures (Reeser, 1984; Gebo and Simons, 1987; Ford, end of the calcaneus. This condition has been associated 1990a; Meldrum, 1990). Its morphology indicates a gen- with an alternating tarsus possessing limited mobility, eralized function with a preponderance of frequent arbo- especially in eversion and plantarflexion (Dagosto, real quadrupedal activities, and specializations for 1988), likely associated with more quadrupedal and increased leaping (Gebo and Simons, 1987; Ford, 1990a; clinging postures. 1994

TABLE 1. Fossil New World monkeys with known postcranial remains Postcranial positional Fossil Age Locality elements BW (g) behavior Dolichocebus 20.0 Ma Sarmiento, Chubut, Argentina A 1,500 AQW, L Carlocebus 17.5–16.5 Ma Pinturas, Santa Cruz, Argentina A, S, U 2,500 AQW, CL Soriacebus 17.5–16.5 Ma Pinturas, Santa Cruz, Argentina A 1,800 AQW, CL Rio Cisnes talus 16.5 Ma Alto Rio Cisnes, Chile A ? AQW, L Homunculus 16.4 Ma Santa Cruz, Santa Cruz, Argentina H, U, R, F 2,700 AQW, L Paralouatta marianae 14.7–18.5 Ma Domo de Zaza, Lagunitas, Cuba A ? AQW Proteropithecia 15.8 Ma Colon Cura, Neuquen, Argentina A 1,500 AQW, L MELDRUM AND YOULATOS 13.5-11.8 Ma , Madgalena Valley, Colombia A 2,000 AQW, L 13.5–11.8 Ma La Venta, Madgalena Valley, Colombia S, H, R, U, Mc, V, P, C, 2,200 AQW, L F, T, Fi, A, Ca, Ta, Mt 13.5–11.8 Ma La Venta, Madgalena Valley, Colombia A 1,000 AQW Laventiana 13.5-11.8 Ma La Venta, Madgalena Valley, Colombia A 850 AQW, L Neosaimiri 13.5–11.8 Ma La Venta, Madgalena Valley, Colombia H, U, F, T, A, C 850 AQW, L Caipora 20 Ka Toca de Boa Vosta, Bahia, Brazil H, R, U, Mc, C, F, T, Fi, 20,000 CL, SUS A, Ca, Ta, Mt Protopithecus 20 Ka Minas Gerais, Brazil H, U, F, A, Ca, Ta 25,000 CL, SUS Toca de Boa Vosta, Bahia, Brazil Paralouatta varonai Holocene Cueva del mono fosil, Cueva alta, Cuba H, C, F, A 10,000 ATQW Xenothrix 6.7 Ka Long Mile Cave, Jamaica H, U, C, F 2,000–5,000 CL, SUS Skeleton cave, Jamaica Antillothrix 3.5 Ka Several sites on Hispaniola U, F, T 2,000–5,000 AQW, CL Abbreviations are used for postcranial elements (A: talus, C: os coxae, Ca: calcaneus, F: femur, Fi: fibula, H: humerus, MC: metacarpals, MT: metatarsals, P: pha- langes, 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). LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES 1995

Fig. 1. Left talus (MACN-CH 362) attributed to Dolichocebus gaimanensis, as seen in dorsal (A), proxi- mal (B), medial (C), plantar (D), distal (E), and lateral views (F). Scale bar equals 0.5 cm.

Carlocebus similarities to the Callicebus clade (Fleagle and Tejedor, The other NWM from Pinturas is the larger (2,600 2002; Tejedor, 2008). Alternately, such morphology could g) Carlocebus. Adaptively, the shearing crests of its be considered homoplasic or primitive and it is possible molars suggest frugivorous habits (Fleagle and Tejedor, that the genus also belongs to an earlier platyrrhine 2002). The genus is quite different from Soriacebus, and radiation, more closely related to Dolichocebus (Kay the more generalized morphology of its teeth suggest et al., 2008; Rosenberger, 2010). 1996 YOULATOS AND MELDRUM verging proximally. There was apparently a strong distal tibiofibular syndesmosis extending 15 mm along the dis- tal tibial shaft, indicating a more stable talocrural joint associated with rapid quadrupedal running and/or leap- ing. 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 combina- tion 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 addi- tion, 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 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 unas- signed and dates to the Friasian SALMA 16.4 Ma Fig. 2. Tali of Pinturas primates. A–D: Referred to Carlocebus cf. (Tejedor, 2003, 2008—Table 1). Generally, the talus bears carmenensis. E referred to Soriacebus ameghinorum. 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 Postcranially, Carlocebus is known from four well- high talar body with the parallel-sided rims, the rela- preserved tali (Fig. 2) (Meldrum, 1990), distal tibia and tively long neck, and the morphology of the tibial stops partial calcaneus (Meldrum, 1993) and a fragmentary and that of the proximal and distal calcaneal facets indi- scapula and ulna (Anapol and Fleagle, 1988). None of cate predominantly arboreal quadrupedal behavior with this material has direct association with craniodental associated leaping (Gebo and Simons, 1987; Meldrum, specimens. The general morphoplogy of the tali approxi- 1990). The relationship between the fauna of this site mates that of Callitrichinae and small Cebinae. More and Santacrucian faunas is not yet well understood precisely, they share a moderately low and broad troch- (Tejedor, 2003). If the evidence confirms that the fauna lea, a very broad, slightly medially directed talar neck, from Rio Cisnes is closer in age to the Santacrucian an oval head in distal view, and a broad shallow poste- fauna, then the platyrrhine radiation would have been rior calcaneal facet, while the dorsal surface of the troch- more extensive during that period than previously lea extends onto the talar neck to form a very deep recognized. cavity for the tibia. These features rather suggest a mix- ture of quadrupedal activities with some moderate leap- Homuncuclus ing behavior probably from vertical postures (Meldrum, 1990). In addition, this repertoire could have been sup- South of the Pinturas site, another fossil platyrrhine plemented by relatively ample and varied talocrural has been unearthed from several sites (Rio Gallegos, movements, frequently associated with clambering. Corrigu¨ en Aike, Monte Observacion) of Santacrucian An isolated distal fragment of a tibia articulates con- age, 16.4 Ma (Tejedor and Rosenberger, 2008). Homun- formably with the aforementioned tali. The shaft is simi- culus patagonicus is a medium-sized NWM (2,700 g) lar in robusticty to Homunculus. It broadens due to an known from partial skulls, mandibular fragments, teeth, expansion of the distolateral border, supporting a broad and long bones (Bluntschli, 1913, 1931; Meldrum, 1993; fibular incisure bounded by well-developed crests con- 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, sive areas of savannas (Bown and Fleagle, 1993; Fleagle and would thus suggest phylogenetic relationships and Tejedor, 2002; Tejedor and Rosenberger, 2008; Rose- within the clade of Cebidae or Pitheciidae (Fleagle and nberger et al, 2009). Tejedor, 2002; Tejedor and Rosenberger, 2008). The den- Limb proportions of Homunculus are similar to mod- tition is rather primitive (Tejedor, 1997, 2008) and the ern quadrupedal platyrrhines, such as Aotus and Calli- more advanced morphologies seen in Proteropithecia and cebus (Meldrum, 1993; Tejedor and Rosenberger, 2008). later Pitheciinae (e.g., Nuciruptor, Cebupithecia) could The humerus displays a number of features that suggest have evolved out of a Homunculus-like dentition (Tejedor climbing behavior, in agreement with the proportion- and Rosenberger, 2008). Functionally, the incisors and ately robust curved radius (Fig. 3). The capitulum is premolars indicate hard-fruit eating, while the relatively spherical and quite ‘‘unrolled’’ relative to the long axis of large cheek teeth suggest an important component of the humeral shaft, providing a greater range of flexion hard fruits and leaves in its diet (Fleagle and Tejedor, and extension (Napier and Davis, 1959; Meldrum et al., 2002; Tejedor and Rosenberger, 2008; Rosenberger et al., 1990). The lateral epicondyle is relatively large (Ford, 2009). A varied diet probably suits the reconstruction of 1990a), the trochlea is cylindrical and the medial epicon- the paleoenvironments as seasonal habitat with more dyle has little dorsal angle (Fleagle and Meldrum, 1988). marginal conditions than a tropical forest, probably In the robust femur, the great degree of extension of resembling the gallery forests along rivers with exten- the femoral head and the distally placed fovea are both 1998 YOULATOS AND MELDRUM features of habitually adducted hindlimbs. The greater facets and its size falls within the expected range of this trochanter is very broad and rugous and overhangs the form. Although, allocation of this specimen is not yet set- femoral shaft anteriorly, providing expanded attachment tled, the relatively narrow head and neck and the more of the vastus lateralis muscle, an extensor of the knee. rounded lateral rim of the trochlea would be suggestive The ridge of bone on the posterior surface of the proxi- of talocrural movements along the sagittal plane, usually mal femoral neck, and the particularly deep patellar associated with quadrupedal activities with some leaping groove, seem to promote rapid for-aft movements of the behaviors (Ford, 1988, 1990a; Meldrum and Kay, 1997). thigh, necessary during leaping activities (Ford, 1988, 1990a; Meldrum, 1993). Therefore, this medium-sized monkey exhibited a mosaic of locomotor behavior that Cebupithecia included quadrupedal walking and leaping, combined with forelimb-assisted climbing. Another fossil member of the Pitheciinae, which is well represented in La Venta, is Cebupithecia sarmien- toi. In effect, Cebupithecia, a medium-sized monkey Proteropithecia (1,800 g), is one of the most complete fossil platyr- In northwest Patagonia, in the Province of Neuquen, rhines ever found other than the subfossils from the the Collon Cura formation has yielded Proteropithecia Caribbean and eastern Brazil, with associated cranial, neuquenensis, a medium-sized (1,600 g) platyrrhine mandibular, dental remains, as well as a partial skelton known from isolated teeth and a talus (Kay et al., 1998). (Fig. 4; Stirton, 1951; Stirton and Savage, 1951; Davis, The site is considerably younger, dating from 15.8 Ma, 1987; Meldrum and Kay, 1990; Meldrum and Lemelin, and the associated fauna is slightly different from the 1991; Meldrum, 1993; Hartwig and Meldrum, 2002). The above mentioned Santacrucian, probably from the Col- dentition is clearly synapomorphic with the living Pithe- loncuran SALMA (South American Land Mammal Age). ciinae, displaying procumbent upper incisors, large pro- The compressed and procumbent lower incisors and the jecting canines that are triangular in cross-section, and shallow basins and crenulated enamel of the low- quadrate molars with poorly developed cusps and crests. crowned molars indicate strong affinities with Pithecii- On the other hand, premolars appear to be less special- nae, and Proteropithecia is considered as a basal mem- ized than in modern forms, and finally the bunodonty ber of the group. Adaptively, Proteropithecia has a molar and shallow hypoflexids and raised talonids appear even structure consistent with fruit- or nut-eating, while its more primitive (Meldrum and Kay, 1997). Thus, Cebupi- incisors rather suggest seed-eating in much the same thecia appears to be more derived than Nuciruptor in manner as extant pitheciins. the direction of living Pitheciinae, with specializations The talus shows overall resemblances to Aotus and for opening hard fruit and seed predation. Its cheek Callicebus. In general, the oval head, the moderate teeth were also able to masticate hard seeds in a similar neck, the shallow, narrow, and well-delineated dorsal tib- manner to extant pitheciins (Meldrum and Kay, 1997). ial stop, the high and moderately wedged trochlea, and Postcranially, Cebupithecia appears to lack most apo- the extended anterior proximal calcaneal facet are fea- morphic traits of modern Pitheciinae (Fleagle and Mel- tures that are frequently associated with relative stabil- drum, 1988; Ford, 1990a; Hartwig and Meldrum, 2002). ity and enhanced movements to the sagittal plane (Ford, Its limb proportions fall within the range of monkeys 1988; Meldrum, 1990). Similar functions usually occur that are mainly quadrupedal and use moderate amounts during arboreal quadrupedal activities and moderate of leaping, such as the cebines and Callicebus (Meldrum leaping activities (Kay et al., 1998). 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 Nuciruptor biccipital groove. These features are frequently associ- The La Venta region in the Magdalena Valley, Colom- ated with controlled movements at the sagittal plane as bia, is the richest fossiliferous Cenozoic localitiy in during quadrupedal activities (Ford, 1988; Meldrum northern South America. From that region, Nuciruptor et al., 1990). The femur shows a marked posterior ridge rubricae is a medium-sized (2,000 g) fossil monkey that at the femoral neck and the head extends on the supe- is represented by a mandible and associated teeth (Mel- rior part of the neck, while the trochlea is high and well drum and Kay, 1997), and possibly a referable isolated demarcated, features that are usually associated with talus. The age of the fossil is estimated at 13.5–11.8 leaping habits (Davis, 1987; Ford, 1990a; Meldrum, Ma. The morphology of the mandibular corpus and the 1993). The distal tibia shows a markedly concave troch- procumbent and moderately elongate lower incisors and lear surface coupled with large inferior projections of the low-crowned molar indicate that it is more derived than anterior and posterior trochlear margin. These traits are Callicebus but more primitive than extant and most associated with a strongly curved and deeply grooved other extinct pitheciines (Meldrum and Kay, 1997). It astragalar trochlea with sharp medial and lateral crests appears to exhibit precisely those intial adaptations of and a distal deep extension on the talar neck. They sug- the dentition predicted for the earliest Pitheciinae, that gest a relatively stable ankle joint adapted for quick is incisors specialized for opening hard fruit and cheek pivots as during leaping (Ford, 1990a). Therefore, Cebu- teeth able to masticate hard seeds (Kinzey, 1992; Mel- pithecia appears to have been a medium-sized quadrupe- drum and Kay, 1997). dal monkey with increased rates of leaping behavior An isolated talus has been excavated in El Cardon (Hartwig and Meldrum, 2002), probably not as fre- Red Beds, a locality immediately adjacent to that of quently exhibited as in modern P. pithecia but more Nuciruptor. The talus is well preserved with superficial likely comparable with the other members of the erosion of the head, posterior tubercles and calcaneal subfamily. LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES 1999

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 Site QWR CL L S Pitheciinae Pithecia pithecia Lago Guri, Venezuela 25.6 21.8 52.6 _ Pithecia pithecia Raleighvallen-Voltzberg, Surinam 25 5 70 _ Pithecia monachus Yasuni, Ecuador 46.8 22.9 28.4 1.9 Chiropotes satanas Lago Guri, Venezuela 41.2 20.4 36.2 2.2 Chiropotes satanas Raleighvallen-Voltzberg, Surinam 80 2 18 _ Cacajao calvus Lake Teiu, Brazil 39.9 25.2 33.8 1.1 Callicebinae Callicebus cupreus Yasuni, Ecuador 54.1 26.7 17.7 1.5 Callicebus brunneus Manu, Peru 49.3 12.4 38.3 _ Callicebus torquatus Estacion Biologica Callicebus, Peru 66.9 9.2 23.9 _

Extant Pitheciinae frequently, but quadrupedal activities involving both walking, climbing, and clambering are more dominant Modern Pitheciinae exhibit a regular repertoire where (Walker and Ayres, 1996). This is also true for Chiropotes both quadrupedal activities and leaping behavior are the (Fleagle and Mittermeier, 1980; Walker and Ayres, 1996). dominant positional categories (Table 2). Among them, Study of the postcranial morphology of this genus has Pithecia appears to be the most saltatory, and more par- revealed functional traits that are associated with fre- ticularly P. pithecia, where almost half of its repertoire quent above branch quadrupedal walking and running, is represented by different forms of horizontal leaps and and some suspensory postures (Fleagle and Meldrum, hops (Fleagle and Mittermeier, 1980; Walker and Ayres, 1988). 1996). This is further evident in the postcranial mor- The other member of this family, Callicebus, which phology of the species, with functional traits that favor represents the basal member of this clade, is basically stability, restricted mobility to the sagittal plane and re- quadrupedal with variable, but generally moderate, sistance to high loads (Fleagle and Meldrum, 1988; rates of leaping behavior (Table 2—Youlatos, 1999; Law- Ford, 1988, 1990). In contrast, P. monachus seems to be ler et al., 2006). more quadrupedal (Youlatos, 1999), and this is reflected A noteworthy positional behavior of the larger Pithe- in its postcranial morphology as well (Meldrum and ciinae is hindlimb suspension, involving extreme plan- Lemelin, 1991; Meldrum and Kay, 1997), underscoring tarflexion and inversion of the ankle, and bracing with the postcranial and positional flexibility of the genus the tail in Chiropotes (Fig. 5—Fleagle and Meldrum, (Walker, 1993). Cacajao also appears to use leaps rather 1988; Meldrum, 1998). This reflects the occasional 2000 YOULATOS AND MELDRUM in order to comprehend other trends of ecological mor- phology within this radiation.

ACTIVE FORAGERS The Miocene paleocommunity of La Venta also include several fossils representing the Cebinae, for which, how- ever, few postcranial remains are known. These include the well-represented genera Neosaimiri and Laventiana (Hartwig and Meldrum, 2002; Tejedor, 2008). In addi- tion, 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 Pith- eciidae (e.g., Ford, 1988; Rosenberger, 1992, 2010; Teje- dor, 2008).

Neosaimiri 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 denti- tion resembles closely Saimiri in the shape and propor- tions 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, pre- molars and the third molar stand out as either autapo- morphies, or synapomorphies with Cebus (Takai, 1994; Tejedor, 2008). Furthermore, Kay and Meldrum (1997) on the basis of dental and mandibular morphology advo- cated 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 Fig. 5. Chiropotes satanas demonstrating hind-limb suspension heavily built monkey than its modern relative. In addi- with tail bracing. tion, 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 climbing and suspensory behaviors reflected in the knee patellar groove, a smaller anterior process of the distal and ankle, and confirm their intermediate position tibia, an absence of a distal surface extension on the an- between the medium-sized generalized Cebinae and the terior tibial shaft, an absence of an anterior midtro- large-bodied suspensory Atelidae (Meldrum, 1990). Con- chlear depression of the talus, and a short distal sidering the reconstructed positional behavior of fossil calcaneus relative to the calcaneal tuberosity. This suite Pitheciinae with those behaviors for extant forms, we of distinguishing features indicates a dominant forelimb observe a consistent pattern of quadrupedal walking– in quadrupedal progression, a less stabilized upper ankle running–bounding behavior with some variable compo- joint, and a shorter power arm for plantar flexion. On nent of leaping and hopping activities. All fossil forms the basis of such functions, Neosaimiri would have been tend to exhibit a pattern resembling Callicebus and Chi- an arboreal quadruped employing frequent horizontal ropotes positional behaviors, quadrupedalism accompa- leaps across gaps in a forested environment. nied by some leaping. If Callicebus represents in some form the postcranial prototype of ancestral platyrrhines Laventiana in its positional behavior (Ford, 1988), then all these forms do not appear to have changed much since the Laventiana annectens is a taxon very closely related to inception of the pitheciine radiation. Within this radia- Saimiri (Rosenberger and Setoguchi, 1991) and is often tion, only Pithecia, and more particularly, P. pithecia (as considered as a junior synomym of Neosaimiri (Takai, there are limited data for other species), departs far 1994; Meldrum and Kay, 1997) or congener of Neosai- from this blueprint. Cacajao also differs, since it evolved miri (Kay and Meldrum, 1997). In La Venta, it is repre- in Amazonian flooded forests with quite discontinuous sented by a rather complete mandible (Rosenberger canopies (Walker and Ayres, 1996). Additional data on et al., 1991c), a talus (Gebo et al., 1990), and a distal the positional behavior of other pitheciins are required tibia (Meldrum, 1993). Its molars exhibit a buccal LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES 2001 nberger, 1987). It was represented originally by a mandi- ble, 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 com- pared 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 troch- lear 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; Mel- drum, 1993).

Extant Cebinae There is a strong bias in the study of positional behav- ior 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 noc- turnal. Anecdotal descriptions and predictions from post- cranial traits suggest a mainly quadrupedal primate with moderate leaping activities (Wright, 1989). This is also supported by postcranial similarities with Callice- bus (Ford, 1988), which exhibits such positional pat- terns. 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 Fig. 6. Distal tibia and talus of IGM 250436 (A) and IGM-KU 8803 variable rates of leaping behavior (Table 3). S. sciureus (B) referred to Laventianna annectens, compared with corresponding seems to be the more saltatorial of the studied species elements of Saimiri sciureus (C), Scale bar equals 1.0 mm. (Fleagle and Mitteremeier, 1980; Youlatos, 1999). S. boli- viensis also uses considerable leaping, but is mainly quadrupedal (Fontaine, 1990), while S. oerstedii exhibits cingulid and a distinct postentoconid notch, proposed as more frequent quadrupedalism than other species of a significant autapomorphy, but variably present in Neo- squirrel monkeys (Boinski, 1989). This positional profile saimiri and Saimiri. seems to agree with the predacious frugivory of squirrel The overall morphology of the talus is most similar to monkeys that range in many forest types exploiting all living Cebinae (Fig. 6). It bears a moderately long talar forest strata (e.g., Janson and Boinski, 1992; Rose- neck, a high and relatively short and wide talar body, nberger, 1992). However, these reported variations may and a narrow talar head (Gebo et al., 1990). The distal result from differing sampling methodologies or habitat tibia is also most similar to Saimiri. Of particular note differences. If both fossil relatives of Saimiri from the is the indication of a well-developed syndesmosis of the Miocene, Neosaimiri and Laventiana, are reconstructed distal tibiofibular joint. The posterior surface of the tibia as quadrupedal leapers, then they perhaps most approxi- is quite flat and the lateral border is marked by a pro- mate S. sciureus in positional patterns, and coinciden- nounced ridge, along which the fibula would be tally, the extant range of the latter covers the La Venta appressed, as in Saimiri and several other platyrrhines site in Colombia. Thus there appears to be no significant including Aotus, Callithrix, Cebuella, and Pithecia. Only changes in locomotor behavior since the Miocene within Saimiri commonly displays the distinctive combination this clade, as within the Aotus lineage. of mediolateral widening and posterior flattening of the Concerning Cebus, modern species appear to be rather distal tibial shaft (Meldrum, 1993). This morphology consistent in their patterns (Table 3). The four species appears to facilitate quadrupedal activities with high for which data are available indicate increased quadru- rates of leaping behavior within an arboreal context. pedal activities, coupled with variably significant rates of leaping and variably moderate climbing/clambering (Fleagle and Mittermeier, 1980; Gebo, 1992; Youlatos, Aotus 1998; 1999; Garber and Rehg, 1999; Wright, 2007; Aotus dindensis is relatively small-bodied (1,000 g) Bezanson, 2009). These behaviors seem to suit the and dates from 13.5 to 11.8 Ma (Setoguchi and Rose- 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 Site QWR CL L S Saimiri oerstedii Corcovado, Costa Rica 88.1 4.5 7.4 _ Saimiri sciureus Yasuni, Ecuador 45.1 24.2 25.4 5.3 Saimiri sciureus Raleighvallen-Voltzberg, Surinam 55 3 42 _ Saimiri boliviensis Monkey Jungle, U.S.A. 73 5 20 2 Cebus capucinus Santa Rosa, Costa Rica 55 26 15 4 Cebus capucinus La Suerte, Costa Rica 60.8 9.9 25.9 3.4 Cebus capucinus La Suerte, Costa Rica 78.1 13.2 5.0 3.7 Cebus albifrons Yasuni, Ecuador 48.5 17.7 27.3 6.5 Cebus apella Nouragues, French Guiana 33.9 29.2 23.6 13.3 Cebus apella Iwokrama, Guyana 53 12 26 9 Cebus apella Raleighvallen-Voltzberg, Surinam 84 5 10 1 Cebus olivaceus Nouragues, French Guiana 32.5 30.8 26.7 10.0 Cebus olivaceus Iwokrama, Guyana 50 11 32 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 Site QWR CL L CC Saguinus fuscicollis Catuaba, Brazil 38 6 38 18 Saguinus fuscicollis Rio Blanco, Peru 47.6 12.4 32.5 6.3 Saguinus tripartitus Yasuni, Ecuador 40.3 10.4 33.7 15.6 Saguinus labiatus Catuaba, Brazil 49 9 37 5 Saguinus geoffroyi Barro Colorado, Panama 43.3 7.4 41.5 7.7 Saguinus midas Nouragues, French Guiana 32.5 28.7 26.5 12.1 Saguinus midas Raleighvallen-Voltzberg, Surinam 76 _ 24 _ Saguinus mystax Rio Blanco, Peru 51.6 12.0 30.9 4.3 Saguinus mystax Padre Isla, Peru 61.5 6.3 27.4 4.8 Leontopithecus chrysomelas London Zoo, UK 51.3 0.9 31.9 15.9 Leontopithecus chrysomelas Edinburgh Zoo, UK 60.2 1.5 23.2 15.1 Leontopithecus rosalia Washington Zoo, USA 44 15 23 15 Callimico goeldii Catuaba, Brazil 18 4 62 16 Cebuella pygmaea Yasuni, Ecuador 27.1 5.8 24.4 42.7 Callithrix jacchus Rio de Janeiro, Brazil 32 13 23 32 agile and destructive omnivore which exploits all forest known solely from cranial, mandibular, and dental material strata, ground included, in a remarkable variety of habi- with no associated postcranial elements thus far recovered. tats, resulting in nearly one of the most expanded geo- graphical range among all NWMs (Janson and Boinski, 1992; Rosenberger, 1992). There are no pertinent fossils Extant Callitrichinae with associated postcranial elements in order to directly Neontological evidence of behavior and foraging pat- assess evolutionary trends within this clade. It is, how- terns suggest different evolutionary patterns within the ever, safe to infer that these medium-sized taxa have callitrichines. Molecular systematists, whose cladistic preserved a largely generalized positional behavior. 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 ge- ‘‘DWARVES AND CLAWS’’ nus intensively use quadrupedal walking and bounding Fossils such as , Patasola, ,and coupled with high rates of leaping, which basically con- Lagonomico, from the middle Miocene La Venta locality, sist of horizontal leaps between terminal branches (Ta- have been related to the callitrichine radiation, although ble 4; Garber, 1980, 1991; Garber and Preutz, 1995; debates about the exact phylogenetic relationships of some Youlatos, 1999; Garber and Leigh, 2001; Youlatos and of them (e.g., Mohanamico and Lagonomico) have not been Gasc, 2001). These positional patterns indicate that tam- fully resolved yet (Rosenberger et al., 1990; Kay, 1994; Kay arins still exploit the small-branch milieu to a great and Meldrum, 1997; Rosenberger, 2002; Tejedor, 2008). This degree while being one of the most ecologically general- radiation is characterized by shared derived features that ized of the large-branch feeders. Their lesser dependence are related to their small size and concern understory, on gums, by comparison with marmosets, is also correla- trunk, and ground use, large and vertical branch use, squir- tive with the generally low rates of claw-climbing and rel-like locomotion using laterally compressed claw-like clinging on large vertical supports (Table 4). nails, and dependence on exudates and arthropods (Ford, The callimico/marmoset radiation was the subject of a 1980; Garber, 1992; Garber et al., 1996). These forms are recent extensive study (Ford et al., 2009). Callimico is LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES 2003 very specialized postcranially, especially in the hind ecological features, particularly adapted to below-branch limbs and ankle joint, which are designed to facilitate suspensory behaviors made possible by such features as increased leaping by providing the necessary mechanical fully prehensile tails (e.g., Erikson, 1963; Rosenberger advantage and required stability for load resistance and Strier, 1989; Strier, 1992). Their early fossil record (Ford, 1988; Garber and Leigh, 2001; Davis, 2002; is relatively scant compared to other clades. The middle Garber et al.; 2005, 2009). Behaviorally, callimicos ex- Miocene from La Venta locality (13.5–11.8 Ma), hibit particularly high rates of leaping, most of which Colombia (Kay et al., 1987) is the earliest representative are vertical leaps (Garber et al.; 2005, 2009), while quad- of this clade, followed by the late Miocene Solimoea from rupedalism, climbing and clawed locomotion are used in Solimoes formation (9–6.8 Ma) Acre, Brazil (Kay and a lesser degree (Garber and Leigh, 2001). These patterns Cozzuol, 2006). There are no postcranial elements repre- appear to be ecologically associated with the exploitation senting these early atelid forms. In stark contrast, of the lower forest strata with abundant vertical sup- younger examples from the late Quaternary consist of ports, where they frequently forage for arthropods and two remarkably complete skeletons of Pleistocene atelids collect fruit and fungi (Porter and Garber, 2004). from Brazil: Protopithecus brasiliensis and Caipora bam- The marmosets, Cebuella and Callitrhix, are by far buiorum. Their age is 20,000 BP (see Rosenberger the most ecologically specialized callitrichines; they et al., 2009). exploit large vertical branches in relation to their tree gouging habits and year-round exudate feeding (Garber, Protopithecus 1992). This is complimented by their locomotor patterns and associated morphology (Table 4; Davis, 2002; Ford Protopithecus brasiliensis is the largest fossil NWM and Davis, 2009). Cebuella exhibits very high rates of (25,000 g) and was discovered in cave deposits in claw-climbing and clinging on large vertical supports as Minas Gerais and Toca da Boa Vista, Bahia (Hartwig well as frequent leaping, including high rates of vertical and Cartelle, 1996). The fossil is known by a virtually leaps (Youlatos, 1999, 2009). Unfortunately, there are no complete skull and skeleton and bears a unique mixture detailed data on the locomotion of Callithrix, apart from of traits, including several derived characters shared by a study in the Jardim Botanico of Rio de Janeiro, where all atelids. The skull shows many morphological similar- C. jacchus emphasized clawed locomotion, used similar ities to Alouatta that could be ulitmately related to the rates of quadrupedal walking and bounding, as well as presence of an enlarged hyoid bone, but it lacks the rather frequent leaps, of which a significant proportion usual specializations for folivory found in the dentition were short (Zaluar et al., 2010). of howler monkeys (Hartwig and Cartelle, 1996). On the other hand, Leontopithecus, is quite specialized Actually, it is very likely that Protopithecus was primar- in its own way, having evolved in the different forests of ily a frugivore unlike Alouatta, which is highly folivo- Mata Atlantica (e.g., Hershkovitz, 1977; Garber, 1992; rous (Rosenberger et al., 2009). Rosenberger et al., 2009): the long and slender upper The postcranial skeleton of Protopithecus is much forelimbs with especially elongated digits III and IV, the more robust than in other Atelidae, probably due to its claw-like nails, and the enlarged incisors indicate an ad- large size. It is most similar to the suspensory Atelinae ept manipulative forager for both non-mobile prey and (i.e., Ateles and Brachyteles), with traits indicatve of fruit, as well as seasonal dependence on exudates glean- ‘‘brachiating’’ adaptations (Hartwig and Cartelle, 1996), ing (Garber, 1992). Unfortunately, there are no data for as opposed to Alouatta, which is more quadrupedal. This Leontopithecus in the wild, but the few studies in zoos is evident in the high intermembral index, low and wide suggest reliance on quadrupedal activities coupled with humeral trochlea, short ulnar olecranon process, and the leaping behavior (Stafford et al., 1994; Karantanis, shape of the radial head (Hartwig and Cartelle, 1996). 2010). Similar positional patterns would facilitate and This combination of cranial vs postcranial features poses suit the intensive manipulative exploitation of the dis- a dilemma for determining its phylogentic relationships continuous canopy of all forest levels that lion tamarins within the family. Hartwig and Cartelle (1996) proposed generally exploit. that Protopithecus is the sister taxon to Alouatta, while These data indicate different positional strategies Fleagle (1999) argued that it is related to the Atelinae. across the different clades of the Callitrichinae. The Jones (2008) likewise proposed two possible outcomes, widespread combination of quadrupedalism and leaping based on character trends related to brachiation within suggests this as the pattern of the common ancestor of this group. In her view, if Protopithecus is the sister- the group, most likely shared by the other members of taxon of Alouatta, there was less change towards an the Cebidae. In effect, leaping behavior is present in all energy-maximizing strategy in the stem atelin lineage, callitrichine clades, but extensive use of vertical leaping the last common ancestor of atelins is less Ateles-like, is only common in Callimico and marmosets. Quadru- and the energy-maximizing strategy would have evolved pedalism is significantly reduced in Callimico and in parallel in the Protopithecus, Ateles, and Brachyteles Cebuella, most likely for different reasons. Finally, terminal lineages. In contrast, if Protopithecus is the sis- clawed climbing and clinging, although used in variable ter taxon of the Atelinae, there are many more parallel- rates across the subfamily, tends to be particularly isms along the individual evolutionary branches (Jones, important in Callitrhix and Cebuella, genera highly 2008). dependent on exudate feeding. Caipora HEAVY WEIGHT CLIMBERS Caipora bambuiorum is another large NWM (20,000 The members of the Atelidae are the largest NWMs g) recovered from Toca da Boa Vista, Bahia, and is rep- and share a set of unique morphological, behavioral and resented 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 Site QWR CL L S Alouatta caraya ENSC, Alegrete, Brazil 41.5 29.3 16.8 12.5 Alouatta caraya Estancia Casa Branca, Brazil 66.4 18.6 2.7 12.3 Alouatta paliatta La Suerte, Costa Rica 81.7 7.9 3.2 7.1 Alouatta paliatta La Pacifica, Costa Rica 47 37 4 13 Alouatta seniculus Raleighvallen-Voltzberg, Surinam 80 16 4 _ Alouatta seniculus Nouragues, French Guiana 37.3 43.9 2.8 16.0 Alouatta seniculus Yasuni, Ecuador 50.9 28.0 2.4 18.4 Alouatta seniculus Tiputini Biodiversity Station, Ecuador 30.1 57.6 1.7 10.6 Alouatta seniculus Fundo Pecuario Masaguaral, Venezuela 32.8 57.1 5.7 4.2 Ateles geoffroyi Barro Colorado, Panama 22.0 24.2 10.9 30.3 Ateles geoffroyi Barro Colorado. Panama 51.1 6.1 23.5 10.9 Ateles geoffroyi Tikal, Guatemala 52 19 1 29 Ateles paniscus Raleighvallen-Voltzberg, Surinam 25.4 17.0 4.2 47.2 Ateles paniscus Nouragues, French Guiana 20.1 28.1 2.6 43.0 Ateles belzebuth Yasuni, Ecuador 20.8 37.9 2.8 35.8 Lagothrix lagotricha Yasuni, Ecuador 28.9 44.5 3.9 22.7 Lagothrix lagotricha Colombia 41.8 38.8 10.8 8.6

(Cartelle and Hartwig, 1996). Caipora appears to be coupled with an array of major forelimb traits, indicate most similar to Ateles in cranial morphology, with a increased forelimb suspension similar to the well- large, rounded braincase and the quadrate, bunodont, described tail-arm brachiation of Ateles (Rosenberger low-cusped molars. and Strier, 1989; Strier, 1992; Jones, 2008); and, (b) per- The postcranium is very robust, probably due to its formance of suspended locomotion may be quite different large size, but the overall morphology is reminiscent of among the genera, as was documented by Cant et al. the suspensory Atelinae and exhibits brachiating loco- (2003) for Lagothrix and Ateles (see also Lockwood, motor adaptations (Cartelle and Hartwig, 1996). This is 1999). As the Atelinae evolved, they apparently became apparent in the high intermebral index, the large globu- larger in body mass and more suspensory in order to for- lar humeral head, the short olecranon process, the round age more efficiently and cover more distances in search radial head and its ulnar facet, and the overall morphol- of sparsely dispersed food sources (Erikson, 1963; Jones, ogy of the metacarpals and metatarsals (Cartelle and 2008). Tail-assited forelimb suspension is a remarkable Hartwig, 1996; Jones, 2008). It is still unknown how locomotor specialization that greatly facilitates canopy these fossil forms attained similar sizes in the Brazilian travel by these large platyrrhines. Ateles is considered forests, where they were recovered (Rosenberger et al., the sister taxon of Lagothrix and Brachyteles (Meireles 2009). The morphology of these recent fossil forms, et al., 1999; but see Collins, 2004), and apparently differ- which are so closely related to the modern taxa, are cer- entiated rapidly from the stem atelin group by pursuing tain to shed a bright light on the evolution of positional this forelimb-dominated suspensory locomotion and pos- behavior in Atelidae once the material is extensively tures (Table 5; Mittermeier, 1978; Cant, 1986; Fontaine, studied. 1990; Youlatos, 2002; Cant et al., 2001; 2003). Subtle dif- ferences in locomotion among the species of spider mon- Extant Atelidae keys do exist (e.g., A. paniscus is the most suspenory species while A. geoffroyi the least; Table 5), but it is dif- Alouatta encompasses the smallest, as well as some of ficult to assess any correlations with habitat or phyloge- the largest, species among the atelids. Howler monkeys netic/eco-morphological parameters (Youlatos, 2008). appear to have differentiated earlier than the other If Brachyteles and Lagothrix are indeed sister-taxa, it forms and their locomotion is characterized by a prepon- suggests that the Ateles-like forelimb-dominated suspen- derance of quadrupedalism. This involves both horizon- sory locomotion evolved in parallel in Brachyteles, in the tal or inclined quadrupedal walking and clambering, distinct Mata Atlantica, while Lagothrix assumed a dif- limited forelimb suspension, and especially tail-assisted ferent regime of frugivory-animalivory, coupled with a hindlimb suspension during feeding postures (Table 5; different locomotor profile involving relatively high rates Fleagle and Mittermeier, 1980; Scho¨n Ybarra and Scho¨n, of quadrupedalism and climbing/clambering activities 1987; Gebo, 1992; Bicca Marques and Calegaro Marques, (Table 5; Defler, 1999; Cant et al., 2001). This is also 1998; Youlatos and Gasc, 2001; Youlatos, 2004; Prates reflected in the postcranium of this genus, which differs and Bicca Marques, 2008; Bezanson, 2009; Guillot, significantly from that of more suspensory Ateles and 2009). Of the studied species, A. seniculus appears to be Brachyteles (Erikson, 1963; Jones, 2008). the one that exhibits more suspensory and much more clambering/climbing activities (Table 5). These distinc- tions may be related to the varied habitats that this ISLAND DISPERSALS wide-ranging species exploits. Currently there are no nonhuman primates living on The remaining three extant genera show a gradient of the Caribbean islands. However, at least four different increasing degrees of suspensory locomotion, with two genera have been unearthed from Pleistocene to Holo- caveats: (a) there are limited data on the positional cene strata of three different islands: Paralouatta from behavior of Brachyteles, although anecdotal observations Cuba, Antillothrix and Insulacebus from Hispaniola, and LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES 2005 Xenothrix from Jamaica (Cooke et al., 2011). The coloni- straight ulna with a narrow proximal sigmoid notch that zation of these islands by primates is potentially set does not flare laterally, the short-necked radius with a prior to the middle Miocene, due to a single talus appa- proximal biccipital tubrosity, the marked and relatively rently of that age from Cuba (see Iturralde Vinent and deep patella groove of the femur, the massive tibial MacPhee, 1999; MacPhee and Horovitz, 2002; Rose- medial malleolus with an extended distal fibular facet, nberger et al., 2009). Colonization would have taken the nonwedged talar trochlea and the short, straight place either via overwater dispersal, probably by rafting and relatively robust metapodials and phalanges (Mac- (Ford, 1986; 1990b) or over a large, short-lived land- Phee and Meldrum, 2006). bridge which connected mainland South America, Cuba, Hispaniola, Puerto Rico, and the Lesser Antilles (Itur- Xenothrix ralde Vinent and MacPhee, 1999). Whether there was a single primate colonization event (Horovitz and Mac- Xenothrix was a Pleistocene, medium to large-sized Phee, 1999; MacPhee and Horovitz, 2002), or multiple primate (2,000–5,000 g) known from several cranial, (Rosenberger; 2002; Rosenberger et al., 2011) remains dental and postcranial elements found in six different uncertain. In either case, these forms underwent re- caves in Jamaica. The relatively short length of the hu- markable specialization, leading to some rather unique merus, wide and shallow biccipital groove, comparably endemic forms for which the phylogenetic relationships broad and distolaterally extensive capitulum, and the remain contested. Some authors propose that all these moderately prominent trochlear lips indicate ample fossils form a monophyletic group which is the sister quadrupedal movements in an arboreal habitat (Mac- taxon of Callicebus (Horovitz and MacPhee, 1999; Mac- Phee and Fleagle, 1991; MacPhee and Meldrum, 2006). Phee and Horovitz, 2002), while others advocate a more Similar adaptations are also evident in the ulna, with a complex biogeography: a pitheciine or Aotus affinity for relatively short olecranon, a proximally wide sigmoid Xenothrix (Rosenberger, 1977; Tejedor, 2008), cebine facet and well-defined radial notch. In contrast, humeral affinities for Antillothrix (MacPhee and Woods, 1982; features such as the deep olecranon fossa and short, and Rosenberger et al, 2011), and alouattine associations for posteriorly directed medial epicondyle indicate more re- Paralouatta (Rivero and Arredondo, 1991; Rosenberger, stricted quadrupedal activities, but these can also be 2002). related to the relatively large size of the (Mac- Phee and Fleagle, 1991; MacPhee and Meldrum, 2006). In the femur, the size and conformation of the greater Paralouatta and lesser trochanters, the short, anteriorly convex dia- The earliest primate fossil in the Greater Antilles is physis, exceptionally robust shaft, large and anteropos- Paralouatta marianae from the Cuban Miocene (14.68– teriorly compressed distal epiphysis, shallow and wide 18.5 Ma) site of Doma de Zaza, known from a single ta- patellar groove, and asymmetry of the condyles indicate lus (MacPhee et al., 2003). The specimen is character- controlled movements in various planes, suggesting cau- ized by a nonwedged trochlea, a long, slightly deviated tious clambering activities (Ford, 1990a,b; MacPhee and neck, a large head, and wide and extended calcaneal fac- Fleagle, 1991; MacPhee and Meldrum, 2006). This is ets, suggesting mid-tarsal mobility that is usually associ- also consistent with tibial morphology with large and ated with arboreal quadrupedal habits (MacPhee and wide tibial plateau, prominence of the tibial tuberosity, Meldrum, 2006). The geological evidence, and the pres- and the depth of evident muscle scars that suggest ence of some marine fauna, indicates that the site lay powerful extension and flexion of the leg at the knee along the banks of the sea where several depositional (MacPhee and Fleagle, 1991). environments were present (MacPhee et al., 2003). Paralouatta varonai, from the Holocene of Cuba is the Antillothrix largest monkey (9,000–10,000 g) from the Antilles, as large as any living platyrrhine. It is known from a well- Antillothrix bernensis was a medium to large-sized preserved skull, several mandibles, isolated teeth and primate (2,000–5,000 g) recovered from several Pleisto- numerous postcranial elements (Horovitz and MacPhee, cene sites in Hispaniola. Two relatively complete skulls 1999; MacPhee and Horovitz, 2002; MacPhee and Mel- have been allocated to the species, as well as some teeth, drum, 2006). The skull exhibits a lack of cranial flexion, isolated postcranial fragments, and a partial skeleto, the face projects upward with somewhat large orbits, with its skull, presenting long bones, ribs, and vertebrae and the braincase is long and low, relatively large with (MacPhee and Horovitz, 2002; Tejedor, 2008; Rosen- strong temporal and nuchal crests (Horovitz and Mac- berger et al., 2011; Kay et al., 2011). Rosenberger (2002) Phee, 1999). The canine is very small and the cheek and Rosenberger et al. (2011) conclude affinities to teeth are crested and wear down in a conspicuously flat extant Cebinae. Others have proposed close relationship fashion, indicating thick enamel (Horovitz and MacPhee, to the Cuban Paralouatta, which together constitute the 1999; Rosenberger et al., 2009). sister group to Xenothrix (Horovitz and MacPhee, 1999; The suite of postcranial characters of Paralouatta is MacPhee and Horovitz, 2002). A second newly discov- not seen in other platyrrhines, but it exhibits intriguing ered skull has been interpreted as a stem platyrrhine, resemblences to certain so-called semiterrestrial Old unrelated to any of the living families of NWMs (Kay World monkeys. These traits favor limb movements rela- et al., 2011). tively restricted to the sagittal plane, some resistance to Several points of interest have been observed on the high reaction forces and overall stability of the joints. isolated postcranials. The tibia displays a central posi- Morphologies reflecting this in the fossil include the ret- tion for a rather deep fibular facet, anterior and poste- roflexed medial epicondyle, the narrow trochlea and the rior trochlear borders extending inferiorly equally, and a deep olecranon fossa in the humerus, the robust and narrowed medial malleolus, all of which are suggestive 2006 YOULATOS AND MELDRUM of sagittally oriented limb movements, that is, rapid ar- 2004). The essence of these behavioral reconstructions boreal quadrupedalism and leaping (Ford, 1986, 1990a; reflect the correlations of locomotor behavior of small to MacPhee and Meldrum, 2006). Kay et al. (2011) note an medium-sized platyrrhines (1,000 g) to substrate undescribed distal humerus fragment associated with grain and texture presented in the landmark work of teeth attributed to Antillothrix resembling that of a typi- Fleagle and Mittermeier (1980). cal platyrrhine arboreal quadruped. On the other hand, A Principal Components Analysis (PCA) of the log- recently described associated femur and ulna are ana- transformed percentages of the distinct locomotor modes tomically distinctive, suggesting quadrupedal and climb- (quadrupedalism, climb/clamber, leap, suspensory, and ing/clambering habits (Rosenberger et al., 2011). On the clawed locomotion) reveals an interesting pattern of loco- basis of cranial shape of one recently recovered skull, motor variation among extant platyrrhines (Fig. 7). others have proposed a locomotor pattern probably simi- Each axis contributed differentially to the separation of lar to modern Alouatta (Kay et al., 2011). the locomotor groups, particularly separating the more specialized forms along respective axes. Medium-sized ADAPTIVE RADIATIONS AND THE platyrrhines characterized by a mixture of quadrupedal- DIVERSIFICATION OF LOCOMOTOR ism and leaping are clustered around the intersection of the axes. This cluster includes Saimiri, Cebus and Calli- PATTERNS IN PLATYRRHINES cebus species. Large-bodied climbers/suspenders were The above review of the locomotor behaviors recon- separated from above-branch locomotors on Factor 1, structed for fossil platyrrhines and those of modern which accounted for 44.7% (Factor 1 loadings of 0.827 taxa, reveals a remarkable diversity among NWMs. This and 0.830, respectively). The large bodied folivore-fru- diversity appears to be differentially distributed among givores exhibit increased climbing and suspensory abil- well-defined divergent clades of extant genera, but with ities and can readily exlploit the high canopies of mainly possible examples of convergence in some fossil taxa. rich, as well as poorer, forests (Strier, 1992). On the Behaviorally, it can be interpreted in two ways: one con- other hand, the claw-climbing and leaping groups were cerns the postcranial adaptations correlated with body separated along Factor 2, which accounted for 29.1% of size and substrate grain, both relative and absolute, that explained variance, (loadings of 0.578 and 0.467, respec- promoted specific locomotor patterns within well-estab- tively). These are small-bodied insectivore-gummivores, lished lineages; the other concerns the way these using claw-climbing, clinging and vertical leaping in the locomotor patterns promote niche partitioning of food understories of diverse types of forested habitats resources within specific assemblages through space and (Garber, 1992). Some taxa, such as the Pitheciinae Chi- time. However, these two views are not mutually exclu- ropotes and Cacajao, and the Callitrichinae Saguinus sive (Rosenberger et al., 2009). Locomotion is one of the and Leontopithecus, overlap considerably with the cen- principal links between morphology, ecology, and phylog- tral cluster, reflecting the less specialized nature of their eny and has been shaped through microhabitat utiliza- locomotor repertoires. Even Alouatta tended towards the tion within specific contexts. central cluster of ‘‘generalists.’’ Assuming platyrrhine monophyly, we might ask what This grouping pattern is not entirely evident, as some was the original blueprint that gave rise to this notable sets of genera are quite dispersed on the plot, but this pattern of locomotor diversity encountered today among may be an artifact of the original data, which was com- the varied Central/South American habitats. On the ba- piled from many separate studies. Problems of compara- sis of a comprehensive analysis of the postcranium of bility across studies with differing localities and both extant and fossil platyrrhines, Ford (1988, 1990a) methodologies have been acknowledged repeatedly in concluded that the ancestral platyrrhine was a small to the past. These inconsistencies of particulars under- medium-sized (1,000 g) arboreal quadruped, which standably introduce variation that will not correlate emphasized quadrupedal running and walking, princi- closely with broader generalizations made here. How- pally on horizontal branches, and included a significant ever, a comprehensive analysis of a selected anatomical component of leaping in its locomotor repertoire. Ford region, the ankle (i.e., talus), which is frequently recov- proposed Aotus as the most useful living model on the ered in the platyrrhine fossil record, revealed a strik- basis of its postcranial traits. This is somehow ironic, in ingly similar pattern to the behavioral data (Meldrum, the sense that there are no detailed quantitative obser- 1990). This was based on eleven dimensions and a multi- vations, only anecdotal information on the locomotor variate analysis of the fundamental proportions of the repertoire of owl monkeys. On the other hand, the post- talus of 300 specimens of platyrrhine genera, excluding cranium of Callicebus is virtually equivalent to Aotus, only Brachyteles and Callimico. The pattern of variation and this genus, as well as Saimiri, manifests similar in this instance revealed four distinguishable groupings: locomotor behaviors: frequent above branch quadruped- a central cluster of small-to-medium-bodied Aotus, Calli- alism, substantial use of horizontal supports, and con- cebus, Saimiri, and finally Cebus, exhibiting quadrupe- siderable leaping in variable rates. The same holds true dal running and leaping; towards one pole, the small- for the closely related Cebus, which frequently employs bodied Callitrichinae, exhibiting claw-assisted scansorial similar locomotion, but it is somewhat larger in body and clinging positional behaviors; towards the other mass and more specialized in exploiting divergent pole, the Pitheciinae, first the more quadrupedal Caca- microhabitats by utilizing more destructive foraging jao and Chiropotes, who also exhibit hindlimb suspen- techniques. The generalized locomotor repertoire uti- sion and foot reversal, followed by Pithecia; finally large- lized by medium-sized platyrrhines has also been pro- bodied Alouatta and the other Atelidae at the extreme, posed, on the basis of assessing the available exhibiting climbing/clambering and suspensory behav- postcranial elements, as a pattern relevant to the prim- iors, with increased tail-assited suspension in the latter itive anthropoid condition (e.g., Gebo and Dagosto, (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), condition, if Branisella is a member of an ancient radia- of the fossil species with known postcrania permitting tion of stem platyrrhines, which bears no apparent affin- locomotor reconstruction, would exhibit a narrower spec- ities to modern taxa (e.g., Rosenberger et al., 1991; trum of variation, with many extinct taxa falling within Takai et al., 2000; Kay et al., 2008). In that case, the the range of the central cloud of species, among quadru- model proposed by Ford (1988), based on the study of pedal leapers and quadrupedal/climbers. By contrast, the locomotor diversity of extant platyrrhines, would the younger large-bodied Caipora and Protopithecus point to the ancestral morphology of the last common would align with the more suspensory extant Atelinae. ancestor of extant platyrrhine genera, rather than the However, these locomotor patterns do not form exclusive earliest and presumed ancestor of all platyrrhines, fossil, units, classified on a strictly phylogenetic basis. They and living. demonstrate adaptive strategies to specific habitats, at The early Miocene fossils considered here, Dolichoce- times convergent, that are shared by more than one bus,Soriacebus, Carlocebus, Homunculus (and Tremace- sympatric or syntopic species (Fleagle and Reed, 1996, bus, not known postcranially) from Patagonia, likely 1999). represent a distinct ancient radiation (Kay et al., 2008; Until the recovery of postcranial elements for the ear- Kay and Fleagle, 2010), in our view. The oldest of these, liest platyrrhine fossil, Branisella, little can be said with Dolichocebus, shows the generalized mixture of quadru- certainty about its locomotor behavior, other than per- pedal activities with leaping behavior, which most haps a likely correlation to its body size and the locomo- closely approximates Ford’s morphotype reconstruction. tor behavior of similar-sized extant playrrhines, that is, If Dolichocebus is indeed a primitive member of the Sai- arboreal quadrupedal running and leaping. This may be miri lineage (Tejedor, 2008; Rosenberger et al., 2009), its a moot point in the search for the ancestral platyrrhine 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 recovered fossil platyrrhines, such as the Callicebus-like extant genera. Otherwise its postcranial generalization frugivore/folivore and quadrupedal leaper Homunculus, would be merely a primitive retention for a small to me- whose inferred locomotion aligns with that of the titi dium-sized platyrrhine. On the other hand, Soriacebus monkey’s generalized positional repertoire. and Carlocebus seem to be postcranially more derived, Even Antillothrix, the Pleistocene Hispaniolan fossil, exhibiting mixed quadrupedal and climbing/clambering, is now considered as a remnant of an early platyrrhine and even some suspensory habits, especially in Soriace- radiation, probably similar to that of the early taxa dis- bus (Meldrum, 1990). These adaptations, which very cussed above (Rosenberger et al., 2011; Kay et al., 2011). likely enabled them to differentially utilize the ancient This is particularly interesting since this fossil seems to forests and exploit the available fruit sources, seem to exhibit a derived morphology correlated with quadruped- parallel the evolution of locomotor patterns in Pithecii- alism, climbing/clambering, and possibly even suspen- nae and Callicebus, where some authors align these fos- sory habits (Rosenberger et al., 2011; Kay et al., 2011). sils (e.g., Rosenberger, 2002; Tejedor, 2008; Rosenberger This behavior could be a novel adaptation to niche parti- et al., 2009). Thus, these platyrrhines may represent tioning in an isolated insular habitat, just as was the early members of the pitheciid clade, or they represent peculiar semiterrestriality of Paralouatta in Cuba, and early forms that were adapted to analogous niches in the kinkajou-like suspension of Xenothrix in Jamaica the early Miocene southern forests, convergent on the (McPhee and Fleagle, 1991). Alternatively, it could have pitheciid condition. By contrast, the dental pitheciine been retention of positional abilities of an earlier radia- Proteropithecia with its associated talus, as well as the tion similar to the early Miocene Argentinean fossils. isolated talus from Chile, show no postcranial similarity However, the overall plasticity of positional behavior or convergence on the derived pitheciine condition, (e.g., Garber and Preutz, 1995) lends support to the for- rather morphologies correlated with generalized quadru- mer hypothesis. pedalism and leaping, correlated with medium to small In the middle Miocene, the rich paleo-community of body size, as in Callicebus for example (Kay et al., La Venta has been extensively studied (e.g., Hartwig 1998). The meager postcranial remains of these taxa do and Meldrum, 2002). The three sets of Nuciruptor and not offer a clear resolution to the question of synapomor- Cebupithecia, Neosaimiri, and Laventiana, plus Aotus phy or homoplasy at this time. A pattern of convergent dindensis, seem to represent three distinct adaptive niche partitioning might also be suggested by other clades. The first favored hard or unripe fruit and seed LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES 2009 eating accessed by quadrupedalism and leaping; the sec- chiating folivore/frugivore inhabiting the Mata Atlantica ond, an insectivorous/frugivorous diet acquired by of southeastern Brazil, leaves a void in the reconstruc- increased bouts of quadrupedal walk/run and leaping; tion of the evolution of suspensory behavior and its rela- and the third, a frugivore/insectivore frequently using tion to frugivory and energy maximization within this quadrupedal walking/running and leaping behavior. large-bodied clade. Nevertheless, field data on the loco- These adaptations seem very comparable to the ones motor ecology of more Ateles species are still required, in observed in modern counterparts of their respective order to obtain a complete image of the adaptive signifi- clades, such as Pithecia, Saimiri, and Aotus, where they cance of tail-forelimb suspension in atelid evolution. are found syntopically. All these three fossil groups seem We are far from completing the evolutionary history of to have retained in some measure the positional adapta- platyrrhines. The recovery of new and more complete tions of the earliest platyrrhine—a mixture of quaruped- fossils is enriching the paleontological record, while alism and leaping. Among the small- to medium-sized additional field studies are adding to an understanding platyrhrines, modern Cebinae and Aotus especially have of the adaptive significance and general plasticity of retained this pattern throughout their long evolutionary locomotor and postural diversity of extant taxa. The history, whereas the Pitheciinae evolved towards two dif- growing platyrrhine postcranial fossil record has ferent patterns: relatively longer limbs and increased witnessed significant additions since last reviewed by suspensory behavior, and in the case of Pithecia pithecia, Meldrum (1993). Novel hypotheses synthesizing the increased clinging and leaping. P. pithecia, evolved to be framework of platyrrhine origins and phylogenetic diver- one of the most saltatorial modern platyrrhines (e.g., sification have been proposed in recent years, focusing Fleagle and Meldrum, 1988).The sister taxa Cacajao and discussions on both morphologies and methodologies. Chiropotes adhere to a more quadrupedal strategy, Hopefully these will lead to clarification of the nature of including a variable but significant amount of leaping, the proto-platyrrhine immigration to the Western Hemi- which is performed in a different manner from that sphere and subsequent pattern of platyrrhine diversifi- encountered in Pithecia (Walker and Ayres, 1996), and cation. Although the evolution of locomotor diversity below-branch behavior, especially hindlimb suspension offers many insights into the adative radiation among (Fleagle and Meldrum; 1988; Meldrum et al., 1997; Mel- platyrrhines, it offers no definitive resolution to compet- drum, 1998). ing hypotheses of platyrrhine phylogeny. Atelidae and Callitrichinae, the two most derived groups that were mentioned earlier, have been the sub- ACKNOWLEDGEMENTS ject of extensive studies, and the fact that they are char- acterized by either very few, but highly derived fossil The authors are particularly grateful to Alfie Rose- members like the Protopithecus and Caipora in the nberger, who invited them to participate in this project. atelid lineage, or fossils of less certain affinities with no His continuous encouragement and editorial guidance preseserved postcranial elements, as in the callitrichine helped us complete this review, which likewise rests lineage, leaves little to discuss. upon the contributions of mentors, colleagues, museum The Callitrichinae stand out because there are compa- curartors, and funders, too numerous to mention singly. rably few field studies on the locomotion and postures of several extant genera, such as Leontopithecus, Mico, Callibella, and Callithrix. Because of their derived post- LITERATURE CITED crania (Ford, 1988; Davis, 2002; Ford and Davis, 2009), Anapol F, Fleagle JG. 1988. Fossil platyrrhine forelimb bones from these genera are expected to be rather specialized in the early Miocene of Argentina. Am J Phys Anthropol 76:417– their positional behavior, but recent studies have shown 428. significant plasticity in other marmosets (e.g., Porter Bauer K, Schreiber A. 1997. Double invasion of Tertiary island and Garber, 2004; Youlatos, 2009). The diversity of adap- South America by ancestral New World monkeys. Biol J Linn Soc tations in these forms could be equivalent to that 20:1–29. observed in Saguinus (e.g., Garber, 1992, 2007). Bezanson M. 2009. Life history and locomotion in Cebus capucinus In contrast, the Atelidae seem to have been over- and Alouatta palliata. Am J Phys Anthropol 140:508–517. sampled in the wild. Alouatta, the most basal member of Bicca-Marques JC, Calegaro-Marques C. 1995. Locomotion of black the group is relatively well known. Some species have howlers in a habitat with discontinuous canopy. Folia primatol been well studied in a variety of habitats and do show 64:55–61. some diversity around a well-established locomotor pat- Bluntschli H. 1913. Die fossilen affen patagonies und der ursprung tern characterized by quadrupedal walking, clambering, der platyrrhinen affen. Anat Anzeig 44:33–43. climbing, and tail-hind limb suspension. However, as Bluntschli H. 1931. Homunculus patagonicus und die ihm zuger- Alouatta is one of the few platyrrhines that is so wide- eihten fossilfunde aus den Santa-Cruz-Schichten patagoniens: spread across the Americas, from dry tropical forests in eine morphologisce revision an hand der originalstucke in der sammlung Ameghino zu La Plata. Genen Morphol Jahr 67:811– southern Mexico to temperate forests in northern Argen- 892. tina, more studies are required to understand the poten- Boinski S. 1989. The positional behavior and substrate use in the tial behavioral flexibility of this platyrrhine. Only Cebus squirrel monkeys: ecological implications. J Hum Evol 18:659– shows a similar degree of adaptive plasticity. Further 677. studies will also shed light on the adaptive significance Bown TM, Larriestra CN. 1990. Sedimentary paleoenvironments of of tail-assisted-hind limb suspension in relation to fossil platyrrhine localities, Miocene Pinturas Formation, Santa diverse micro-habitat parameters. Two of the more Cruz Province, Argentina. J Hum Evol 19:87–119. derived members of the group, Ateles and Lagothrix, are Cant JGH. 1986. Locomotion and feeding postures of spider and now well known from the field, but the lack of system- howling monkeys: field study and evolutionary interpretation. atic quatitative data for Brachyteles, as a tail-arm bra- Folia primatol 46:l–14. 2010 YOULATOS AND MELDRUM

Cant JGH, Youlatos D, Rose MD. 2001. Locomotor behavior of Lago- Garber PA. 1991. A comparative study of positional behavior in thrix lagothricha and Ateles belzebuth in Yasuni National Park, three species of tamarind monkeys. Primates 32:219–230. Ecuador: general patterns and nonsuspensory modes. J Hum Evol Garber PA. 1992. Vertical clinging, small body size, and the evolu- 41:141–166. tion of feeding adaptations in the Callitrichinae. Am J Phys Cant JGH, Youlatos D, Rose MD. 2003. Suspensory locomotion of Anthropol 88:469–482. Lagothrix lagothricha and Ateles belzebuth in Yasuni National Garber PA. 2007. Primate locomotor behavior and ecology. In: Park, Ecuador. J Hum Evol 44:685–699. Campbell C, Fuentes A, MacKinnon KC, Panger M, Bearder S, Cartelle C, Hartwig WC. 1996. A new extinct primate among the editors. Primates in perspective. Oxford: Oxford University Press. Pleistocene megafauna of Bahia, Brazil. Proc Natl Acad Sci USA p 543–560. 93:6405–6409. Garber PA, Leigh SR. 2001. Patterns of positional behavior in Ciochon RL, Chiarelli AB. 1980. Evolutionary biology of the New mixed-species troops of Callimico goeldii, Saguinus labiatus, and World monkeys and continental drift. New York: Plenum. Saguinus fuscicollis in northwestern Brazil. Am J Primatol Ciochon RL, Corruccini RS. 1975. Morphometric analysis of platyr- 54:17–31. rhine femora with taxonomic implications and notes on two fossil Garber PA, Blomquist GE, Anzenberger G. 2005. Kinematic analy- forms. J Hum Evol 4:193–217. sis of trunk-to-trunk leaping in Callimico goeldii. Int J Primatol Collins AC. 2004. Atelinae phylogenetic relationships: the trichot- 26:223–240. omy revived? Am J Phys Anthropol 124:285–296. Garber PA, Rosenberger AL, Norconk MA. 1996. Marmoset miscon- Cooke SB, Rosenberger AL, Turvey S. 2011. An extinct monkey ceptions. In: Norconk MA, Rosenberger AL, Garber PA, editors. from Haiti and the origins of Greater Antillean primates. Proc Adaptive radiations of neotropical primates. New York: Plenum Natl Acad Sci USA 108:2699–2704. Press. p 87–95. Dagosto M. 1988. Implications of postcranial evidence for the origin Garber PA, Sallenave A, Blomquist GE, Anzenberger G. 2009. A of Euprimates. J Hum Evol 17:35–56. comparative study of the kinematics of trunk-to-trunk leaping in Davis LC. 2002. Functional morphology of the forelimb and long Callimico goeldi, Callitrhix jacchus, and Cebuella pygmaea. In: bones in the (Platyrrhini, Primates). PhD Disserta- Ford SM, Porter LM, Davis LC, editors. The smallest anthro- tion. Carbondale, Southern Illinois University. poids: the marmoset/callimico radiation. New York: Springer Ver- Davis LC. 1987. Morphological evidences of the positional behaviour lag. p 259–278 in the hindlimb of Cebupithecia sarmientoi (Primates: Platyr- Garber PA, Preutz D. 1995. The positional behavior of moustached rhini). MA Thesis, Arizona State University. tamarin monkeys: effects of habitat on locomotor variability and Defler TR. 1999. Locomotion and posture in Lagothrix lagotricha. locomotor stability. J Hum Evol 28:411–426. Folia primatol 70:313–327. Garber PA. Rehg JA. 1999. The ecological role of the prehensile tail Erikson GE. 1963. Brachiation in the new World monkeys and in white-faced capuchins (Cebus capucinus). Am J Phys Anthropol anthropoid apes. Symp Zool Soc Lond 10:135–164. 110:325–339. Fleagle JG. 1999. Primate adaptation and evolution. 2nd ed. San Gebo DL. 1992. Locomotor and postural behavior in Alouatta pal- Diego: Academic Press. liata and Cebus capucinus. Am J Primatol 26:277–290. Fleagle JG, Meldrum DJ. 1988. Locomotor behavior and skeletal Gebo DL, Dagosto M. 2004. Anthropoid origins: postcranial evidence morphology of two sympatric pitheciine monkeys, Pithecia pithe- from the Eocene of Asia. In: Ross CF, Kay RF, editors. Anthropoid cia and Chiropotes satanas. Am J Primatol 16:227–249. Origins: New Visions. New York: Kluwer Academic/Plenum. p Fleagle JG, Mittermeier RA. 1980. Locomotor behavior and compar- 369–380. ative ecology of seven Surinam monkeys. Am J Phys Anthropol Gebo DL, Dagosto M, Rosenberger AL, Setoguchi T. 1990. New pla- 52:301–314. tyrrhine tali from La Venta, Colombia. J Hum Evol 19:737–746. Fleagle JG, Reed KE. 1996. Comparing primate communities: a Gebo DL, Simons EL. 1987. Morphology and locomotor adaptations multivariate approach. J Hum Evol 30:489–510. of the foot of early Oligocene anthropoids, Am J Phys Anthropol Fleagle JG, Reed KE. 1999. Phylogenetic and temporal perspectives 74:83–101. on primate ecology. In: Fleagle JG, Janson C, Reed KE, editors. Guillot D. 2009. Measures of postural and locomotor performance in Primate communities. New York: Cambridge University Press. wild atelid primates: a comparative analysis of Alouatta senicu- p 92–115. lus, Lagothrix poeppigii, and Ateles belzebuth. Ph.D. Dissertation, Fleagle JG, Tejedor MF. 2002. Early platyrrhines of southern South Boston University. America. In: Hartwig WC, editor. The primate fossil record. Cam- Harada ML, Schneider H, Schneider MPC, Sampaio I, Czelusniak bridge: Cambridge University Press. p 161–173. J, Goodman M. 1995. DNA evidence on the phylogenetic system- Fontaine R. 1990. Positional behavior in Saimiri boliviensis and atics of New World monkeys: support for the sistergrouping of Ateles geoffroyi. Am J Phys Anthropol 82:485–508. Cebus and Saimiri from two unlinked nuclear genes. Mol Phylo- Ford SM. 1980. Callitrichids as phyletic dwarfs, and the place of genet Evol 4:331–349. the Callitrichidae in Platyrrhini. Primates 21:31–43. Hartwig W, Meldrum DJ. 2002. Miocene platyrrhines of the north- Ford SM. 1988. Postcranial adaptations of the earliest platyrrhine. ern Neotropics. In: Hartwig WC, editor. The primate fossil record. J Hum Evol 17:155–192. Cambridge: Cambridge University Press. p. 175–187. Ford SM. 1990a. Locomotor adaptations of fossil platyrrhines. Hartwig WC, Cartelle C. 1996. A complete skeleton of the giant J Hum Evol 19:141–173. South American primate Protopithecus. Nature 381:307–311. Ford SM. 1990b. Platyrrhine evolution in the West Indies. J Hum Hershkovitz P. 1977. Living New World Monkeys (Platyrrhini): with Evol 19:237–254. an Introduction to Primates. Vol 1. Chicago: University of Chicago Ford SM, Davis LC. 1992. Systematics and body size: implications Press. for feeding adaptations in New World monkeys. Am J Phys Hoffstetter MR. 1980. Origin and deployment of New World mon- ANthropol 88:415–468. keys emphasizing the southern continents route. In: Ciochon RF, Ford SM, Davis LC. 2009. Marmoset postcrania and the skeleton of Chiarelli AB, editors. Evolutionary biology of New World monkeys the dwarf marmoset, Callibella humilis. In: Ford SM, Porter LM, and continental drift. New York: Plenum Press. p 103–122. Davis LC, editors. The smallest anthropoids: the marmoset/calli- Houle A. 1999. The origin of platyrrhines: an evaluation of the Ant- mico radiation. New York: Springer Verlag. p 411–448. arctic scenario and the floating island model. Am J Phys Anthro- Ford SM, Porter LM, Davis LC. 2009. The smallest anthropoids: pol 109:541–559. the marmoset/callimico radiation. New York: Springer Verlag. Hodgson JA, Sterner KN, Matthews LJ, Burrell A, Jani RA, Raaum Garber PA. 1980. Locomotor behavior and feeding ecology of the RL, Stewart CB, Distotell TR. 2009. Successive radiations, not Panamanian tamarin (Saguinus oedipus geoffroyi, Callitrichidae, stasis, in the South American primate fauna. Proc Natl Acad Sci Primates). Int J Primatol 1:185–201. USA 106:5534–5539. LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES 2011

Horovitz I. 1999. A phylogenetic study of living and fossil platyr- MacFadden BJ. 2000. Cenozoic mammalian herbivores from the rhines. Am Mus Novit 3269:1–40. Americas: Reconstructing ancient diets and terrestrial commun- Horovitz I, MacPhee RDE. 1999. The Quaternary Cuban platyr- ities. Ann Rev Ecol Syst 31:33–59. rhine Paralouatta varonai and the origin of Antillean monkeys. MacPhee RDE, Horovitz I. 2002. Extinct Quaternary platyrrhines J Hum Evol 36:33–68. of the Greater Antilles and Brazil. In: Hartwig WC, editor. The Horovitz I, Zardoya R, Meyer A. 1998. Platyrrhine systematics: a Primate Fossil Record. Cambridge: Cambridge University Press. systematic analysis of molecular and morphological data. Am J p 189–200. Phys Anthropol 106:261–281. MacPhee RDE, Fleagle JG. 1991. Postcranial remains of Xenothrix Iturralde Vinent MA, MacPhee RDE. 1999. Paleogeography of the mcgregori (Primates, Xenotrichidae) and other Late Quaternary Caribbean region: implications for Cenozoic biogeography. Bull from Long Mile Cave, Jamaica. Bull Am Mus Nat Hist Am Mus Nat Hist 238:1–95. 206:287–321. Jones AL. 2008. The evolution of brachiation in atelid primates, an- MacPhee RDE, Meldrum DJ. 2006. Postcranial remains of the cestral character states and history. Am J Phys Anthropol extinct monkeys of the Greater Antilles (Platyrrhini, Callicebinae, 137:123–144. Xenotrichini), with a consideration of semiterrestriality in Paral- Janson CH, Boinski S. 1992. Morphological and behavioral adapta- ouatta. Am Mus Novit 3516:1–65. tions for foraging in generalist primates—the case of cebines. Am MacPhee RDE, Iturralde-Vinent MA, Gaffney ES. 2003. Domo de J Phys Anthropol 88:483–498. Zaza, an Early Miocene vertebrate locality in south-central Cuba, Karantanis NE. 2010. Comparative positional behaviour in three with notes on the tectonic evolution of Puerto Rico and Mona Pas- captive callitrichid species: Leontopithecus chrysomelas, Saguinus sage. Am Mus Novit 3394:1–42. imperator and Cebuella pygmaea. MSc Thesis, University College MacPhee RDE, Woods CA. 1982. A new fossil cebine from Hispa- of London. niola. Am J Phys Anthropol 58:419–436. Kay RF. 1990. The phyletic relationships of extant and fossil Pithe- Meireles CM, Czelusniak J, Schneider MPC, Muniz JAPC, Brigido ciinae (Platyrrhini, Anthropoidea). J Hum Evol 19:175–208. MC, Ferreira HS, Goodman M. 1993. Molecular phylogeny of Kay RF. 1994. ‘‘Giant’’ tamarin from the Miocene of Colombia. Am J atelid NewWorld monkeys (Platyrrhini, Atelinae) based on g-glo- Phys Anthropol 95:333–353. bin gene sequences: evidence that Brachyteles is the sister group Kay RF, Campbell V, Rossie JB, Colbert MW, Rowe TB. 2004. Olfac- of Lagothrix. Mol Phylogenet Evol 12:10–30. tory fossa of Tremacebus harringtoni (Platyrrhini, early Miocene, Meldrum DJ. 1990. New fossil platyrrhine tali from the early Mio- Sacanana, Argentina): implications for activity pattern. Anat Rec cene of Argentina. Am J Phys Anthropol 83:403–418. A 281:1157–1172. Meldrum DJ. 1993. Postcranial adaptations and positional behavior Kay RF, Cozzuol MA. 2006. New platyrrhine monkeys from the Soli- in fossil platyrrhines. In: Gebo DL, editor. Postcranial adaptation mo˜es Formation (late Miocene, Acre State, Brazil). J Hum Evol in nonhuman primates. DeKalb: Northern Illinois University, p 50:673–686. 235–251. Kay RF, Fleagle JG, Mitchell TRT, Colbert M, Bown T, Powers DW. Meldrum DJ. 1998. Tail-assisted hindlimb suspension as a transi- 2008. The anatomy of Dolichocebus gaimanensis, a stem platyr- tional behavior in the evolution of prehensile tails. In: Strasser E, rhine monkey from Argentina. J Hum Evol 54:323–382. Fleagle JG, McHenry HM, editors. Advances in primatology: pri- Kay RF, Johnson D, Meldrum DJ, 1998. A new pitheciin primate mate locomotion. New York: Plenum Press. p 145–156. from the middle Miocene of Argentina. Am J Primatol 45:317– Meldrum DJ, Dagosto MD, White J. 1997. Hindlimb suspension 336. and hindfoot reversal in Varecia variegata and other arboreal Kay RF, Fleagle JG. 2010. Stem taxa. Homoplasy, long lineages, mammals. Am J Phys Anthropol 103:85–102. and the phylogenetic position of Dolichocebus. J Hum Evol Meldrum DJ, Fleagle JG, Kay RF. 1990. Partial humeri of two Mio- 59:218–222. cene Colombian primates. Am J Phys Anthropol 81:413–422. Kay RF, Hunt, KD, Beeker CD, Conrad GW, Johnson CC, Keller J. Meldrum DJ, Kay RF. 1997a. Nuciruptor rubricae, a new pitheciin 2011. Preliminary notes on a newly discovered skull of the extinct seed predator from the Miocene of Colombia. Am J Phys Anthro- monkey Antillothrix from Hispaniola and the origin of the pol 102:407–427. Greater Antillean monkeys. J Hum Evol 60:124–128. Meldrum DJ, Kay RF. 1997b. Primate postcranial fossils from the Kay RF, Madden RH, Plavcan JM, Cifelli RL, Diaz JG. 1987. Stirto- Miocene of Colombia. In: Kay RF, Madden RH, Cifelli RL, Flynn nia victoriae, a new species of Miocene Colombian primate. J, editors. A history of neotropical fauna: vertebrate paleontology J Hum Evol 16:173–196. of the miocene of Tropical South America. Washington DC: Smith- Kay RF, Meldrum DJ. 1997. A new small platyrrhine from the Mio- sonian Institution Press. p 459–472. cene of Colombia and the phyletic position of the callitrichines. Meldrum DJ, Lemelin P. 1991. Axial skeleton of Cebupithecia sar- In: Kay RF, Madden RH, Cifelli RL, Flynn J, editors. A history of mientoi (Pitheciinae, Platyrrhini) from the middle Miocene of La neotropical fauna: vertebrate paleontology of the miocene of Trop- Venta, Colombia. Am J Primatol 25:69–90. ical South America. Washington DC: Smithsonian Institution Mittermeier RA. 1978. Locomotion and posture in Ateles geoffroyi Press. p 435–458. and Ateles paniscus. Folia primatol 30:161–193. Kay RF, Williams BA, Anaya F. 2001. The adaptation of Branisella Nakatsukasa M, Takai M, Setoguchi T. 1997. Functional morphol- boliviana, the earliest South American monkey. In: Plavcan JM, ogy of the postcranium and locomotor behaviour of Neosaimiri van Schaik C, Kay RF, Jungers WL, editors. Reconstructing fieldsi,aSaimiri-like middle Miocene platyrrhine. Am J Phys behavior in the primate fossil record. New York: Kluwer Aca- Anthropol 102:515–544. demic/Plenum Publishers. p 339–370. Napier JR, Davis PR. 1959. The forelimb skeleton and associated Kinzey WG. 1992. Dietary and dental adaptations in the Pitehcii- remains of Proconsul africanus. Fossil Mam Afr 16:1–69. nae. Am J Phys Anthropol 88:499–514. Opazo JC, Wildman DE, Prychitko T, Johnson RM, Goodman M. Lawler RR, Ford SM, Wright PC, Easley SP. 2006. The locomotor 2006. Phylogenetic relationships and divergence times among behavior of Callicebus brunneus and Callicebus torquatus. Folia New World monkeys (Platyrrhini, Primates). Mol Phylogenet Evol primatol 77:228–239. 40:274–280. Lockwood CA. 1999. Homoplasy and adaptation in the atelid post- Pascual R, Ortiz Jaureguizar E. 1990. Evolving climates and mam- cranium. Am J Phys Anthropol 108:459–482. mal faunas in Cenozoic South America. J Hum Evol 19:23–60. Luchterhand K, Kay RF, Madden RH. 1986. Mohanamico hershko- Porter LM, Garber PA. 2004. Goeldi’s monkey: a primate paradox? vitzi, gen. et sp. Nov., un primate du Mioce`ne moyen d’Ame´rique Evol Anthrop 13:104–115. du Sud. Comp Rend Acad Sci Paris 303:1753–1758. Prates HM, Bicca Marques JC. 2008. Age-sex analysis of activity MacFadden BJ. 1990. Chronology of Cenozoic primate localities in budget, diet, and positional behavior in Alouatta caraya in an South America. J Hum Evol 19:7–21. orchard forest. Int J Primatol 29:703–715. 2012 YOULATOS AND MELDRUM

Reeser LA. 1984. Morphological affinities of new fossil talus of Doli- Stirton RA. 1951. Ceboid monkeys from the Miocene of Columbia. chocebus gaimanensis. Am J Phys Anthropol 63:206–207. Bull Univ Calif Publ Geol Sci 28:315–356. Rivero M, Arredondo O. 1991. Paralouatta varonai, a new Quater- Stirton RA, Savage DE. 1951. A new monkey from the La Venta nary platyrrhine from Cuba. J Hum Evol 21:1–11. Miocen of Colombia. Compil Estud Geol Offic Colombia 7:345– Rosenberger AL. 1977. Xenothrix and ceboid phylogeny. J Hum Evol 356. 6:461–481. Strier KB. 1992. Atelinae adaptations: behavioral strategies and Rosenberger AL. 1979. Cranial anatomy and implications of Dolicho- ecological constraints. Am J Phys Anthropol 88:515–524. cebus, a late Oligocene ceboid primate. Nature 279 (5712):416–418. Takai M. 1994. New specimens of Neosaimiri fieldsi from La Venta, Rosenberger AL. 1992. Evolution of feeding niches in New World Colombia: A middle Miocene ancestor of the living squirrel mon- monkeys. Am J Phys Anthropol 88:525–562. keys. J Hum Evol 27:329–360. Rosenberger AL. 2002. Platyrrhine paleontology and systematics: Takai M, Anaya F. 1996. New specimens of the oldest fossil platyr- the paradigm shifts. In: Hartwig WC, editor. The primate fossil rhine, Branisella boliviana, from Salla, Bolivia. Am J Phys record. Cambridge: Cambridge University Press. p 151–160. Anthropol 99:301–317. Rosenberger AL. 2010. Platyrrhines, PAUP, parallelism, and the Takai M, Anaya F, Shigehara N, Setoguchi T. 2000. New fossil Long Lineage Hypothesis: a reply to Kay et al. (2008). J Hum materials of the earliest , Branisella boliviana, Evol 59:214–217. and the problem of platyrrhine origins. Am J Phys Anthropol Rosenberger AL, Hartwig WC, Takai M, Setoguchi T, Shigahara N. 111:263–281. 1991a. Dental variabilty in Saimiri and the taxonomic status of Takai M, Anaya F, Suzuki H, Shigehara N, Setoguchi T. 2001. A Neosaimiri fieldsi, and early from La Venta, new platyrrhine from the middle Miocene of La Venta, Colombia, Columbia. Int J Primatol 12:291–302. and the phyletic position of Callicebinae. Anthropol Sci 109:289– Rosenberger AL, Hartwig WC, Wolff RG. 1991b. Szalatavus attri- 308. cuspis, an early platyrrhine primate. Folia primatol 56:225–233. Tejedor MF. 2003. New fossil primate from Chile. J Hum Evol Rosenberger AL, Setoguchi T, Hartwig WC. 1991c. Laventiana 44:515–520. annectens, new genus and species: fossil evidence for the origin of Tejedor MF. 2008. The origin and evolution of Neotropical monkeys. callitrichine monkeys. Proc Natl Acad Sci USA 88:2137–2140. Arquiv Mus Nac Rio Jan 66:251–269. Rosenberger AL, Setoguchi T, Shigehara N. 1990. The fossil record Tejedor MF, Rosenberger AL. 2008. A neotype for Homunculus pata- of callitrichine primates. J Hum Evol 19:209–236. gonicus Ameghino 1891, and a new interpretation of the taxon. Rosenberger AL, Strier KB. 1989. Adaptive radiation of the atelid Paleoanthropology 2008:68–82. primates. J Hum Evol 18:717–750. Walker SE. 1993. Positional Adaptations and Ecology of the Pithe- Rosenberger AL, Tejedor MF, Cooke S, Pekar S. 2009. Platyrrhine ciini. Ph.D. Dissertation, City University of New York. ecophylogenetics, past and present. In: Garber P, Estrada A, Walker SE, Ayres JM. 1996. Positional behavior of the white uakari Bicca-Marques JC. Heymann EW, Strier KB, editors. South (Cacajao calvus calvus). Am J Phys Anthropol 101:161–172. American primates: comparative perspectives in the study of Wildman DE, Jameson NM, Opazo JC, Yi SV. 2009. A fully resolved behavior, ecology and conservation. New York: Springer. p 69– genus level phylogeny of neotropical primates (Platyrrhini). Mol 113. Phylogenet Evol 53:694–702. Rosenberger AL, Cooke SB, Rimoli R, Ni X, Cardoso L. 2011. First Wright KA. 2007. The relationship between locomotor behavior and skull of Antillothrix bernensis, an extinct relict monkey from the limb morphology in brown (Cebus apella) and weeper (Cebus oli- Dominican Republic. Proc Biol Sci 278:67–74. vaceus) capuchins. Am J Primatol 69:736–756. Schneider H, Canavez FC, Sampaio I, Moreira MAM, Tagliaro CH, Wright PC. 1989. The nocturnal primate niche in the New World. J Seuanez HN. 2001. Can molecular data place each Neotropical Hum Evol 18:635–658. monkey in its own branch? Chromosoma 109:515–523. Youlatos D. 1998. Positional behavior of two sympatric Guianan Schneider H, Sampaio I, Harada ML, Barroso CML, Schneider capuchin monkeys, the brown capuchin (Cebus apella) and the MPC, Czelusniak J, Goodman M. 1996. Molecular phylogeny of wedge-capped capuchin (Cebus olivaceus). Mammalia 62:351–365. the New World monkeys (Platyrrhini, Primates) based on two Youlatos D. 1999. Comparative locomotion of six sympatric primates unlinked nuclear genes: IRBP interon 1 and e-globin sequences. in Ecuador. Ann Sci Nat Zool 20:161–168. Am J Phys Anthropol 100:153–179. Youlatos D. 2002. Positional behavior of black spider monkey (Ateles Schneider H, Schneider MPC, Sampaio I, Harada ML, Stanhoope paniscus) in French Guiana. Int J Primatol 23:1071–1093. M, Czelusniak J, Goodman M. 1993. Molecular phylogeny of the Youlatos D. 2004. Multivariate analysis of organismal and habitat New World monkeys (Platyrhini, Primates). Mol Phylogenet Evol parameters in two Neotropical primate communities. Am J Phys 2:225–242. Anthropol 123:181–194. Scho¨n Ybarra MA, Scho¨n MA. 1987. Positional behavior and limb Youlatos D. 2008. Locomotion and positional behavior of spider bone adaptations in red howling monkeys (Alouatta senicuhs). monkeys. In: Campbell CJ, editor. Spider monkeys: behavior, ecol- Folia primatol 49:70–89. ogy and evolution of the genus Ateles. Cambridge: Cambridge Schrago CG. 2007. On the time scale of New World primate diversi- University Press. p 185–219. fication. Am J Phys Anthropol 132:344–354. Youlatos D. 2009. Locomotion, postures, and habitat use by pygmy Seiffert ER, Simons EL, Simons CVM. 2004. Phylogenetic, biogeo- marmosets (Cebuella pygmaea). In: Ford SM, Porter LM, Davis graphic, and adaptive implications of new fossil evidence bearing LC, editors. The smallest anthropoids: the marmoset/callimico on crown anthropoid origins and early stem catarrhine evolution. radiation. New York: Springer Verlag. p 279–297. In: Ross C, Kay RF, editors. Anthropoid origins: new visions. New Youlatos D, Gasc JP. 2001. Comparative positional behaviour of five York: Kluwer Academic/Plenum Publishers. p 157–182. primates. In: Bongers F, Charles-Dominique P, Forget M, The´ry Setoguchi T, Rosenberger AL. 1987. A fossil owl monkey from La M, editors. Nouragues: dynamics and plant-animal interactions in Venta, Colombia. Nature 326:692–694. a neotropical rain forest. Dordrecht: Kluwer Academic Publishers. Singer SS, Schmitz J, Schwiegk C, Zischler H. 2003. Molecular p 103–114. cladistic markers in New World monkey phylogeny (Platyrrhini, Zaluar MT, Rocha Barbosa O, Loguercio MF, Rangel CH, Primates). Mol Phylogen Evol 26:490–501. Youlatos D. 2010. Utilizac¸a˜o do habitat, locomoc¸a˜o e postura de Stafford BJ, Rosenberger AL, Beck BB. 1994. Locomotion of free- Callithrix jacchus Linnaeus, 1758 (Mammalia, Primates). ranging golden lion tamarins (Leontopithecus rosalia) at the V Congresso Brasileiro de Mastozoologia, Sa˜o Pedro/ Sa˜o Paulo, National Zoological Park. Zoo Biol 13:33–344. Brazil.