Locomotor Diversification in New World MonkeysRunning Climbing or Clawing Along Evolutionary Branches.код для вставкиСкачать
THE ANATOMICAL RECORD 294:1991–2012 (2011) Locomotor Diversification in New World Monkeys: Running, Climbing, or Clawing Along Evolutionary Branches 1 DIONISIOS YOULATOS1* AND JEFF MELDRUM2 Department of Zoology, Aristotle University of Thessaloniki, School of Biology, Thessaloniki, Greece 2 Department of Biological Sciences, Idaho State University, Pocatello, Idaho ABSTRACT Modern platyrrhines exhibit a remarkable diversity of locomotor and postural adaptations, which evolved along multiple trajectories since the initial immigration to the island continent of South America. We trace this diversiﬁcation by reviewing the available paleontological and neontological data for postcranial morphology and ecological adaptation. Fossil platyrrhines are notably diverse, from the Oligocene Branisella, to the varied Patagonian early Miocene quadurpedal-leaping and quadrupedalclimbing fossils of disputed afﬁnities, on through the rich middle Miocene Colombian quadurpedal-leaping forms. More recent taxa exhibit even more derived positional patterns, from the largest suspensory atelids in Pleistocene Brazil, to the remarkable Antillean radiation with suspensory forms and also semiterrestrial species, with postcranial morphology convergent on some Old World monkeys. Field studies of positional behavior of modern platyrrhines set the framework for a spectrum of locomotor adaptations. Central within this spectrum is a cluster of medium-sized species with generalized locomotion (quadrupedal-leaping). At opposite poles lie the more derived conditions: large-bodied species exhibiting locomotor specializations for climbing-suspension; small-bodied species exhibiting adaptations for claw climbing and leaping. This behavior-based spectrum of locomotor diversiﬁcation is similarly evident in a morphology-based pattern, that is, that produced by the shape of the talus. The implications of the record of platyrrhine postcranial evolution for the competing hypotheses of platyrrhine phylogenetic patterns, the ‘‘long lineage hypothesis’’ and the ‘‘stem platyrrhine hypothesis,’’ are considered. Anat C 2011 Wiley Periodicals, Inc. Rec, 294:1991–2012, 2011. V Key words: platyrrhines; locomotion; evolution; fossils; talus New World Monkeys (NWMs) are a diverse radiation of anthropoid primates that currently occupy a wide range of habitats spanning the American continents, from southern Mexico to Northern Argentina. They represent almost 1/3 of all living primates, with several extant species discovered and identiﬁed quite recently and others differentiated through more profound taxonomic analyses (see Rosenberger et al., 2009). The present day diversity of NWMs is generally held to be the result of a single colonization by a group of primitive anthropoids, which rafted over the Paleogene Atlantic Ocean from Western Africa aided by paleowinds and currents (Ciochon and Chiarelli, 1980; Hoffstetter, 1980; Fleagle, 1999; Houle, 1999). If this scenario holds true, C 2011 WILEY PERIODICALS, INC. V NWMs are most likely monophyletic, a conclusion that has received support from molecular studies, such as transposable Alu elements (Singer et al., 2003). Grant sponsor: Aristotle University of Thessaloniki. *Correspondence to: Dionisios Youlatos, Aristotle University of Thessaloniki, School of Biology, Department of Zoology, GR54124 Thessaloniki, Greece. Fax: þ302310998269. E-mail: firstname.lastname@example.org Received 15 September 2011; Accepted 16 September 2011 DOI 10.1002/ar.21508 Published online 1 November 2011 in Wiley Online Library (wileyonlinelibrary.com). 1992 YOULATOS AND MELDRUM Alternately, multiple colonization lineages, or events, would have resulted in paraphyly in NWMs, as suggested by the analysis of antigenic determinants from selected serum proteins (Bauer and Schreiber, 1997). In either case, the timing of this event, or events, remains uncertain, but likely occurred sometime before the late Eocene, earlier than 37 Ma (Houle, 1999; Kay et al., 2004; Seiffert et al., 2004). To survive the transoceanic journey, protoplatyrrhines were likely preadapted to strong seasonal variations in water availability in their original (African) environment (Houle, 1999). South America of that time was characterized by a cooler, seasonal climate, and dominated by a mixture of forests and vast open grasslands (MacFadden, 2000). This diverse habitat undoubtedly played a signiﬁcant role in platyrrhine diversiﬁcation and dispersal. Modern platyrrhines occupy diverse habitats such as the forests of the great Amazonian basin, the semideciduous Atlantic forests, and the drier savannas, grasslands, or shrub lands that exist either within extensive forested areas (e.g., Guyanan savannas) or on the fringes of great forests (e.g., Venezuelan llanos). The exploitation of such varied habitats has resulted in distinct morphological, ecological and behavioral adaptations, which are broadly correlated to speciﬁc phylogenetic groups (Ford and Davis, 1992; Rosenberger, 1992; Fleagle and Reed, 1996, 1999; Youlatos, 2004; Rosenberger et al., 2009). The depth of these lneages is still debated. Rosenberger et al. (2009) and Rosenberger (2010) advocate the ‘‘long lineage hypothesis’’ (LLH) that modern NWMs are characterized by a number of long-lived clades and the sufﬁciently known fossil taxa are actually early afﬁliates of these. The interpretation of some divergence date estimates, based on molecular clock data, appear to support the LLH (e.g., Schneider et al., 2001; Opazo et al., 2006; Schrago, 2007). In contrast, Kay et al. (2008) and Kay and Fleagle (2010) propose the ‘‘stem platyrrhine hypothesis,’’ concluding that most early Patagonian fossils bear no relationships to particular modern clades. Instead, they comprise an earlier radiation, now largely extinct, and ﬁlled niches analogous to the ones occupied by modern platyrrhines, which are presumed to be the latest in a series of radiations. Kay and Fleagle (2010) point out that different methodologies produce varying results from the same data, that is Opazo et al. (2006), and that alternate divergence times lend support to the stem playrrhine hypothesis. Modern platyrrhines form groups with rather evident and distinct adaptations that have been well-studied behaviorally (e.g., Garber, 1992; Janson and Boinski, 1992; Kinzey, 1992; Rosenberger, 1992; Strier, 1992) and morphologically (e.g., Erikson, 1963; Hershkovitz, 1977; Fleagle and Meldrum, 1988; Ford and Davis, 2009). In this article we will adhere to the revised phylogeny of Kay et al. (2008), that is the Pitheciidae consist of the Pitheciinae (Cacajao, Pithecia, Chiropotes) and Callicebus; the Cebidae consist of the Cebinae ([Cebus, Saimiri] and Aotus} and the Callitrichinae; the Atelidae are Alouatta, Ateles, Barchyteles, and Lagothrix. This is not to say that alternate phylogenies are without merit. However, the subtleties of distinctions are beyond the scope of this review of postcranial and locomotor diversiﬁcation. Pitheciids are medium-sized forest canopy dwellers, which move mainly quadrupedally, on intermediate length limbs, with variable rates of suspension (especially hindlimb suspension) and leaping, and feed on hard or unripe fruit, as well as seeds, insects and leaves (Kinzey, 1992). Cebines are medium-sized dwellers of many forest types and all forest strata, which forage both on fruit and invertebrate and vertebrate prey via more active and manipulative behaviors, moving along with quadrupedalism and leaping (Janson and Boinski, 1992). Callitrichines are small, mainly predacious dwellers of diverse forest types and strata, which base their diets on arthropods and gums using quadrupedalism, leaping and clawed scansorial locomotion in variable degrees (Garber, 1992). Finally, atelids are the largest NWMs dwelling in the upper canopy layers, depend mainly on fruit and leaves and employ more climb/clambering and suspensory patterns of locomotion, on relatively lengthened limbs, via the aid of their prehensile tails (Rosenberger and Strier, 1989; Strier, 1992). The successful exploitation of these divergent niches requires positional behaviors that enable food foraging, manipulation, and ingestion, access to potential mates and escape from potential predators (see e.g., Garber, 2007). Therefore, the study of primate locomotion is fundamental to understanding their adaptive diversity. The objective of this review is to summarize locomotor patterns for both fossil and modern NWMs, deciphering correlated patterns of adaptive radiation. While the fossil record of NWMs, especially with regard to postcranial remains, is relatively scarce, growing interest in the extant taxa of NWMs over the past decades has yielded detailed numerous quantitative reports of their anatomy and positional behavior. A lack of signiﬁcant contributions for certain groups, past and present, is evident, as well as the aforementioned lack of concensus on phylogenetic relationships between fossil and modern taxa. By bringing together this information now, we hope to stimulate the recovery of more fossils, compell additional study of the diverse moderns, and provide a fresh framework for asking questions. OLDEST PLATYRRHINES Branisella The oldest records of NWMs in the Americas are Branisella boliviana and Szalatavus attricuspis from the late Oligocene, more precisely the Deseadan South American Land Mammal Age (SALMA) 26 Ma (Rosenberger et al., 1991c; Fleagle, 1999; Tejedor, 2008; Rosenberger et al., 2009). These earliest undoubted New World anthropoid fossils consist mainly of dental and fragmentary mandibular and cranial elements that have been unearthed from the locality of Salla, Bolivia (Takai and Anaya, 1996; Takai et al., 2000). The phylogenetic relations of Branisella and Szalatavus are still debated. Some authors, based on speciﬁc dental characters, suggest that the latter may be a junior synonym of the former and that they are both related to the rather derived modern callitrichines (Takai et al., 2000). Alternatively, these early forms are considered to bear no differential afﬁliation to particular modern NWMs and do not establish the morphology of the modern platyrrhine morphotype (Fleagle and Tejedor, 2002). Branisella is 10 million years younger than the estimated age of invasion LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES of proto-platyrrhines to South America (Kay et al., 2004, 2008). This gap is vexing since caviomorph rodents, which are considered likely coimmigrants with platyrrhines, have been unearthed in earlier strata (e.g., McFadden, 1990; Rosenberger et al., 2009). No postcranial fossils attributed to Branisella have been recovered, providing no direct evidence of their adaptations for positional behaviors. However, one of the most notable features of the dentition of Branisella is the high-crowned lower teeth and the heavy wear of their cusps that may indicate a diet of very abrasive food, such as silica-rich leaves or grasses (Takai et al., 2000; Kay et al., 2001). On this basis some have inferred a signiﬁcant commitment to terrestriality, or at least an understory habit in relatively open woodland where dental resistance to abrasives would have been an important selective factor. The paleo environment of Salla is described as semiarid, where mainly high-crowned nonprimate mammalian grazers roamed (McFadden, 1990). This might suit the proﬁle of proto-platyrrhines as suggested by Houle (1999), that is, adapted to strong seasonal variations in water availability in their original (African) environment. However, given the small body size of 1,000 g, it is unlikely that terrestrial specializations played a signiﬁcant role in the positional behavior of Branisella. Any further inferences about its positional behavior, in the absence of postcranial fossils, must remain highly speculative. THE SOUTHERN CONE: AN EARLY RADIATION? Dolichocebus The oldest NWM fossil with referred postcranial elements is Dolichocebus gaimanensis from the Sarmiento formation, Chubut Province, Argentina (Table 1). The fossil, known from an almost complete but badly crushed cranium, several isolated teeth, mandibular fragments and a talus, dates from the early Miocene, Colhuehuapian SALMA at 20 Ma (Meldrum, 1990; Fleagle and Tejedor, 2002; Kay et al., 2008). The phylogenetic afﬁnities of this species have given rise to very divergent views reﬂecting differing interpretations of platyrrhine evolutionary radiations (Kay et al., 2008; Kay and Fleagle, 2010; Rosenberger, 2010). One view, based mainly on a number of apparent cranial and postcranial synapomorphies, argues that the fossil is an early member of the lineage leading to modern Saimiri (Reeser, 1984; Gebo and Simons, 1987; Rosenberger, 1992; Tejedor, 2008; Rosenberger et al., 2009; Rosenberger, 2010). An alternative view, relying most recently on a large craniodental parsimony analysis, characterizes this fossil and several others (see below), as stem platyrrhines, as noted above (Meldrum, 1993; Kay et al., 2008; Hodgson et al., 2009; Kay and Fleagle, 2010). The sole postcranial element that has been attributed to D. gaimanensis is a well-preserved talus (Fig. 1) which appears to bear the closest morphological afﬁnity to Saimiri, Cebus, and Callicebus but looks remarkably primitive in its lack of most conspicuous platyrrhine features (Reeser, 1984; Gebo and Simons, 1987; Ford, 1990a; Meldrum, 1990). Its morphology indicates a generalized function with a preponderance of frequent arboreal quadrupedal activities, and specializations for increased leaping (Gebo and Simons, 1987; Ford, 1990a; 1993 Meldrum, 1993). A generalized positional pattern such as this would have enabled the medium-sized Dolichocebus (1,500 g: Kay et al., 2008) to exploit a particularly diversiﬁed seasonal mosaic habitat, which may have typiﬁed the southern cone of South America during this period (Rosenberger et al., 2009). Southwards, the Pinturas Formation in the northwest of Santa Cruz Province, Argentina, has yielded a relatively diverse collection of fossil NWMs (Fleagle and Tejedor, 2002; Tejedor, 2008). They date from the early Santacrucian SALMA with an age estimate of 17.5–16.5 Ma (Fleagle and Tejedor, 2002; Rosenberger et al., 2009). Two genera are described, Soriacebus and Carlocebus, which both include referred postcranial elements (Table 1). Their morphology has provoked interesting debates over the phylogeny of early platyrrhines. Soriacebus Soriacebus, with an estimated body weight of 1,800 g, is characterized by an anterior dentition and a deep mandibular ramus, which resemble those of living Pitheciinae. It was initially described as having resemblances to Callitrichinae and Pitheciinae (Luchterhand et al., 1986) and then argued to be an early member of the latter group (Rosenberger et al., 1990; Rosenberger, 1992; Tejedor, 2000, 2008). However, its posterior teeth are distinct and other studies again called into question pitheciine afﬁnities, and supported the placement of this genus with others in a stem platyrrhine group including Dolichocebus (Kay, 1990; Kay et al., 2008; Kay and Fleagle, 2010) among others. The single talus (Fig. 2) attributed to S. amenghinorum most resembles those of Pithecia and Alouatta (Meldrum, 1990). Functionally, the low, broad, and moderately wedged trochlea and the short neck partly covered by a distal extension of the trochlea all indicate extensive talocrural movements in multiple planes (Ford, 1988, 1990a; Meldrum, 1990). Therefore, this morphology would be suggestive of arboreal quadrupedal activities with frequent climbing/leaping and even suspensory activities, similar to extant Pithecia (Fleagle and Meldrum, 1988). This repertoire also correlates with body size and the reconstructed diet, which is frugivory, likely specializing on unripe and woody fruit, but without any specialized seed-predator behavior (Rosenberger, 1992; Meldrum and Kay, 1997b; Rosenberger et al., 2009). Whether the similarities in talar morphology between S. ameghinorum and pitheciines indicate phylogenetic afﬁnity or homoplasy, as with aspects of the dentition, remains uncertain. A smaller species of this genus, S. adrianae, has an estimated body weight of 800–900 g (Fleagle, 1990). Younger than S. ameghinorum, it differs only in a few subtle dental traits. A partial calcaneus was recovered from a locality rich in dental remains of S. adrianae and is of appropriate size to be provisionally allocated to this species (Meldrum, 1993). The fossil preserves a very narrow anterior calcaneal facet that stops short of the distal end of the calcaneus. This condition has been associated with an alternating tarsus possessing limited mobility, especially in eversion and plantarﬂexion (Dagosto, 1988), likely associated with more quadrupedal and clinging postures. 3.5 Ka Holocene 6.7 Ka Minas Gerais, Brazil Toca de Boa Vosta, Bahia, Brazil Cueva del mono fosil, Cueva alta, Cuba Long Mile Cave, Jamaica Skeleton cave, Jamaica Several sites on Hispaniola U, F, T H, C, F, A H, U, C, F A A, S, U A A H, U, R, F A A A S, H, R, U, Mc, V, P, C, F, T, Fi, A, Ca, Ta, Mt A A H, U, F, T, A, C H, R, U, Mc, C, F, T, Fi, A, Ca, Ta, Mt H, U, F, A, Ca, Ta Postcranial elements 2,000–5,000 10,000 2,000–5,000 25,000 1,000 850 850 20,000 1,500 2,500 1,800 ? 2,700 ? 1,500 2,000 2,200 BW (g) AQW, CL ATQW CL, SUS CL, SUS AQW AQW, L AQW, L CL, SUS AQW, L AQW, CL AQW, CL AQW, L AQW, L AQW AQW, L AQW, L AQW, L positional behavior Abbreviations are used for postcranial elements (A: talus, C: os coxae, Ca: calcaneus, F: femur, Fi: ﬁbula, H: humerus, MC: metacarpals, MT: metatarsals, P: phalanges, R: radius, S: scapula, T: Tibia, Ta: distal tarsals, U: ulna, V: vertebrae) and for inferred positional behavior (AQW: arboreal quadrupedal walk/run, ATQW: arboreal and terrestrial quadrupedal walk/run, CL: climb and clamber, L: horizontal leaping, SUS: suspensory and brachiation). Antillothrix Paralouatta varonai Xenothrix 20 Ka 13.5–11.8 Ma 13.5-11.8 Ma 13.5–11.8 Ma 20 Ka Aotus dindensis Laventiana Neosaimiri Caipora Protopithecus Sarmiento, Chubut, Argentina Pinturas, Santa Cruz, Argentina Pinturas, Santa Cruz, Argentina Alto Rio Cisnes, Chile Santa Cruz, Santa Cruz, Argentina Domo de Zaza, Lagunitas, Cuba Colon Cura, Neuquen, Argentina La Venta, Madgalena Valley, Colombia La Venta, Madgalena Valley, Colombia 20.0 Ma 17.5–16.5 Ma 17.5–16.5 Ma 16.5 Ma 16.4 Ma 14.7–18.5 Ma 15.8 Ma 13.5-11.8 Ma 13.5–11.8 Ma Dolichocebus Carlocebus Soriacebus Rio Cisnes talus Homunculus Paralouatta marianae Proteropithecia Nuciruptor Cebupithecia La Venta, Madgalena Valley, Colombia La Venta, Madgalena Valley, Colombia La Venta, Madgalena Valley, Colombia Toca de Boa Vosta, Bahia, Brazil Locality Age Fossil TABLE 1. Fossil New World monkeys with known postcranial remains 1994 YOULATOS AND MELDRUM LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES 1995 Fig. 1. Left talus (MACN-CH 362) attributed to Dolichocebus gaimanensis, as seen in dorsal (A), proximal (B), medial (C), plantar (D), distal (E), and lateral views (F). Scale bar equals 0.5 cm. Carlocebus The other NWM from Pinturas is the larger (2,600 g) Carlocebus. Adaptively, the shearing crests of its molars suggest frugivorous habits (Fleagle and Tejedor, 2002). The genus is quite different from Soriacebus, and the more generalized morphology of its teeth suggest similarities to the Callicebus clade (Fleagle and Tejedor, 2002; Tejedor, 2008). Alternately, such morphology could be considered homoplasic or primitive and it is possible that the genus also belongs to an earlier platyrrhine radiation, more closely related to Dolichocebus (Kay et al., 2008; Rosenberger, 2010). 1996 YOULATOS AND MELDRUM verging proximally. There was apparently a strong distal tibioﬁbular syndesmosis extending 15 mm along the distal tibial shaft, indicating a more stable talocrural joint associated with rapid quadrupedal running and/or leaping. A partial calcaneus is also referred to this genus. The posterior articular facet is quite long with a low angle to the long axis of the calcaneus. The anterior facet is very broad and extends to the distal end of the calcaneus. These features are associated with either leaping or suspensory climbing behaviors or a combination of the two (Ford, 1990a). These behavioral patterns are also suggested by the morphology of the fragmented scapula and ulna. The piriform shape of the glenohumeral facet and the angles of the spine with the axillary border and that with the glenoid indicate quadrupedal behavior with enhanced forelimb use, such as climbing and clambering. In addition, the height of the coronoid process, the reduced width of the sigmoid notch, and the moderate olecranon indicate an ulna that works mainly in controlled ﬂexed stances similar to those encountered during climbing and climbing activities (Anapol and Fleagle, 1988). The similarities in the positional behavior of both Soriacebus and Carlocebus, which employ quadrupedal activities along with climbing/clambering behaviors, appear consistent with their reconstructed frugivorous diets and suited to the paleoenvironmental evidence. Pinturas was very likely a mixed habitat, dominated by tropical forests, along with partly forested and watered areas, as well as even drier areas where dune formation could have been feasible (Bown and Larriestra, 1990). SEEDS OF EARLY DIVERSIFICATION Fig. 2. Tali of Pinturas primates. A–D: Referred to Carlocebus cf. carmenensis. E referred to Soriacebus ameghinorum. Postcranially, Carlocebus is known from four wellpreserved tali (Fig. 2) (Meldrum, 1990), distal tibia and partial calcaneus (Meldrum, 1993) and a fragmentary scapula and ulna (Anapol and Fleagle, 1988). None of this material has direct association with craniodental specimens. The general morphoplogy of the tali approximates that of Callitrichinae and small Cebinae. More precisely, they share a moderately low and broad trochlea, a very broad, slightly medially directed talar neck, an oval head in distal view, and a broad shallow posterior calcaneal facet, while the dorsal surface of the trochlea extends onto the talar neck to form a very deep cavity for the tibia. These features rather suggest a mixture of quadrupedal activities with some moderate leaping behavior probably from vertical postures (Meldrum, 1990). In addition, this repertoire could have been supplemented by relatively ample and varied talocrural movements, frequently associated with clambering. An isolated distal fragment of a tibia articulates conformably with the aforementioned tali. The shaft is similar in robusticty to Homunculus. It broadens due to an expansion of the distolateral border, supporting a broad ﬁbular incisure bounded by well-developed crests con- Slightly north and westwards in the southern cone, lies the Chilean site of Alto Rio Cisnes, which has yielded a single primate talus that is currently unassigned and dates to the Friasian SALMA 16.4 Ma (Tejedor, 2003, 2008—Table 1). Generally, the talus bears some similarities to that of Callicebus and to those tali referred to the Miocene Carlocebus, but is smaller, nearer the size of Pithecia. Functionally, the moderately high talar body with the parallel-sided rims, the relatively long neck, and the morphology of the tibial stops and that of the proximal and distal calcaneal facets indicate predominantly arboreal quadrupedal behavior with associated leaping (Gebo and Simons, 1987; Meldrum, 1990). The relationship between the fauna of this site and Santacrucian faunas is not yet well understood (Tejedor, 2003). If the evidence conﬁrms that the fauna from Rio Cisnes is closer in age to the Santacrucian fauna, then the platyrrhine radiation would have been more extensive during that period than previously recognized. Homuncuclus South of the Pinturas site, another fossil platyrrhine has been unearthed from several sites (Rio Gallegos, Corrigüen Aike, Monte Observacion) of Santacrucian age, 16.4 Ma (Tejedor and Rosenberger, 2008). Homunculus patagonicus is a medium-sized NWM (2,700 g) known from partial skulls, mandibular fragments, teeth, and long bones (Bluntschli, 1913, 1931; Meldrum, 1993; Tejedor and Rosenberger, 2008). The overall morphology LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES 1997 Fig. 3. Speculative reconstruction of the skeleton of Homunculus patagonicus. Darkened areas indicate the associated elements of specimen MACN-A 635. Scale bar equals 5.0 cm. of the species is reminiscent of Aotus and Callicebus, and would thus suggest phylogenetic relationships within the clade of Cebidae or Pitheciidae (Fleagle and Tejedor, 2002; Tejedor and Rosenberger, 2008). The dentition is rather primitive (Tejedor, 1997, 2008) and the more advanced morphologies seen in Proteropithecia and later Pitheciinae (e.g., Nuciruptor, Cebupithecia) could have evolved out of a Homunculus-like dentition (Tejedor and Rosenberger, 2008). Functionally, the incisors and premolars indicate hard-fruit eating, while the relatively large cheek teeth suggest an important component of hard fruits and leaves in its diet (Fleagle and Tejedor, 2002; Tejedor and Rosenberger, 2008; Rosenberger et al., 2009). A varied diet probably suits the reconstruction of the paleoenvironments as seasonal habitat with more marginal conditions than a tropical forest, probably resembling the gallery forests along rivers with exten- sive areas of savannas (Bown and Fleagle, 1993; Fleagle and Tejedor, 2002; Tejedor and Rosenberger, 2008; Rosenberger et al, 2009). Limb proportions of Homunculus are similar to modern quadrupedal platyrrhines, such as Aotus and Callicebus (Meldrum, 1993; Tejedor and Rosenberger, 2008). The humerus displays a number of features that suggest climbing behavior, in agreement with the proportionately robust curved radius (Fig. 3). The capitulum is spherical and quite ‘‘unrolled’’ relative to the long axis of the humeral shaft, providing a greater range of ﬂexion and extension (Napier and Davis, 1959; Meldrum et al., 1990). The lateral epicondyle is relatively large (Ford, 1990a), the trochlea is cylindrical and the medial epicondyle has little dorsal angle (Fleagle and Meldrum, 1988). In the robust femur, the great degree of extension of the femoral head and the distally placed fovea are both 1998 YOULATOS AND MELDRUM features of habitually adducted hindlimbs. The greater trochanter is very broad and rugous and overhangs the femoral shaft anteriorly, providing expanded attachment of the vastus lateralis muscle, an extensor of the knee. The ridge of bone on the posterior surface of the proximal femoral neck, and the particularly deep patellar groove, seem to promote rapid for-aft movements of the thigh, necessary during leaping activities (Ford, 1988, 1990a; Meldrum, 1993). Therefore, this medium-sized monkey exhibited a mosaic of locomotor behavior that included quadrupedal walking and leaping, combined with forelimb-assisted climbing. Proteropithecia In northwest Patagonia, in the Province of Neuquen, the Collon Cura formation has yielded Proteropithecia neuquenensis, a medium-sized (1,600 g) platyrrhine known from isolated teeth and a talus (Kay et al., 1998). The site is considerably younger, dating from 15.8 Ma, and the associated fauna is slightly different from the above mentioned Santacrucian, probably from the Colloncuran SALMA (South American Land Mammal Age). The compressed and procumbent lower incisors and the shallow basins and crenulated enamel of the lowcrowned molars indicate strong afﬁnities with Pitheciinae, and Proteropithecia is considered as a basal member of the group. Adaptively, Proteropithecia has a molar structure consistent with fruit- or nut-eating, while its incisors rather suggest seed-eating in much the same manner as extant pitheciins. The talus shows overall resemblances to Aotus and Callicebus. In general, the oval head, the moderate neck, the shallow, narrow, and well-delineated dorsal tibial stop, the high and moderately wedged trochlea, and the extended anterior proximal calcaneal facet are features that are frequently associated with relative stability and enhanced movements to the sagittal plane (Ford, 1988; Meldrum, 1990). Similar functions usually occur during arboreal quadrupedal activities and moderate leaping activities (Kay et al., 1998). Nuciruptor The La Venta region in the Magdalena Valley, Colombia, is the richest fossiliferous Cenozoic localitiy in northern South America. From that region, Nuciruptor rubricae is a medium-sized (2,000 g) fossil monkey that is represented by a mandible and associated teeth (Meldrum and Kay, 1997), and possibly a referable isolated talus. The age of the fossil is estimated at 13.5–11.8 Ma. The morphology of the mandibular corpus and the procumbent and moderately elongate lower incisors and low-crowned molar indicate that it is more derived than Callicebus but more primitive than extant and most other extinct pitheciines (Meldrum and Kay, 1997). It appears to exhibit precisely those intial adaptations of the dentition predicted for the earliest Pitheciinae, that is incisors specialized for opening hard fruit and cheek teeth able to masticate hard seeds (Kinzey, 1992; Meldrum and Kay, 1997). An isolated talus has been excavated in El Cardon Red Beds, a locality immediately adjacent to that of Nuciruptor. The talus is well preserved with superﬁcial erosion of the head, posterior tubercles and calcaneal facets and its size falls within the expected range of this form. Although, allocation of this specimen is not yet settled, the relatively narrow head and neck and the more rounded lateral rim of the trochlea would be suggestive of talocrural movements along the sagittal plane, usually associated with quadrupedal activities with some leaping behaviors (Ford, 1988, 1990a; Meldrum and Kay, 1997). Cebupithecia Another fossil member of the Pitheciinae, which is well represented in La Venta, is Cebupithecia sarmientoi. In effect, Cebupithecia, a medium-sized monkey (1,800 g), is one of the most complete fossil platyrrhines ever found other than the subfossils from the Caribbean and eastern Brazil, with associated cranial, mandibular, dental remains, as well as a partial skelton (Fig. 4; Stirton, 1951; Stirton and Savage, 1951; Davis, 1987; Meldrum and Kay, 1990; Meldrum and Lemelin, 1991; Meldrum, 1993; Hartwig and Meldrum, 2002). The dentition is clearly synapomorphic with the living Pitheciinae, displaying procumbent upper incisors, large projecting canines that are triangular in cross-section, and quadrate molars with poorly developed cusps and crests. On the other hand, premolars appear to be less specialized than in modern forms, and ﬁnally the bunodonty and shallow hypoﬂexids and raised talonids appear even more primitive (Meldrum and Kay, 1997). Thus, Cebupithecia appears to be more derived than Nuciruptor in the direction of living Pitheciinae, with specializations for opening hard fruit and seed predation. Its cheek teeth were also able to masticate hard seeds in a similar manner to extant pitheciins (Meldrum and Kay, 1997). Postcranially, Cebupithecia appears to lack most apomorphic traits of modern Pitheciinae (Fleagle and Meldrum, 1988; Ford, 1990a; Hartwig and Meldrum, 2002). Its limb proportions fall within the range of monkeys that are mainly quadrupedal and use moderate amounts of leaping, such as the cebines and Callicebus (Meldrum and Lemelin, 1991; Hartwig and Meldrum, 2002). The humerus is characterized by a large lateral epicondyle, a sharp trochleo-capitular ridge and a narrow and deep biccipital groove. These features are frequently associated with controlled movements at the sagittal plane as during quadrupedal activities (Ford, 1988; Meldrum et al., 1990). The femur shows a marked posterior ridge at the femoral neck and the head extends on the superior part of the neck, while the trochlea is high and well demarcated, features that are usually associated with leaping habits (Davis, 1987; Ford, 1990a; Meldrum, 1993). The distal tibia shows a markedly concave trochlear surface coupled with large inferior projections of the anterior and posterior trochlear margin. These traits are associated with a strongly curved and deeply grooved astragalar trochlea with sharp medial and lateral crests and a distal deep extension on the talar neck. They suggest a relatively stable ankle joint adapted for quick pivots as during leaping (Ford, 1990a). Therefore, Cebupithecia appears to have been a medium-sized quadrupedal monkey with increased rates of leaping behavior (Hartwig and Meldrum, 2002), probably not as frequently exhibited as in modern P. pithecia but more likely comparable with the other members of the subfamily. 1999 LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES Fig. 4. Reconstruction of the composite skeletal anatomy of Cebupithecia sarmientoi. Darkened areas indicate preserved portions of the skeleton. Scale bar equals 5.0 cm. TABLE 2. Percentages of major locomotor modes of extant Pitheciidae (QWR, arboreal quadrupedal walk, bound, run; CL, clamber, vertical climb; L, leap, drop, hop; S, bridge and suspensory locomotion) Species Pitheciinae Pithecia pithecia Pithecia pithecia Pithecia monachus Chiropotes satanas Chiropotes satanas Cacajao calvus Callicebinae Callicebus cupreus Callicebus brunneus Callicebus torquatus Site QWR CL L S Lago Guri, Venezuela Raleighvallen-Voltzberg, Surinam Yasuni, Ecuador Lago Guri, Venezuela Raleighvallen-Voltzberg, Surinam Lake Teiu, Brazil 25.6 25 46.8 41.2 80 39.9 21.8 5 22.9 20.4 2 25.2 52.6 70 28.4 36.2 18 33.8 _ _ 1.9 2.2 _ 1.1 Yasuni, Ecuador Manu, Peru Estacion Biologica Callicebus, Peru 54.1 49.3 66.9 26.7 12.4 9.2 17.7 38.3 23.9 1.5 _ _ Extant Pitheciinae Modern Pitheciinae exhibit a regular repertoire where both quadrupedal activities and leaping behavior are the dominant positional categories (Table 2). Among them, Pithecia appears to be the most saltatory, and more particularly P. pithecia, where almost half of its repertoire is represented by different forms of horizontal leaps and hops (Fleagle and Mittermeier, 1980; Walker and Ayres, 1996). This is further evident in the postcranial morphology of the species, with functional traits that favor stability, restricted mobility to the sagittal plane and resistance to high loads (Fleagle and Meldrum, 1988; Ford, 1988, 1990). In contrast, P. monachus seems to be more quadrupedal (Youlatos, 1999), and this is reﬂected in its postcranial morphology as well (Meldrum and Lemelin, 1991; Meldrum and Kay, 1997), underscoring the postcranial and positional ﬂexibility of the genus (Walker, 1993). Cacajao also appears to use leaps rather frequently, but quadrupedal activities involving both walking, climbing, and clambering are more dominant (Walker and Ayres, 1996). This is also true for Chiropotes (Fleagle and Mittermeier, 1980; Walker and Ayres, 1996). Study of the postcranial morphology of this genus has revealed functional traits that are associated with frequent above branch quadrupedal walking and running, and some suspensory postures (Fleagle and Meldrum, 1988). The other member of this family, Callicebus, which represents the basal member of this clade, is basically quadrupedal with variable, but generally moderate, rates of leaping behavior (Table 2—Youlatos, 1999; Lawler et al., 2006). A noteworthy positional behavior of the larger Pitheciinae is hindlimb suspension, involving extreme plantarﬂexion and inversion of the ankle, and bracing with the tail in Chiropotes (Fig. 5—Fleagle and Meldrum, 1988; Meldrum, 1998). This reﬂects the occasional 2000 YOULATOS AND MELDRUM in order to comprehend other trends of ecological morphology within this radiation. ACTIVE FORAGERS The Miocene paleocommunity of La Venta also include several fossils representing the Cebinae, for which, however, few postcranial remains are known. These include the well-represented genera Neosaimiri and Laventiana (Hartwig and Meldrum, 2002; Tejedor, 2008). In addition, we also consider here Aotus dindensis, if night monkeys actually form an integral part of the Cebidae (e.g., Schneider et al., 1993, 1996; Horovitz et al., 1998; Opazo et al., 2006; Kay et al., 2008), and not of the Pitheciidae (e.g., Ford, 1988; Rosenberger, 1992, 2010; Tejedor, 2008). Neosaimiri Fig. 5. Chiropotes satanas demonstrating hind-limb suspension with tail bracing. climbing and suspensory behaviors reﬂected in the knee and ankle, and conﬁrm their intermediate position between the medium-sized generalized Cebinae and the large-bodied suspensory Atelidae (Meldrum, 1990). Considering the reconstructed positional behavior of fossil Pitheciinae with those behaviors for extant forms, we observe a consistent pattern of quadrupedal walking– running–bounding behavior with some variable component of leaping and hopping activities. All fossil forms tend to exhibit a pattern resembling Callicebus and Chiropotes positional behaviors, quadrupedalism accompanied by some leaping. If Callicebus represents in some form the postcranial prototype of ancestral platyrrhines in its positional behavior (Ford, 1988), then all these forms do not appear to have changed much since the inception of the pitheciine radiation. Within this radiation, only Pithecia, and more particularly, P. pithecia (as there are limited data for other species), departs far from this blueprint. Cacajao also differs, since it evolved in Amazonian ﬂooded forests with quite discontinuous canopies (Walker and Ayres, 1996). Additional data on the positional behavior of other pitheciins are required Neosaimiri ﬁeldsi is a relatively small platyrrhine (850 g) from the middle Miocene strata of La Venta, with obvious afﬁnities to modern Saimiri. This form is known from several mandibles, many isolated teeth, as well as an array of postcranial material (Meldrum et al., 1990; Takai, 1994; Nakatsukasa et al., 1997). The dentition resembles closely Saimiri in the shape and proportions of the molars and crowns of other teeth (Takai, 1994), which seemed to support the proposal set out by Rosenberger et al. (1991a) for synonomy within Saimiri. However, several differences in the upper incisors, premolars and the third molar stand out as either autapomorphies, or synapomorphies with Cebus (Takai, 1994; Tejedor, 2008). Furthermore, Kay and Meldrum (1997) on the basis of dental and mandibular morphology advocated recognition of Neosaimiri, and it is to this position we subscribe. In terms of postcranial morphology, Neosaimiri, as reviewed by Nakatsukasa et al. (1997), is characterized by more rugose muscular markings indicating a more heavily built monkey than its modern relative. In addition, it possesses a high humeral head, a distinct distal humeral articular surface, a long olecranon process, a very robust femoral neck, a narrow and deep femoral patellar groove, a smaller anterior process of the distal tibia, an absence of a distal surface extension on the anterior tibial shaft, an absence of an anterior midtrochlear depression of the talus, and a short distal calcaneus relative to the calcaneal tuberosity. This suite of distinguishing features indicates a dominant forelimb in quadrupedal progression, a less stabilized upper ankle joint, and a shorter power arm for plantar ﬂexion. On the basis of such functions, Neosaimiri would have been an arboreal quadruped employing frequent horizontal leaps across gaps in a forested environment. Laventiana Laventiana annectens is a taxon very closely related to Saimiri (Rosenberger and Setoguchi, 1991) and is often considered as a junior synomym of Neosaimiri (Takai, 1994; Meldrum and Kay, 1997) or congener of Neosaimiri (Kay and Meldrum, 1997). In La Venta, it is represented by a rather complete mandible (Rosenberger et al., 1991c), a talus (Gebo et al., 1990), and a distal tibia (Meldrum, 1993). Its molars exhibit a buccal LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES 2001 nberger, 1987). It was represented originally by a mandible, fragmentary maxilla, and possibly an isolated talus, but other material has since been added (Takai et al., 2001). The morphology of the dentition is very similar to modern Aotus, with slight differences in the incisors and the less elevated premolar trigonids. The general morphology of the talus has been compared with that of Aotus and Callicebus (Gebo et al., 1990). Alternately, comparisons have been made to the talar morphology of the Callitrichinae (Meldrum, 1993). Functionally, the large head, the wide and short neck, the moderate height of the square-shaped trochlea, the comparably shallow groove, the rounded medial trochlear crest, and the more obliquely facing tibial malleolar cup are a combination of features that enable arboreal quadrupedal movements of the foot with no indications for extensive climbing or leaping (Gebo et al., 1990; Meldrum, 1993). Extant Cebinae Fig. 6. Distal tibia and talus of IGM 250436 (A) and IGM-KU 8803 (B) referred to Laventianna annectens, compared with corresponding elements of Saimiri sciureus (C), Scale bar equals 1.0 mm. cingulid and a distinct postentoconid notch, proposed as a signiﬁcant autapomorphy, but variably present in Neosaimiri and Saimiri. The overall morphology of the talus is most similar to living Cebinae (Fig. 6). It bears a moderately long talar neck, a high and relatively short and wide talar body, and a narrow talar head (Gebo et al., 1990). The distal tibia is also most similar to Saimiri. Of particular note is the indication of a well-developed syndesmosis of the distal tibioﬁbular joint. The posterior surface of the tibia is quite ﬂat and the lateral border is marked by a pronounced ridge, along which the ﬁbula would be appressed, as in Saimiri and several other platyrrhines including Aotus, Callithrix, Cebuella, and Pithecia. Only Saimiri commonly displays the distinctive combination of mediolateral widening and posterior ﬂattening of the distal tibial shaft (Meldrum, 1993). This morphology appears to facilitate quadrupedal activities with high rates of leaping behavior within an arboreal context. Aotus Aotus dindensis is relatively small-bodied (1,000 g) and dates from 13.5 to 11.8 Ma (Setoguchi and Rose- There is a strong bias in the study of positional behavior of capuchin and squirrel monkeys over owl monkeys. Thus, there are no detailed data on the locomotion and postures of Aotus; not surprisingly, as it is mainly nocturnal. Anecdotal descriptions and predictions from postcranial traits suggest a mainly quadrupedal primate with moderate leaping activities (Wright, 1989). This is also supported by postcranial similarities with Callicebus (Ford, 1988), which exhibits such positional patterns. If this is true, there appears to be little change within this clade since the Miocene, as A. dindensis from La Venta, is reconstructed to exhibit similar behaviors. On the other hand, data on three Saimiri species are available and all show primarily quadrupedalism, with variable rates of leaping behavior (Table 3). S. sciureus seems to be the more saltatorial of the studied species (Fleagle and Mitteremeier, 1980; Youlatos, 1999). S. boliviensis also uses considerable leaping, but is mainly quadrupedal (Fontaine, 1990), while S. oerstedii exhibits more frequent quadrupedalism than other species of squirrel monkeys (Boinski, 1989). This positional proﬁle seems to agree with the predacious frugivory of squirrel monkeys that range in many forest types exploiting all forest strata (e.g., Janson and Boinski, 1992; Rosenberger, 1992). However, these reported variations may result from differing sampling methodologies or habitat differences. If both fossil relatives of Saimiri from the Miocene, Neosaimiri and Laventiana, are reconstructed as quadrupedal leapers, then they perhaps most approximate S. sciureus in positional patterns, and coincidentally, the extant range of the latter covers the La Venta site in Colombia. Thus there appears to be no signiﬁcant changes in locomotor behavior since the Miocene within this clade, as within the Aotus lineage. Concerning Cebus, modern species appear to be rather consistent in their patterns (Table 3). The four species for which data are available indicate increased quadrupedal activities, coupled with variably signiﬁcant rates of leaping and variably moderate climbing/clambering (Fleagle and Mittermeier, 1980; Gebo, 1992; Youlatos, 1998; 1999; Garber and Rehg, 1999; Wright, 2007; Bezanson, 2009). These behaviors seem to suit the adaptive proﬁle of this generalist genus as a particularly 2002 YOULATOS AND MELDRUM TABLE 3. Percentages of major locomotor modes of extant Cebidae: the Cebinae (QWR, arboreal quadrupedal walk, bound, run; CL, clamber, vertical climb; L, leap, drop, hop; S, bridge and suspensory locomotion) Species Saimiri oerstedii Saimiri sciureus Saimiri sciureus Saimiri boliviensis Cebus capucinus Cebus capucinus Cebus capucinus Cebus albifrons Cebus apella Cebus apella Cebus apella Cebus olivaceus Cebus olivaceus Site QWR CL L S Corcovado, Costa Rica Yasuni, Ecuador Raleighvallen-Voltzberg, Surinam Monkey Jungle, U.S.A. Santa Rosa, Costa Rica La Suerte, Costa Rica La Suerte, Costa Rica Yasuni, Ecuador Nouragues, French Guiana Iwokrama, Guyana Raleighvallen-Voltzberg, Surinam Nouragues, French Guiana Iwokrama, Guyana 88.1 45.1 55 73 55 60.8 78.1 48.5 33.9 53 84 32.5 50 4.5 24.2 3 5 26 9.9 13.2 17.7 29.2 12 5 30.8 11 7.4 25.4 42 20 15 25.9 5.0 27.3 23.6 26 10 26.7 32 _ 5.3 _ 2 4 3.4 3.7 6.5 13.3 9 1 10.0 7 TABLE 4. Percentages of major locomotor modes of extant Cebidae: the Callitrichinae (QWR, arboreal quadrupedal walk, bound, run; CL, clamber, vertical climb; L, leap, drop, hop; CC, clawed locomotion) Species Saguinus fuscicollis Saguinus fuscicollis Saguinus tripartitus Saguinus labiatus Saguinus geoffroyi Saguinus midas Saguinus midas Saguinus mystax Saguinus mystax Leontopithecus chrysomelas Leontopithecus chrysomelas Leontopithecus rosalia Callimico goeldii Cebuella pygmaea Callithrix jacchus Site QWR CL L CC Catuaba, Brazil Rio Blanco, Peru Yasuni, Ecuador Catuaba, Brazil Barro Colorado, Panama Nouragues, French Guiana Raleighvallen-Voltzberg, Surinam Rio Blanco, Peru Padre Isla, Peru London Zoo, UK Edinburgh Zoo, UK Washington Zoo, USA Catuaba, Brazil Yasuni, Ecuador Rio de Janeiro, Brazil 38 47.6 40.3 49 43.3 32.5 76 51.6 61.5 51.3 60.2 44 18 27.1 32 6 12.4 10.4 9 7.4 28.7 _ 12.0 6.3 0.9 1.5 15 4 5.8 13 38 32.5 33.7 37 41.5 26.5 24 30.9 27.4 31.9 23.2 23 62 24.4 23 18 6.3 15.6 5 7.7 12.1 _ 4.3 4.8 15.9 15.1 15 16 42.7 32 agile and destructive omnivore which exploits all forest strata, ground included, in a remarkable variety of habitats, resulting in nearly one of the most expanded geographical range among all NWMs (Janson and Boinski, 1992; Rosenberger, 1992). There are no pertinent fossils with associated postcranial elements in order to directly assess evolutionary trends within this clade. It is, however, safe to infer that these medium-sized taxa have preserved a largely generalized positional behavior. ‘‘DWARVES AND CLAWS’’ Fossils such as Mohanamico, Patasola, Micodon, and Lagonomico, from the middle Miocene La Venta locality, have been related to the callitrichine radiation, although debates about the exact phylogenetic relationships of some of them (e.g., Mohanamico and Lagonomico) have not been fully resolved yet (Rosenberger et al., 1990; Kay, 1994; Kay and Meldrum, 1997; Rosenberger, 2002; Tejedor, 2008). This radiation is characterized by shared derived features that are related to their small size and concern understory, trunk, and ground use, large and vertical branch use, squirrel-like locomotion using laterally compressed claw-like nails, and dependence on exudates and arthropods (Ford, 1980; Garber, 1992; Garber et al., 1996). These forms are known solely from cranial, mandibular, and dental material with no associated postcranial elements thus far recovered. Extant Callitrichinae Neontological evidence of behavior and foraging patterns suggest different evolutionary patterns within the callitrichines. Molecular systematists, whose cladistic model is followed here, place Saguinus as as the most basal member of this clade (e.g., Wildman et al., 2009 and references cited therein). Several species of this genus intensively use quadrupedal walking and bounding coupled with high rates of leaping, which basically consist of horizontal leaps between terminal branches (Table 4; Garber, 1980, 1991; Garber and Preutz, 1995; Youlatos, 1999; Garber and Leigh, 2001; Youlatos and Gasc, 2001). These positional patterns indicate that tamarins still exploit the small-branch milieu to a great degree while being one of the most ecologically generalized of the large-branch feeders. Their lesser dependence on gums, by comparison with marmosets, is also correlative with the generally low rates of claw-climbing and clinging on large vertical supports (Table 4). The callimico/marmoset radiation was the subject of a recent extensive study (Ford et al., 2009). Callimico is LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES very specialized postcranially, especially in the hind limbs and ankle joint, which are designed to facilitate increased leaping by providing the necessary mechanical advantage and required stability for load resistance (Ford, 1988; Garber and Leigh, 2001; Davis, 2002; Garber et al.; 2005, 2009). Behaviorally, callimicos exhibit particularly high rates of leaping, most of which are vertical leaps (Garber et al.; 2005, 2009), while quadrupedalism, climbing and clawed locomotion are used in a lesser degree (Garber and Leigh, 2001). These patterns appear to be ecologically associated with the exploitation of the lower forest strata with abundant vertical supports, where they frequently forage for arthropods and collect fruit and fungi (Porter and Garber, 2004). The marmosets, Cebuella and Callitrhix, are by far the most ecologically specialized callitrichines; they exploit large vertical branches in relation to their tree gouging habits and year-round exudate feeding (Garber, 1992). This is complimented by their locomotor patterns and associated morphology (Table 4; Davis, 2002; Ford and Davis, 2009). Cebuella exhibits very high rates of claw-climbing and clinging on large vertical supports as well as frequent leaping, including high rates of vertical leaps (Youlatos, 1999, 2009). Unfortunately, there are no detailed data on the locomotion of Callithrix, apart from a study in the Jardim Botanico of Rio de Janeiro, where C. jacchus emphasized clawed locomotion, used similar rates of quadrupedal walking and bounding, as well as rather frequent leaps, of which a signiﬁcant proportion were short (Zaluar et al., 2010). On the other hand, Leontopithecus, is quite specialized in its own way, having evolved in the different forests of Mata Atlantica (e.g., Hershkovitz, 1977; Garber, 1992; Rosenberger et al., 2009): the long and slender upper forelimbs with especially elongated digits III and IV, the claw-like nails, and the enlarged incisors indicate an adept manipulative forager for both non-mobile prey and fruit, as well as seasonal dependence on exudates gleaning (Garber, 1992). Unfortunately, there are no data for Leontopithecus in the wild, but the few studies in zoos suggest reliance on quadrupedal activities coupled with leaping behavior (Stafford et al., 1994; Karantanis, 2010). Similar positional patterns would facilitate and suit the intensive manipulative exploitation of the discontinuous canopy of all forest levels that lion tamarins generally exploit. These data indicate different positional strategies across the different clades of the Callitrichinae. The widespread combination of quadrupedalism and leaping suggests this as the pattern of the common ancestor of the group, most likely shared by the other members of the Cebidae. In effect, leaping behavior is present in all callitrichine clades, but extensive use of vertical leaping is only common in Callimico and marmosets. Quadrupedalism is signiﬁcantly reduced in Callimico and Cebuella, most likely for different reasons. Finally, clawed climbing and clinging, although used in variable rates across the subfamily, tends to be particularly important in Callitrhix and Cebuella, genera highly dependent on exudate feeding. 2003 ecological features, particularly adapted to below-branch suspensory behaviors made possible by such features as fully prehensile tails (e.g., Erikson, 1963; Rosenberger and Strier, 1989; Strier, 1992). Their early fossil record is relatively scant compared to other clades. The middle Miocene Stirtonia from La Venta locality (13.5–11.8 Ma), Colombia (Kay et al., 1987) is the earliest representative of this clade, followed by the late Miocene Solimoea from Solimoes formation (9–6.8 Ma) Acre, Brazil (Kay and Cozzuol, 2006). There are no postcranial elements representing these early atelid forms. In stark contrast, younger examples from the late Quaternary consist of two remarkably complete skeletons of Pleistocene atelids from Brazil: Protopithecus brasiliensis and Caipora bambuiorum. Their age is 20,000 BP (see Rosenberger et al., 2009). Protopithecus Protopithecus brasiliensis is the largest fossil NWM (25,000 g) and was discovered in cave deposits in Minas Gerais and Toca da Boa Vista, Bahia (Hartwig and Cartelle, 1996). The fossil is known by a virtually complete skull and skeleton and bears a unique mixture of traits, including several derived characters shared by all atelids. The skull shows many morphological similarities to Alouatta that could be ulitmately related to the presence of an enlarged hyoid bone, but it lacks the usual specializations for folivory found in the dentition of howler monkeys (Hartwig and Cartelle, 1996). Actually, it is very likely that Protopithecus was primarily a frugivore unlike Alouatta, which is highly folivorous (Rosenberger et al., 2009). The postcranial skeleton of Protopithecus is much more robust than in other Atelidae, probably due to its large size. It is most similar to the suspensory Atelinae (i.e., Ateles and Brachyteles), with traits indicatve of ‘‘brachiating’’ adaptations (Hartwig and Cartelle, 1996), as opposed to Alouatta, which is more quadrupedal. This is evident in the high intermembral index, low and wide humeral trochlea, short ulnar olecranon process, and the shape of the radial head (Hartwig and Cartelle, 1996). This combination of cranial vs postcranial features poses a dilemma for determining its phylogentic relationships within the family. Hartwig and Cartelle (1996) proposed that Protopithecus is the sister taxon to Alouatta, while Fleagle (1999) argued that it is related to the Atelinae. Jones (2008) likewise proposed two possible outcomes, based on character trends related to brachiation within this group. In her view, if Protopithecus is the sistertaxon of Alouatta, there was less change towards an energy-maximizing strategy in the stem atelin lineage, the last common ancestor of atelins is less Ateles-like, and the energy-maximizing strategy would have evolved in parallel in the Protopithecus, Ateles, and Brachyteles terminal lineages. In contrast, if Protopithecus is the sister taxon of the Atelinae, there are many more parallelisms along the individual evolutionary branches (Jones, 2008). Caipora HEAVY WEIGHT CLIMBERS The members of the Atelidae are the largest NWMs and share a set of unique morphological, behavioral and Caipora bambuiorum is another large NWM (20,000 g) recovered from Toca da Boa Vista, Bahia, and is represented by a second nearly complete skull and skeleton 2004 YOULATOS AND MELDRUM TABLE 5. Percentages of major locomotor modes of extant Atelidae (QWR, arboreal quadrupedal walk, bound, run; CL, clamber, vertical climb; L, leap, drop, hop; S, bridge and suspensory locomotion)s Species Alouatta caraya Alouatta caraya Alouatta paliatta Alouatta paliatta Alouatta seniculus Alouatta seniculus Alouatta seniculus Alouatta seniculus Alouatta seniculus Ateles geoffroyi Ateles geoffroyi Ateles geoffroyi Ateles paniscus Ateles paniscus Ateles belzebuth Lagothrix lagotricha Lagothrix lagotricha Site QWR CL L S ENSC, Alegrete, Brazil Estancia Casa Branca, Brazil La Suerte, Costa Rica La Paciﬁca, Costa Rica Raleighvallen-Voltzberg, Surinam Nouragues, French Guiana Yasuni, Ecuador Tiputini Biodiversity Station, Ecuador Fundo Pecuario Masaguaral, Venezuela Barro Colorado, Panama Barro Colorado. Panama Tikal, Guatemala Raleighvallen-Voltzberg, Surinam Nouragues, French Guiana Yasuni, Ecuador Yasuni, Ecuador Colombia 41.5 66.4 81.7 47 80 37.3 50.9 30.1 32.8 22.0 51.1 52 25.4 20.1 20.8 28.9 41.8 29.3 18.6 7.9 37 16 43.9 28.0 57.6 57.1 24.2 6.1 19 17.0 28.1 37.9 44.5 38.8 16.8 2.7 3.2 4 4 2.8 2.4 1.7 5.7 10.9 23.5 1 4.2 2.6 2.8 3.9 10.8 12.5 12.3 7.1 13 _ 16.0 18.4 10.6 4.2 30.3 10.9 29 47.2 43.0 35.8 22.7 8.6 (Cartelle and Hartwig, 1996). Caipora appears to be most similar to Ateles in cranial morphology, with a large, rounded braincase and the quadrate, bunodont, low-cusped molars. The postcranium is very robust, probably due to its large size, but the overall morphology is reminiscent of the suspensory Atelinae and exhibits brachiating locomotor adaptations (Cartelle and Hartwig, 1996). This is apparent in the high intermebral index, the large globular humeral head, the short olecranon process, the round radial head and its ulnar facet, and the overall morphology of the metacarpals and metatarsals (Cartelle and Hartwig, 1996; Jones, 2008). It is still unknown how these fossil forms attained similar sizes in the Brazilian forests, where they were recovered (Rosenberger et al., 2009). The morphology of these recent fossil forms, which are so closely related to the modern taxa, are certain to shed a bright light on the evolution of positional behavior in Atelidae once the material is extensively studied. Extant Atelidae Alouatta encompasses the smallest, as well as some of the largest, species among the atelids. Howler monkeys appear to have differentiated earlier than the other forms and their locomotion is characterized by a preponderance of quadrupedalism. This involves both horizontal or inclined quadrupedal walking and clambering, limited forelimb suspension, and especially tail-assisted hindlimb suspension during feeding postures (Table 5; Fleagle and Mittermeier, 1980; Schön Ybarra and Schön, 1987; Gebo, 1992; Bicca Marques and Calegaro Marques, 1998; Youlatos and Gasc, 2001; Youlatos, 2004; Prates and Bicca Marques, 2008; Bezanson, 2009; Guillot, 2009). Of the studied species, A. seniculus appears to be the one that exhibits more suspensory and much more clambering/climbing activities (Table 5). These distinctions may be related to the varied habitats that this wide-ranging species exploits. The remaining three extant genera show a gradient of increasing degrees of suspensory locomotion, with two caveats: (a) there are limited data on the positional behavior of Brachyteles, although anecdotal observations coupled with an array of major forelimb traits, indicate increased forelimb suspension similar to the welldescribed tail-arm brachiation of Ateles (Rosenberger and Strier, 1989; Strier, 1992; Jones, 2008); and, (b) performance of suspended locomotion may be quite different among the genera, as was documented by Cant et al. (2003) for Lagothrix and Ateles (see also Lockwood, 1999). As the Atelinae evolved, they apparently became larger in body mass and more suspensory in order to forage more efﬁciently and cover more distances in search of sparsely dispersed food sources (Erikson, 1963; Jones, 2008). Tail-assited forelimb suspension is a remarkable locomotor specialization that greatly facilitates canopy travel by these large platyrrhines. Ateles is considered the sister taxon of Lagothrix and Brachyteles (Meireles et al., 1999; but see Collins, 2004), and apparently differentiated rapidly from the stem atelin group by pursuing this forelimb-dominated suspensory locomotion and postures (Table 5; Mittermeier, 1978; Cant, 1986; Fontaine, 1990; Youlatos, 2002; Cant et al., 2001; 2003). Subtle differences in locomotion among the species of spider monkeys do exist (e.g., A. paniscus is the most suspenory species while A. geoffroyi the least; Table 5), but it is difﬁcult to assess any correlations with habitat or phylogenetic/eco-morphological parameters (Youlatos, 2008). If Brachyteles and Lagothrix are indeed sister-taxa, it suggests that the Ateles-like forelimb-dominated suspensory locomotion evolved in parallel in Brachyteles, in the distinct Mata Atlantica, while Lagothrix assumed a different regime of frugivory-animalivory, coupled with a different locomotor proﬁle involving relatively high rates of quadrupedalism and climbing/clambering activities (Table 5; Deﬂer, 1999; Cant et al., 2001). This is also reﬂected in the postcranium of this genus, which differs signiﬁcantly from that of more suspensory Ateles and Brachyteles (Erikson, 1963; Jones, 2008). ISLAND DISPERSALS Currently there are no nonhuman primates living on the Caribbean islands. However, at least four different genera have been unearthed from Pleistocene to Holocene strata of three different islands: Paralouatta from Cuba, Antillothrix and Insulacebus from Hispaniola, and LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES Xenothrix from Jamaica (Cooke et al., 2011). The colonization of these islands by primates is potentially set prior to the middle Miocene, due to a single talus apparently of that age from Cuba (see Iturralde Vinent and MacPhee, 1999; MacPhee and Horovitz, 2002; Rosenberger et al., 2009). Colonization would have taken place either via overwater dispersal, probably by rafting (Ford, 1986; 1990b) or over a large, short-lived landbridge which connected mainland South America, Cuba, Hispaniola, Puerto Rico, and the Lesser Antilles (Iturralde Vinent and MacPhee, 1999). Whether there was a single primate colonization event (Horovitz and MacPhee, 1999; MacPhee and Horovitz, 2002), or multiple (Rosenberger; 2002; Rosenberger et al., 2011) remains uncertain. In either case, these forms underwent remarkable specialization, leading to some rather unique endemic forms for which the phylogenetic relationships remain contested. Some authors propose that all these fossils form a monophyletic group which is the sister taxon of Callicebus (Horovitz and MacPhee, 1999; MacPhee and Horovitz, 2002), while others advocate a more complex biogeography: a pitheciine or Aotus afﬁnity for Xenothrix (Rosenberger, 1977; Tejedor, 2008), cebine afﬁnities for Antillothrix (MacPhee and Woods, 1982; Rosenberger et al, 2011), and alouattine associations for Paralouatta (Rivero and Arredondo, 1991; Rosenberger, 2002). Paralouatta The earliest primate fossil in the Greater Antilles is Paralouatta marianae from the Cuban Miocene (14.68– 18.5 Ma) site of Doma de Zaza, known from a single talus (MacPhee et al., 2003). The specimen is characterized by a nonwedged trochlea, a long, slightly deviated neck, a large head, and wide and extended calcaneal facets, suggesting mid-tarsal mobility that is usually associated with arboreal quadrupedal habits (MacPhee and Meldrum, 2006). The geological evidence, and the presence of some marine fauna, indicates that the site lay along the banks of the sea where several depositional environments were present (MacPhee et al., 2003). Paralouatta varonai, from the Holocene of Cuba is the largest monkey (9,000–10,000 g) from the Antilles, as large as any living platyrrhine. It is known from a wellpreserved skull, several mandibles, isolated teeth and numerous postcranial elements (Horovitz and MacPhee, 1999; MacPhee and Horovitz, 2002; MacPhee and Meldrum, 2006). The skull exhibits a lack of cranial ﬂexion, the face projects upward with somewhat large orbits, and the braincase is long and low, relatively large with strong temporal and nuchal crests (Horovitz and MacPhee, 1999). The canine is very small and the cheek teeth are crested and wear down in a conspicuously ﬂat fashion, indicating thick enamel (Horovitz and MacPhee, 1999; Rosenberger et al., 2009). The suite of postcranial characters of Paralouatta is not seen in other platyrrhines, but it exhibits intriguing resemblences to certain so-called semiterrestrial Old World monkeys. These traits favor limb movements relatively restricted to the sagittal plane, some resistance to high reaction forces and overall stability of the joints. Morphologies reﬂecting this in the fossil include the retroﬂexed medial epicondyle, the narrow trochlea and the deep olecranon fossa in the humerus, the robust and 2005 straight ulna with a narrow proximal sigmoid notch that does not ﬂare laterally, the short-necked radius with a proximal biccipital tubrosity, the marked and relatively deep patella groove of the femur, the massive tibial medial malleolus with an extended distal ﬁbular facet, the nonwedged talar trochlea and the short, straight and relatively robust metapodials and phalanges (MacPhee and Meldrum, 2006). Xenothrix Xenothrix was a Pleistocene, medium to large-sized primate (2,000–5,000 g) known from several cranial, dental and postcranial elements found in six different caves in Jamaica. The relatively short length of the humerus, wide and shallow biccipital groove, comparably broad and distolaterally extensive capitulum, and the moderately prominent trochlear lips indicate ample quadrupedal movements in an arboreal habitat (MacPhee and Fleagle, 1991; MacPhee and Meldrum, 2006). Similar adaptations are also evident in the ulna, with a relatively short olecranon, a proximally wide sigmoid facet and well-deﬁned radial notch. In contrast, humeral features such as the deep olecranon fossa and short, and posteriorly directed medial epicondyle indicate more restricted quadrupedal activities, but these can also be related to the relatively large size of the animal (MacPhee and Fleagle, 1991; MacPhee and Meldrum, 2006). In the femur, the size and conformation of the greater and lesser trochanters, the short, anteriorly convex diaphysis, exceptionally robust shaft, large and anteroposteriorly compressed distal epiphysis, shallow and wide patellar groove, and asymmetry of the condyles indicate controlled movements in various planes, suggesting cautious clambering activities (Ford, 1990a,b; MacPhee and Fleagle, 1991; MacPhee and Meldrum, 2006). This is also consistent with tibial morphology with large and wide tibial plateau, prominence of the tibial tuberosity, and the depth of evident muscle scars that suggest powerful extension and ﬂexion of the leg at the knee (MacPhee and Fleagle, 1991). Antillothrix Antillothrix bernensis was a medium to large-sized primate (2,000–5,000 g) recovered from several Pleistocene sites in Hispaniola. Two relatively complete skulls have been allocated to the species, as well as some teeth, isolated postcranial fragments, and a partial skeleto, with its skull, presenting long bones, ribs, and vertebrae (MacPhee and Horovitz, 2002; Tejedor, 2008; Rosenberger et al., 2011; Kay et al., 2011). Rosenberger (2002) and Rosenberger et al. (2011) conclude afﬁnities to extant Cebinae. Others have proposed close relationship to the Cuban Paralouatta, which together constitute the sister group to Xenothrix (Horovitz and MacPhee, 1999; MacPhee and Horovitz, 2002). A second newly discovered skull has been interpreted as a stem platyrrhine, unrelated to any of the living families of NWMs (Kay et al., 2011). Several points of interest have been observed on the isolated postcranials. The tibia displays a central position for a rather deep ﬁbular facet, anterior and posterior trochlear borders extending inferiorly equally, and a narrowed medial malleolus, all of which are suggestive 2006 YOULATOS AND MELDRUM of sagittally oriented limb movements, that is, rapid arboreal quadrupedalism and leaping (Ford, 1986, 1990a; MacPhee and Meldrum, 2006). Kay et al. (2011) note an undescribed distal humerus fragment associated with teeth attributed to Antillothrix resembling that of a typical platyrrhine arboreal quadruped. On the other hand, recently described associated femur and ulna are anatomically distinctive, suggesting quadrupedal and climbing/clambering habits (Rosenberger et al., 2011). On the basis of cranial shape of one recently recovered skull, others have proposed a locomotor pattern probably similar to modern Alouatta (Kay et al., 2011). ADAPTIVE RADIATIONS AND THE DIVERSIFICATION OF LOCOMOTOR PATTERNS IN PLATYRRHINES The above review of the locomotor behaviors reconstructed for fossil platyrrhines and those of modern taxa, reveals a remarkable diversity among NWMs. This diversity appears to be differentially distributed among well-deﬁned divergent clades of extant genera, but with possible examples of convergence in some fossil taxa. Behaviorally, it can be interpreted in two ways: one concerns the postcranial adaptations correlated with body size and substrate grain, both relative and absolute, that promoted speciﬁc locomotor patterns within well-established lineages; the other concerns the way these locomotor patterns promote niche partitioning of food resources within speciﬁc assemblages through space and time. However, these two views are not mutually exclusive (Rosenberger et al., 2009). Locomotion is one of the principal links between morphology, ecology, and phylogeny and has been shaped through microhabitat utilization within speciﬁc contexts. Assuming platyrrhine monophyly, we might ask what was the original blueprint that gave rise to this notable pattern of locomotor diversity encountered today among the varied Central/South American habitats. On the basis of a comprehensive analysis of the postcranium of both extant and fossil platyrrhines, Ford (1988, 1990a) concluded that the ancestral platyrrhine was a small to medium-sized (1,000 g) arboreal quadruped, which emphasized quadrupedal running and walking, principally on horizontal branches, and included a signiﬁcant component of leaping in its locomotor repertoire. Ford proposed Aotus as the most useful living model on the basis of its postcranial traits. This is somehow ironic, in the sense that there are no detailed quantitative observations, only anecdotal information on the locomotor repertoire of owl monkeys. On the other hand, the postcranium of Callicebus is virtually equivalent to Aotus, and this genus, as well as Saimiri, manifests similar locomotor behaviors: frequent above branch quadrupedalism, substantial use of horizontal supports, and considerable leaping in variable rates. The same holds true for the closely related Cebus, which frequently employs similar locomotion, but it is somewhat larger in body mass and more specialized in exploiting divergent microhabitats by utilizing more destructive foraging techniques. The generalized locomotor repertoire utilized by medium-sized platyrrhines has also been proposed, on the basis of assessing the available postcranial elements, as a pattern relevant to the primitive anthropoid condition (e.g., Gebo and Dagosto, 2004). The essence of these behavioral reconstructions reﬂect the correlations of locomotor behavior of small to medium-sized platyrrhines (1,000 g) to substrate grain and texture presented in the landmark work of Fleagle and Mittermeier (1980). A Principal Components Analysis (PCA) of the logtransformed percentages of the distinct locomotor modes (quadrupedalism, climb/clamber, leap, suspensory, and clawed locomotion) reveals an interesting pattern of locomotor variation among extant platyrrhines (Fig. 7). Each axis contributed differentially to the separation of the locomotor groups, particularly separating the more specialized forms along respective axes. Medium-sized platyrrhines characterized by a mixture of quadrupedalism and leaping are clustered around the intersection of the axes. This cluster includes Saimiri, Cebus and Callicebus species. Large-bodied climbers/suspenders were separated from above-branch locomotors on Factor 1, which accounted for 44.7% (Factor 1 loadings of 0.827 and 0.830, respectively). The large bodied folivore-frugivores exhibit increased climbing and suspensory abilities and can readily exlploit the high canopies of mainly rich, as well as poorer, forests (Strier, 1992). On the other hand, the claw-climbing and leaping groups were separated along Factor 2, which accounted for 29.1% of explained variance, (loadings of 0.578 and 0.467, respectively). These are small-bodied insectivore-gummivores, using claw-climbing, clinging and vertical leaping in the understories of diverse types of forested habitats (Garber, 1992). Some taxa, such as the Pitheciinae Chiropotes and Cacajao, and the Callitrichinae Saguinus and Leontopithecus, overlap considerably with the central cluster, reﬂecting the less specialized nature of their locomotor repertoires. Even Alouatta tended towards the central cluster of ‘‘generalists.’’ This grouping pattern is not entirely evident, as some sets of genera are quite dispersed on the plot, but this may be an artifact of the original data, which was compiled from many separate studies. Problems of comparability across studies with differing localities and methodologies have been acknowledged repeatedly in the past. These inconsistencies of particulars understandably introduce variation that will not correlate closely with broader generalizations made here. However, a comprehensive analysis of a selected anatomical region, the ankle (i.e., talus), which is frequently recovered in the platyrrhine fossil record, revealed a strikingly similar pattern to the behavioral data (Meldrum, 1990). This was based on eleven dimensions and a multivariate analysis of the fundamental proportions of the talus of 300 specimens of platyrrhine genera, excluding only Brachyteles and Callimico. The pattern of variation in this instance revealed four distinguishable groupings: a central cluster of small-to-medium-bodied Aotus, Callicebus, Saimiri, and ﬁnally Cebus, exhibiting quadrupedal running and leaping; towards one pole, the smallbodied Callitrichinae, exhibiting claw-assisted scansorial and clinging positional behaviors; towards the other pole, the Pitheciinae, ﬁrst the more quadrupedal Cacajao and Chiropotes, who also exhibit hindlimb suspension and foot reversal, followed by Pithecia; ﬁnally largebodied Alouatta and the other Atelidae at the extreme, exhibiting climbing/clambering and suspensory behaviors, with increased tail-assited suspension in the latter (Fig. 8). LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES 2007 Fig. 7. Plot of modern platyrrhine genera on the ﬁrst two axes of the Principal Component Analysis, based on log-transformed percentages of grouped locomotor modes (quadrupedalism, climb/clamber, suspensory, leap and claw-climb). The inferred placement, on either plot (Figs. 7 and 8), of the fossil species with known postcrania permitting locomotor reconstruction, would exhibit a narrower spectrum of variation, with many extinct taxa falling within the range of the central cloud of species, among quadrupedal leapers and quadrupedal/climbers. By contrast, the younger large-bodied Caipora and Protopithecus would align with the more suspensory extant Atelinae. However, these locomotor patterns do not form exclusive units, classiﬁed on a strictly phylogenetic basis. They demonstrate adaptive strategies to speciﬁc habitats, at times convergent, that are shared by more than one sympatric or syntopic species (Fleagle and Reed, 1996, 1999). Until the recovery of postcranial elements for the earliest platyrrhine fossil, Branisella, little can be said with certainty about its locomotor behavior, other than perhaps a likely correlation to its body size and the locomotor behavior of similar-sized extant playrrhines, that is, arboreal quadrupedal running and leaping. This may be a moot point in the search for the ancestral platyrrhine condition, if Branisella is a member of an ancient radiation of stem platyrrhines, which bears no apparent afﬁnities to modern taxa (e.g., Rosenberger et al., 1991; Takai et al., 2000; Kay et al., 2008). In that case, the model proposed by Ford (1988), based on the study of the locomotor diversity of extant platyrrhines, would point to the ancestral morphology of the last common ancestor of extant platyrrhine genera, rather than the earliest and presumed ancestor of all platyrrhines, fossil, and living. The early Miocene fossils considered here, Dolichocebus, Soriacebus, Carlocebus, Homunculus (and Tremacebus, not known postcranially) from Patagonia, likely represent a distinct ancient radiation (Kay et al., 2008; Kay and Fleagle, 2010), in our view. The oldest of these, Dolichocebus, shows the generalized mixture of quadrupedal activities with leaping behavior, which most closely approximates Ford’s morphotype reconstruction. If Dolichocebus is indeed a primitive member of the Saimiri lineage (Tejedor, 2008; Rosenberger et al., 2009), its generalized locomotor reconstruction may be the bridge 2008 YOULATOS AND MELDRUM Fig. 8. Three-dimension Principal Coordinates ordination of extant platyrrhine genera computed from generic means of log transformed ratios. The minimum spanning tree is projected onto the horizontal plan (see Meldrum, 1990). between the early Miocene radiation and the diversity of extant genera. Otherwise its postcranial generalization would be merely a primitive retention for a small to medium-sized platyrrhine. On the other hand, Soriacebus and Carlocebus seem to be postcranially more derived, exhibiting mixed quadrupedal and climbing/clambering, and even some suspensory habits, especially in Soriacebus (Meldrum, 1990). These adaptations, which very likely enabled them to differentially utilize the ancient forests and exploit the available fruit sources, seem to parallel the evolution of locomotor patterns in Pitheciinae and Callicebus, where some authors align these fossils (e.g., Rosenberger, 2002; Tejedor, 2008; Rosenberger et al., 2009). Thus, these platyrrhines may represent early members of the pitheciid clade, or they represent early forms that were adapted to analogous niches in the early Miocene southern forests, convergent on the pitheciid condition. By contrast, the dental pitheciine Proteropithecia with its associated talus, as well as the isolated talus from Chile, show no postcranial similarity or convergence on the derived pitheciine condition, rather morphologies correlated with generalized quadrupedalism and leaping, correlated with medium to small body size, as in Callicebus for example (Kay et al., 1998). The meager postcranial remains of these taxa do not offer a clear resolution to the question of synapomorphy or homoplasy at this time. A pattern of convergent niche partitioning might also be suggested by other recovered fossil platyrrhines, such as the Callicebus-like frugivore/folivore and quadrupedal leaper Homunculus, whose inferred locomotion aligns with that of the titi monkey’s generalized positional repertoire. Even Antillothrix, the Pleistocene Hispaniolan fossil, is now considered as a remnant of an early platyrrhine radiation, probably similar to that of the early taxa discussed above (Rosenberger et al., 2011; Kay et al., 2011). This is particularly interesting since this fossil seems to exhibit a derived morphology correlated with quadrupedalism, climbing/clambering, and possibly even suspensory habits (Rosenberger et al., 2011; Kay et al., 2011). This behavior could be a novel adaptation to niche partitioning in an isolated insular habitat, just as was the peculiar semiterrestriality of Paralouatta in Cuba, and the kinkajou-like suspension of Xenothrix in Jamaica (McPhee and Fleagle, 1991). Alternatively, it could have been retention of positional abilities of an earlier radiation similar to the early Miocene Argentinean fossils. However, the overall plasticity of positional behavior (e.g., Garber and Preutz, 1995) lends support to the former hypothesis. In the middle Miocene, the rich paleo-community of La Venta has been extensively studied (e.g., Hartwig and Meldrum, 2002). The three sets of Nuciruptor and Cebupithecia, Neosaimiri, and Laventiana, plus Aotus dindensis, seem to represent three distinct adaptive clades. The ﬁrst favored hard or unripe fruit and seed LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES eating accessed by quadrupedalism and leaping; the second, an insectivorous/frugivorous diet acquired by increased bouts of quadrupedal walk/run and leaping; and the third, a frugivore/insectivore frequently using quadrupedal walking/running and leaping behavior. These adaptations seem very comparable to the ones observed in modern counterparts of their respective clades, such as Pithecia, Saimiri, and Aotus, where they are found syntopically. All these three fossil groups seem to have retained in some measure the positional adaptations of the earliest platyrrhine—a mixture of quarupedalism and leaping. Among the small- to medium-sized platyrhrines, modern Cebinae and Aotus especially have retained this pattern throughout their long evolutionary history, whereas the Pitheciinae evolved towards two different patterns: relatively longer limbs and increased suspensory behavior, and in the case of Pithecia pithecia, increased clinging and leaping. P. pithecia, evolved to be one of the most saltatorial modern platyrrhines (e.g., Fleagle and Meldrum, 1988).The sister taxa Cacajao and Chiropotes adhere to a more quadrupedal strategy, including a variable but signiﬁcant amount of leaping, which is performed in a different manner from that encountered in Pithecia (Walker and Ayres, 1996), and below-branch behavior, especially hindlimb suspension (Fleagle and Meldrum; 1988; Meldrum et al., 1997; Meldrum, 1998). Atelidae and Callitrichinae, the two most derived groups that were mentioned earlier, have been the subject of extensive studies, and the fact that they are characterized by either very few, but highly derived fossil members like the Protopithecus and Caipora in the atelid lineage, or fossils of less certain afﬁnities with no preseserved postcranial elements, as in the callitrichine lineage, leaves little to discuss. The Callitrichinae stand out because there are comparably few ﬁeld studies on the locomotion and postures of several extant genera, such as Leontopithecus, Mico, Callibella, and Callithrix. Because of their derived postcrania (Ford, 1988; Davis, 2002; Ford and Davis, 2009), these genera are expected to be rather specialized in their positional behavior, but recent studies have shown signiﬁcant plasticity in other marmosets (e.g., Porter and Garber, 2004; Youlatos, 2009). The diversity of adaptations in these forms could be equivalent to that observed in Saguinus (e.g., Garber, 1992, 2007). In contrast, the Atelidae seem to have been oversampled in the wild. Alouatta, the most basal member of the group is relatively well known. Some species have been well studied in a variety of habitats and do show some diversity around a well-established locomotor pattern characterized by quadrupedal walking, clambering, climbing, and tail-hind limb suspension. However, as Alouatta is one of the few platyrrhines that is so widespread across the Americas, from dry tropical forests in southern Mexico to temperate forests in northern Argentina, more studies are required to understand the potential behavioral ﬂexibility of this platyrrhine. Only Cebus shows a similar degree of adaptive plasticity. Further studies will also shed light on the adaptive signiﬁcance of tail-assisted-hind limb suspension in relation to diverse micro-habitat parameters. Two of the more derived members of the group, Ateles and Lagothrix, are now well known from the ﬁeld, but the lack of systematic quatitative data for Brachyteles, as a tail-arm bra- 2009 chiating folivore/frugivore inhabiting the Mata Atlantica of southeastern Brazil, leaves a void in the reconstruction of the evolution of suspensory behavior and its relation to frugivory and energy maximization within this large-bodied clade. Nevertheless, ﬁeld data on the locomotor ecology of more Ateles species are still required, in order to obtain a complete image of the adaptive signiﬁcance of tail-forelimb suspension in atelid evolution. We are far from completing the evolutionary history of platyrrhines. The recovery of new and more complete fossils is enriching the paleontological record, while additional ﬁeld studies are adding to an understanding of the adaptive signiﬁcance and general plasticity of locomotor and postural diversity of extant taxa. The growing platyrrhine postcranial fossil record has witnessed signiﬁcant additions since last reviewed by Meldrum (1993). Novel hypotheses synthesizing the framework of platyrrhine origins and phylogenetic diversiﬁcation have been proposed in recent years, focusing discussions on both morphologies and methodologies. Hopefully these will lead to clariﬁcation of the nature of the proto-platyrrhine immigration to the Western Hemisphere and subsequent pattern of platyrrhine diversiﬁcation. Although the evolution of locomotor diversity offers many insights into the adative radiation among platyrrhines, it offers no deﬁnitive resolution to competing hypotheses of platyrrhine phylogeny. ACKNOWLEDGEMENTS The authors are particularly grateful to Alﬁe Rosenberger, who invited them to participate in this project. His continuous encouragement and editorial guidance helped us complete this review, which likewise rests upon the contributions of mentors, colleagues, museum curartors, and funders, too numerous to mention singly. LITERATURE CITED Anapol F, Fleagle JG. 1988. Fossil platyrrhine forelimb bones from the early Miocene of Argentina. Am J Phys Anthropol 76:417– 428. Bauer K, Schreiber A. 1997. Double invasion of Tertiary island South America by ancestral New World monkeys. Biol J Linn Soc 20:1–29. Bezanson M. 2009. Life history and locomotion in Cebus capucinus and Alouatta palliata. Am J Phys Anthropol 140:508–517. Bicca-Marques JC, Calegaro-Marques C. 1995. Locomotion of black howlers in a habitat with discontinuous canopy. Folia primatol 64:55–61. Bluntschli H. 1913. Die fossilen affen patagonies und der ursprung der platyrrhinen affen. Anat Anzeig 44:33–43. Bluntschli H. 1931. Homunculus patagonicus und die ihm zugereihten fossilfunde aus den Santa-Cruz-Schichten patagoniens: eine morphologisce revision an hand der originalstucke in der sammlung Ameghino zu La Plata. Genen Morphol Jahr 67:811– 892. Boinski S. 1989. The positional behavior and substrate use in the squirrel monkeys: ecological implications. J Hum Evol 18:659– 677. Bown TM, Larriestra CN. 1990. Sedimentary paleoenvironments of fossil platyrrhine localities, Miocene Pinturas Formation, Santa Cruz Province, Argentina. J Hum Evol 19:87–119. Cant JGH. 1986. Locomotion and feeding postures of spider and howling monkeys: ﬁeld study and evolutionary interpretation. Folia primatol 46:l–14. 2010 YOULATOS AND MELDRUM Cant JGH, Youlatos D, Rose MD. 2001. Locomotor behavior of Lagothrix lagothricha and Ateles belzebuth in Yasuni National Park, Ecuador: general patterns and nonsuspensory modes. J Hum Evol 41:141–166. Cant JGH, Youlatos D, Rose MD. 2003. Suspensory locomotion of Lagothrix lagothricha and Ateles belzebuth in Yasuni National Park, Ecuador. J Hum Evol 44:685–699. Cartelle C, Hartwig WC. 1996. A new extinct primate among the Pleistocene megafauna of Bahia, Brazil. Proc Natl Acad Sci USA 93:6405–6409. Ciochon RL, Chiarelli AB. 1980. Evolutionary biology of the New World monkeys and continental drift. New York: Plenum. Ciochon RL, Corruccini RS. 1975. Morphometric analysis of platyrrhine femora with taxonomic implications and notes on two fossil forms. J Hum Evol 4:193–217. Collins AC. 2004. Atelinae phylogenetic relationships: the trichotomy revived? Am J Phys Anthropol 124:285–296. Cooke SB, Rosenberger AL, Turvey S. 2011. An extinct monkey from Haiti and the origins of Greater Antillean primates. Proc Natl Acad Sci USA 108:2699–2704. Dagosto M. 1988. Implications of postcranial evidence for the origin of Euprimates. J Hum Evol 17:35–56. Davis LC. 2002. Functional morphology of the forelimb and long bones in the Callitrichidae (Platyrrhini, Primates). PhD Dissertation. Carbondale, Southern Illinois University. Davis LC. 1987. Morphological evidences of the positional behaviour in the hindlimb of Cebupithecia sarmientoi (Primates: Platyrrhini). MA Thesis, Arizona State University. Deﬂer TR. 1999. Locomotion and posture in Lagothrix lagotricha. Folia primatol 70:313–327. Erikson GE. 1963. Brachiation in the new World monkeys and anthropoid apes. Symp Zool Soc Lond 10:135–164. Fleagle JG. 1999. Primate adaptation and evolution. 2nd ed. San Diego: Academic Press. Fleagle JG, Meldrum DJ. 1988. Locomotor behavior and skeletal morphology of two sympatric pitheciine monkeys, Pithecia pithecia and Chiropotes satanas. Am J Primatol 16:227–249. Fleagle JG, Mittermeier RA. 1980. Locomotor behavior and comparative ecology of seven Surinam monkeys. Am J Phys Anthropol 52:301–314. Fleagle JG, Reed KE. 1996. Comparing primate communities: a multivariate approach. J Hum Evol 30:489–510. Fleagle JG, Reed KE. 1999. Phylogenetic and temporal perspectives on primate ecology. In: Fleagle JG, Janson C, Reed KE, editors. Primate communities. New York: Cambridge University Press. p 92–115. Fleagle JG, Tejedor MF. 2002. Early platyrrhines of southern South America. In: Hartwig WC, editor. The primate fossil record. Cambridge: Cambridge University Press. p 161–173. Fontaine R. 1990. Positional behavior in Saimiri boliviensis and Ateles geoffroyi. Am J Phys Anthropol 82:485–508. Ford SM. 1980. Callitrichids as phyletic dwarfs, and the place of the Callitrichidae in Platyrrhini. Primates 21:31–43. Ford SM. 1988. Postcranial adaptations of the earliest platyrrhine. J Hum Evol 17:155–192. Ford SM. 1990a. Locomotor adaptations of fossil platyrrhines. J Hum Evol 19:141–173. Ford SM. 1990b. Platyrrhine evolution in the West Indies. J Hum Evol 19:237–254. Ford SM, Davis LC. 1992. Systematics and body size: implications for feeding adaptations in New World monkeys. Am J Phys ANthropol 88:415–468. Ford SM, Davis LC. 2009. Marmoset postcrania and the skeleton of the dwarf marmoset, Callibella humilis. In: Ford SM, Porter LM, Davis LC, editors. The smallest anthropoids: the marmoset/callimico radiation. New York: Springer Verlag. p 411–448. Ford SM, Porter LM, Davis LC. 2009. The smallest anthropoids: the marmoset/callimico radiation. New York: Springer Verlag. Garber PA. 1980. Locomotor behavior and feeding ecology of the Panamanian tamarin (Saguinus oedipus geoffroyi, Callitrichidae, Primates). Int J Primatol 1:185–201. Garber PA. 1991. A comparative study of positional behavior in three species of tamarind monkeys. Primates 32:219–230. Garber PA. 1992. Vertical clinging, small body size, and the evolution of feeding adaptations in the Callitrichinae. Am J Phys Anthropol 88:469–482. Garber PA. 2007. Primate locomotor behavior and ecology. In: Campbell C, Fuentes A, MacKinnon KC, Panger M, Bearder S, editors. Primates in perspective. Oxford: Oxford University Press. p 543–560. Garber PA, Leigh SR. 2001. Patterns of positional behavior in mixed-species troops of Callimico goeldii, Saguinus labiatus, and Saguinus fuscicollis in northwestern Brazil. Am J Primatol 54:17–31. Garber PA, Blomquist GE, Anzenberger G. 2005. Kinematic analysis of trunk-to-trunk leaping in Callimico goeldii. Int J Primatol 26:223–240. Garber PA, Rosenberger AL, Norconk MA. 1996. Marmoset misconceptions. In: Norconk MA, Rosenberger AL, Garber PA, editors. Adaptive radiations of neotropical primates. New York: Plenum Press. p 87–95. Garber PA, Sallenave A, Blomquist GE, Anzenberger G. 2009. A comparative study of the kinematics of trunk-to-trunk leaping in Callimico goeldi, Callitrhix jacchus, and Cebuella pygmaea. In: Ford SM, Porter LM, Davis LC, editors. The smallest anthropoids: the marmoset/callimico radiation. New York: Springer Verlag. p 259–278 Garber PA, Preutz D. 1995. The positional behavior of moustached tamarin monkeys: effects of habitat on locomotor variability and locomotor stability. J Hum Evol 28:411–426. Garber PA. Rehg JA. 1999. The ecological role of the prehensile tail in white-faced capuchins (Cebus capucinus). Am J Phys Anthropol 110:325–339. Gebo DL. 1992. Locomotor and postural behavior in Alouatta palliata and Cebus capucinus. Am J Primatol 26:277–290. Gebo DL, Dagosto M. 2004. Anthropoid origins: postcranial evidence from the Eocene of Asia. In: Ross CF, Kay RF, editors. Anthropoid Origins: New Visions. New York: Kluwer Academic/Plenum. p 369–380. Gebo DL, Dagosto M, Rosenberger AL, Setoguchi T. 1990. New platyrrhine tali from La Venta, Colombia. J Hum Evol 19:737–746. Gebo DL, Simons EL. 1987. Morphology and locomotor adaptations of the foot of early Oligocene anthropoids, Am J Phys Anthropol 74:83–101. Guillot D. 2009. Measures of postural and locomotor performance in wild atelid primates: a comparative analysis of Alouatta seniculus, Lagothrix poeppigii, and Ateles belzebuth. Ph.D. Dissertation, Boston University. Harada ML, Schneider H, Schneider MPC, Sampaio I, Czelusniak J, Goodman M. 1995. DNA evidence on the phylogenetic systematics of New World monkeys: support for the sistergrouping of Cebus and Saimiri from two unlinked nuclear genes. Mol Phylogenet Evol 4:331–349. Hartwig W, Meldrum DJ. 2002. Miocene platyrrhines of the northern Neotropics. In: Hartwig WC, editor. The primate fossil record. Cambridge: Cambridge University Press. p. 175–187. Hartwig WC, Cartelle C. 1996. A complete skeleton of the giant South American primate Protopithecus. Nature 381:307–311. Hershkovitz P. 1977. Living New World Monkeys (Platyrrhini): with an Introduction to Primates. Vol 1. Chicago: University of Chicago Press. Hoffstetter MR. 1980. Origin and deployment of New World monkeys emphasizing the southern continents route. In: Ciochon RF, Chiarelli AB, editors. Evolutionary biology of New World monkeys and continental drift. New York: Plenum Press. p 103–122. Houle A. 1999. The origin of platyrrhines: an evaluation of the Antarctic scenario and the ﬂoating island model. Am J Phys Anthropol 109:541–559. Hodgson JA, Sterner KN, Matthews LJ, Burrell A, Jani RA, Raaum RL, Stewart CB, Distotell TR. 2009. Successive radiations, not stasis, in the South American primate fauna. Proc Natl Acad Sci USA 106:5534–5539. LOCOMOTION IN FOSSIL AND EXTANT PLATYRRHINES Horovitz I. 1999. A phylogenetic study of living and fossil platyrrhines. Am Mus Novit 3269:1–40. Horovitz I, MacPhee RDE. 1999. The Quaternary Cuban platyrrhine Paralouatta varonai and the origin of Antillean monkeys. J Hum Evol 36:33–68. Horovitz I, Zardoya R, Meyer A. 1998. Platyrrhine systematics: a systematic analysis of molecular and morphological data. Am J Phys Anthropol 106:261–281. Iturralde Vinent MA, MacPhee RDE. 1999. Paleogeography of the Caribbean region: implications for Cenozoic biogeography. Bull Am Mus Nat Hist 238:1–95. Jones AL. 2008. The evolution of brachiation in atelid primates, ancestral character states and history. Am J Phys Anthropol 137:123–144. Janson CH, Boinski S. 1992. Morphological and behavioral adaptations for foraging in generalist primates—the case of cebines. Am J Phys Anthropol 88:483–498. Karantanis NE. 2010. Comparative positional behaviour in three captive callitrichid species: Leontopithecus chrysomelas, Saguinus imperator and Cebuella pygmaea. MSc Thesis, University College of London. Kay RF. 1990. The phyletic relationships of extant and fossil Pitheciinae (Platyrrhini, Anthropoidea). J Hum Evol 19:175–208. Kay RF. 1994. ‘‘Giant’’ tamarin from the Miocene of Colombia. Am J Phys Anthropol 95:333–353. Kay RF, Campbell V, Rossie JB, Colbert MW, Rowe TB. 2004. Olfactory fossa of Tremacebus harringtoni (Platyrrhini, early Miocene, Sacanana, Argentina): implications for activity pattern. Anat Rec A 281:1157–1172. Kay RF, Cozzuol MA. 2006. New platyrrhine monkeys from the Solimões Formation (late Miocene, Acre State, Brazil). J Hum Evol 50:673–686. Kay RF, Fleagle JG, Mitchell TRT, Colbert M, Bown T, Powers DW. 2008. The anatomy of Dolichocebus gaimanensis, a stem platyrrhine monkey from Argentina. J Hum Evol 54:323–382. Kay RF, Johnson D, Meldrum DJ, 1998. A new pitheciin primate from the middle Miocene of Argentina. Am J Primatol 45:317– 336. Kay RF, Fleagle JG. 2010. Stem taxa. Homoplasy, long lineages, and the phylogenetic position of Dolichocebus. J Hum Evol 59:218–222. Kay RF, Hunt, KD, Beeker CD, Conrad GW, Johnson CC, Keller J. 2011. Preliminary notes on a newly discovered skull of the extinct monkey Antillothrix from Hispaniola and the origin of the Greater Antillean monkeys. J Hum Evol 60:124–128. Kay RF, Madden RH, Plavcan JM, Cifelli RL, Diaz JG. 1987. Stirtonia victoriae, a new species of Miocene Colombian primate. J Hum Evol 16:173–196. Kay RF, Meldrum DJ. 1997. A new small platyrrhine from the Miocene of Colombia and the phyletic position of the callitrichines. In: Kay RF, Madden RH, Cifelli RL, Flynn J, editors. A history of neotropical fauna: vertebrate paleontology of the miocene of Tropical South America. Washington DC: Smithsonian Institution Press. p 435–458. Kay RF, Williams BA, Anaya F. 2001. The adaptation of Branisella boliviana, the earliest South American monkey. In: Plavcan JM, van Schaik C, Kay RF, Jungers WL, editors. Reconstructing behavior in the primate fossil record. New York: Kluwer Academic/Plenum Publishers. p 339–370. Kinzey WG. 1992. Dietary and dental adaptations in the Pitehciinae. Am J Phys Anthropol 88:499–514. Lawler RR, Ford SM, Wright PC, Easley SP. 2006. The locomotor behavior of Callicebus brunneus and Callicebus torquatus. Folia primatol 77:228–239. Lockwood CA. 1999. Homoplasy and adaptation in the atelid postcranium. Am J Phys Anthropol 108:459–482. Luchterhand K, Kay RF, Madden RH. 1986. Mohanamico hershkovitzi, gen. et sp. Nov., un primate du Miocène moyen d’Amérique du Sud. Comp Rend Acad Sci Paris 303:1753–1758. MacFadden BJ. 1990. Chronology of Cenozoic primate localities in South America. J Hum Evol 19:7–21. 2011 MacFadden BJ. 2000. Cenozoic mammalian herbivores from the Americas: Reconstructing ancient diets and terrestrial communities. Ann Rev Ecol Syst 31:33–59. MacPhee RDE, Horovitz I. 2002. Extinct Quaternary platyrrhines of the Greater Antilles and Brazil. In: Hartwig WC, editor. The Primate Fossil Record. Cambridge: Cambridge University Press. p 189–200. MacPhee RDE, Fleagle JG. 1991. Postcranial remains of Xenothrix mcgregori (Primates, Xenotrichidae) and other Late Quaternary mammals from Long Mile Cave, Jamaica. Bull Am Mus Nat Hist 206:287–321. MacPhee RDE, Meldrum DJ. 2006. Postcranial remains of the extinct monkeys of the Greater Antilles (Platyrrhini, Callicebinae, Xenotrichini), with a consideration of semiterrestriality in Paralouatta. Am Mus Novit 3516:1–65. MacPhee RDE, Iturralde-Vinent MA, Gaffney ES. 2003. Domo de Zaza, an Early Miocene vertebrate locality in south-central Cuba, with notes on the tectonic evolution of Puerto Rico and Mona Passage. Am Mus Novit 3394:1–42. MacPhee RDE, Woods CA. 1982. A new fossil cebine from Hispaniola. Am J Phys Anthropol 58:419–436. Meireles CM, Czelusniak J, Schneider MPC, Muniz JAPC, Brigido MC, Ferreira HS, Goodman M. 1993. Molecular phylogeny of atelid NewWorld monkeys (Platyrrhini, Atelinae) based on g-globin gene sequences: evidence that Brachyteles is the sister group of Lagothrix. Mol Phylogenet Evol 12:10–30. Meldrum DJ. 1990. New fossil platyrrhine tali from the early Miocene of Argentina. Am J Phys Anthropol 83:403–418. Meldrum DJ. 1993. Postcranial adaptations and positional behavior in fossil platyrrhines. In: Gebo DL, editor. Postcranial adaptation in nonhuman primates. DeKalb: Northern Illinois University, p 235–251. Meldrum DJ. 1998. Tail-assisted hindlimb suspension as a transitional behavior in the evolution of prehensile tails. In: Strasser E, Fleagle JG, McHenry HM, editors. Advances in primatology: primate locomotion. New York: Plenum Press. p 145–156. Meldrum DJ, Dagosto MD, White J. 1997. Hindlimb suspension and hindfoot reversal in Varecia variegata and other arboreal mammals. Am J Phys Anthropol 103:85–102. Meldrum DJ, Fleagle JG, Kay RF. 1990. Partial humeri of two Miocene Colombian primates. Am J Phys Anthropol 81:413–422. Meldrum DJ, Kay RF. 1997a. Nuciruptor rubricae, a new pitheciin seed predator from the Miocene of Colombia. Am J Phys Anthropol 102:407–427. Meldrum DJ, Kay RF. 1997b. Primate postcranial fossils from the Miocene of Colombia. In: Kay RF, Madden RH, Cifelli RL, Flynn J, editors. A history of neotropical fauna: vertebrate paleontology of the miocene of Tropical South America. Washington DC: Smithsonian Institution Press. p 459–472. Meldrum DJ, Lemelin P. 1991. Axial skeleton of Cebupithecia sarmientoi (Pitheciinae, Platyrrhini) from the middle Miocene of La Venta, Colombia. Am J Primatol 25:69–90. Mittermeier RA. 1978. Locomotion and posture in Ateles geoffroyi and Ateles paniscus. Folia primatol 30:161–193. Nakatsukasa M, Takai M, Setoguchi T. 1997. Functional morphology of the postcranium and locomotor behaviour of Neosaimiri ﬁeldsi, a Saimiri-like middle Miocene platyrrhine. Am J Phys Anthropol 102:515–544. Napier JR, Davis PR. 1959. The forelimb skeleton and associated remains of Proconsul africanus. Fossil Mam Afr 16:1–69. Opazo JC, Wildman DE, Prychitko T, Johnson RM, Goodman M. 2006. Phylogenetic relationships and divergence times among New World monkeys (Platyrrhini, Primates). Mol Phylogenet Evol 40:274–280. Pascual R, Ortiz Jaureguizar E. 1990. Evolving climates and mammal faunas in Cenozoic South America. J Hum Evol 19:23–60. Porter LM, Garber PA. 2004. Goeldi’s monkey: a primate paradox? Evol Anthrop 13:104–115. Prates HM, Bicca Marques JC. 2008. Age-sex analysis of activity budget, diet, and positional behavior in Alouatta caraya in an orchard forest. Int J Primatol 29:703–715. 2012 YOULATOS AND MELDRUM Reeser LA. 1984. Morphological afﬁnities of new fossil talus of Dolichocebus gaimanensis. Am J Phys Anthropol 63:206–207. Rivero M, Arredondo O. 1991. Paralouatta varonai, a new Quaternary platyrrhine from Cuba. J Hum Evol 21:1–11. Rosenberger AL. 1977. Xenothrix and ceboid phylogeny. J Hum Evol 6:461–481. Rosenberger AL. 1979. Cranial anatomy and implications of Dolichocebus, a late Oligocene ceboid primate. Nature 279 (5712):416–418. Rosenberger AL. 1992. Evolution of feeding niches in New World monkeys. Am J Phys Anthropol 88:525–562. Rosenberger AL. 2002. Platyrrhine paleontology and systematics: the paradigm shifts. In: Hartwig WC, editor. The primate fossil record. Cambridge: Cambridge University Press. p 151–160. Rosenberger AL. 2010. Platyrrhines, PAUP, parallelism, and the Long Lineage Hypothesis: a reply to Kay et al. (2008). J Hum Evol 59:214–217. Rosenberger AL, Hartwig WC, Takai M, Setoguchi T, Shigahara N. 1991a. Dental variabilty in Saimiri and the taxonomic status of Neosaimiri ﬁeldsi, and early squirrel monkey from La Venta, Columbia. Int J Primatol 12:291–302. Rosenberger AL, Hartwig WC, Wolff RG. 1991b. Szalatavus attricuspis, an early platyrrhine primate. Folia primatol 56:225–233. Rosenberger AL, Setoguchi T, Hartwig WC. 1991c. Laventiana annectens, new genus and species: fossil evidence for the origin of callitrichine monkeys. Proc Natl Acad Sci USA 88:2137–2140. Rosenberger AL, Setoguchi T, Shigehara N. 1990. The fossil record of callitrichine primates. J Hum Evol 19:209–236. Rosenberger AL, Strier KB. 1989. Adaptive radiation of the atelid primates. J Hum Evol 18:717–750. Rosenberger AL, Tejedor MF, Cooke S, Pekar S. 2009. Platyrrhine ecophylogenetics, past and present. In: Garber P, Estrada A, Bicca-Marques JC. Heymann EW, Strier KB, editors. South American primates: comparative perspectives in the study of behavior, ecology and conservation. New York: Springer. p 69– 113. Rosenberger AL, Cooke SB, Rimoli R, Ni X, Cardoso L. 2011. First skull of Antillothrix bernensis, an extinct relict monkey from the Dominican Republic. Proc Biol Sci 278:67–74. Schneider H, Canavez FC, Sampaio I, Moreira MAM, Tagliaro CH, Seuanez HN. 2001. Can molecular data place each Neotropical monkey in its own branch? Chromosoma 109:515–523. Schneider H, Sampaio I, Harada ML, Barroso CML, Schneider MPC, Czelusniak J, Goodman M. 1996. Molecular phylogeny of the New World monkeys (Platyrrhini, Primates) based on two unlinked nuclear genes: IRBP interon 1 and e-globin sequences. Am J Phys Anthropol 100:153–179. Schneider H, Schneider MPC, Sampaio I, Harada ML, Stanhoope M, Czelusniak J, Goodman M. 1993. Molecular phylogeny of the New World monkeys (Platyrhini, Primates). Mol Phylogenet Evol 2:225–242. Schön Ybarra MA, Schön MA. 1987. Positional behavior and limb bone adaptations in red howling monkeys (Alouatta senicuhs). Folia primatol 49:70–89. Schrago CG. 2007. On the time scale of New World primate diversiﬁcation. Am J Phys Anthropol 132:344–354. Seiffert ER, Simons EL, Simons CVM. 2004. Phylogenetic, biogeographic, and adaptive implications of new fossil evidence bearing on crown anthropoid origins and early stem catarrhine evolution. In: Ross C, Kay RF, editors. Anthropoid origins: new visions. New York: Kluwer Academic/Plenum Publishers. p 157–182. Setoguchi T, Rosenberger AL. 1987. A fossil owl monkey from La Venta, Colombia. Nature 326:692–694. Singer SS, Schmitz J, Schwiegk C, Zischler H. 2003. Molecular cladistic markers in New World monkey phylogeny (Platyrrhini, Primates). Mol Phylogen Evol 26:490–501. Stafford BJ, Rosenberger AL, Beck BB. 1994. Locomotion of freeranging golden lion tamarins (Leontopithecus rosalia) at the National Zoological Park. Zoo Biol 13:33–344. Stirton RA. 1951. Ceboid monkeys from the Miocene of Columbia. Bull Univ Calif Publ Geol Sci 28:315–356. Stirton RA, Savage DE. 1951. A new monkey from the La Venta Miocen of Colombia. Compil Estud Geol Ofﬁc Colombia 7:345– 356. Strier KB. 1992. Atelinae adaptations: behavioral strategies and ecological constraints. Am J Phys Anthropol 88:515–524. Takai M. 1994. New specimens of Neosaimiri ﬁeldsi from La Venta, Colombia: A middle Miocene ancestor of the living squirrel monkeys. J Hum Evol 27:329–360. Takai M, Anaya F. 1996. New specimens of the oldest fossil platyrrhine, Branisella boliviana, from Salla, Bolivia. Am J Phys Anthropol 99:301–317. Takai M, Anaya F, Shigehara N, Setoguchi T. 2000. New fossil materials of the earliest New World Monkey, Branisella boliviana, and the problem of platyrrhine origins. Am J Phys Anthropol 111:263–281. Takai M, Anaya F, Suzuki H, Shigehara N, Setoguchi T. 2001. A new platyrrhine from the middle Miocene of La Venta, Colombia, and the phyletic position of Callicebinae. Anthropol Sci 109:289– 308. Tejedor MF. 2003. New fossil primate from Chile. J Hum Evol 44:515–520. Tejedor MF. 2008. The origin and evolution of Neotropical monkeys. Arquiv Mus Nac Rio Jan 66:251–269. Tejedor MF, Rosenberger AL. 2008. A neotype for Homunculus patagonicus Ameghino 1891, and a new interpretation of the taxon. Paleoanthropology 2008:68–82. Walker SE. 1993. Positional Adaptations and Ecology of the Pitheciini. Ph.D. Dissertation, City University of New York. Walker SE, Ayres JM. 1996. Positional behavior of the white uakari (Cacajao calvus calvus). Am J Phys Anthropol 101:161–172. Wildman DE, Jameson NM, Opazo JC, Yi SV. 2009. A fully resolved genus level phylogeny of neotropical primates (Platyrrhini). Mol Phylogenet Evol 53:694–702. Wright KA. 2007. The relationship between locomotor behavior and limb morphology in brown (Cebus apella) and weeper (Cebus olivaceus) capuchins. Am J Primatol 69:736–756. Wright PC. 1989. The nocturnal primate niche in the New World. J Hum Evol 18:635–658. Youlatos D. 1998. Positional behavior of two sympatric Guianan capuchin monkeys, the brown capuchin (Cebus apella) and the wedge-capped capuchin (Cebus olivaceus). Mammalia 62:351–365. Youlatos D. 1999. Comparative locomotion of six sympatric primates in Ecuador. Ann Sci Nat Zool 20:161–168. Youlatos D. 2002. Positional behavior of black spider monkey (Ateles paniscus) in French Guiana. Int J Primatol 23:1071–1093. Youlatos D. 2004. Multivariate analysis of organismal and habitat parameters in two Neotropical primate communities. Am J Phys Anthropol 123:181–194. Youlatos D. 2008. Locomotion and positional behavior of spider monkeys. In: Campbell CJ, editor. Spider monkeys: behavior, ecology and evolution of the genus Ateles. Cambridge: Cambridge University Press. p 185–219. Youlatos D. 2009. Locomotion, postures, and habitat use by pygmy marmosets (Cebuella pygmaea). In: Ford SM, Porter LM, Davis LC, editors. The smallest anthropoids: the marmoset/callimico radiation. New York: Springer Verlag. p 279–297. Youlatos D, Gasc JP. 2001. Comparative positional behaviour of ﬁve primates. In: Bongers F, Charles-Dominique P, Forget M, Théry M, editors. Nouragues: dynamics and plant-animal interactions in a neotropical rain forest. Dordrecht: Kluwer Academic Publishers. p 103–114. Zaluar MT, Rocha Barbosa O, Loguercio MF, Rangel CH, Youlatos D. 2010. Utilização do habitat, locomoção e postura de Callithrix jacchus Linnaeus, 1758 (Mammalia, Primates). V Congresso Brasileiro de Mastozoologia, São Pedro/ São Paulo, Brazil.