Proximal femoral anatomy of a sivaladapid primate from the late middle Eocene Pondaung formation (central Myanmar)

The postcranial anatomy of the Asian sivaladapid adapiforms is still virtually undocumented, whereas dental remains of these primates have been known for several decades. Little is known about their positional behavior as a result. In this article, we describe a partial left femur of a medium-sized primate preserving its entire proximal portion and a significant length of its shaft. This fossil was recently recovered from the fossiliferous locality of Thamingyauk in the late middle Eocene Pondaung Formation (central Myanmar). This femur is considered to pertain to the same individual as two tarsal elements (fragmentary talus and calcaneus) from the same locality (same location), and attributed to a medium-sized sivaladapid adapiform primate (Kyitchaungia takaii). This new postcranial element provides the first documentation of femoral anatomy among Sivaladapidae from Asia. The mechanical implications deriving from the musculoskeletal interpretation of this bone indicate an animal that probably engaged in a kind of active arboreal quadrupedalism with some degree of proficiency in leaping. Even though many musculoskeletal aspects suggest that branch walking and running were important parts of its locomotor repertoire, in other details it appears that relatively complex movements at the hip joint were actually possible and probably associated with climbing or some hindlimb suspensory activities.     

Femoral head trabecular bone structure in two omomyid primates

The study of the three-dimensional structure of trabecular bone and its relationship to locomotor behavioral differences across different primate taxa provides a potentially useful analytic tool for reconstructing the behavior of extinct taxa. The purpose of the current study is to quantify the three-dimensional architecture of trabecular bone in the femoral head of Omomys carteri and Shoshonius cooperi and to compare this structure to that of several extant strepsirrhine taxa. Bone volume fraction (BV/TV) and fabric anisotropy were quantified in three dimensions using serial high-resolution X-ray computed tomography scan data collected from one femoral head from each fossil taxon. Three cubic volumes of interest (VOI) were identified within the femoral head. The BV/TV was quantified by assessing the percentage of bone voxels within each VOI and the structural anisotropy was quantified using the star volume distribution method. The Omomys femur used here has a high BV/TV with the galagine-like pattern of decreasing BV/TV from the superior to the inferior half of the femoral head. The fabric structure, however, is more lorisine-like in being relatively isotropic throughout the femoral head. The trabecular structure in Omomys is unique in its mix of features and appears to be most similar overall to the lorisines, suggesting that Omomys engaged in a quadrupedal mode of locomotion. By contrast the Shoshonius specimen possesses a relatively uniform BV/TV across the head but displays the distinctly galagine-like pattern of increasing anisotropy moving inferiorly in the femoral head. Taken as a whole, the trabecular structure in Shoshonius appears to be most like that of the galagines and is consistent with that of either an occasional leaper-quadruped or a specialized leaper. Despite the overall similarities in the external postcranial anatomy of Omomys and Shoshonius, the results of this study indicate potentially important differences in the magnitude and orientation of the external loads at the hip joint, suggesting that these animals engaged in divergent locomotor behaviors.     

Morphological and functional differentiation in the lumbar spine of lorisids and galagids

The striking contrast in positional behavior exhibited by lorisids (slow quadrupedalism/suspension) and galagids (leaping/quadrupedalism) is well reflected in their postcranial morphology, particularly in the limbs. Although they exhibit very different spinal postures and movements, vertebral adaptations have been less well explored in these taxa. This study addressed morphological and functional differentiation in the lumbar vertebrae of four species of lorisids and five species of galagids. Linear and angular measurements of lumbar vertebrae were compared among taxa using canonical variates analysis (CVA) in conjunction with pairwise comparisons among selected variables. The results were interpreted in the context of a broader comparative sample, including the addition of indriids to the CVA. Compared to galagids, lorisids have relatively shorter lumbar spinous processes that are more perpendicularly (to caudally) oriented relative to a coronal plane. Lorisids also have relatively wider laminae and more transversely oriented prezygapophyses. These features promote lumbar stability and reflect antipronogrady, multiplane spinal movements, and upside-down suspension. Within lorisids, vertebral body length and height vary with body size, reflecting the additional resistance to bending that is required for larger body sizes. Galagid lumbar shape is influenced by body size, but does not show strong variation in accordance with positional behavior differences as defined here. Galagids, indriids, and lorisids are distinct in lumbar morphology and function, but their similarities in lumbar length reduction are suggestive of antipronograde postures in the common ancestor of the galagids, including those who have shifted to a more quadrupedal locomotor repertoire.     

Functional aspects of strepsirrhine lumbar vertebral bodies and spinous processes

The relationship between form and function in the lumbar vertebral column has been well documented among platyrrhines and especially catarrhines, while functional studies of postcranial morphology among strepsirrhines have concentrated predominantly on the limbs. This morphometric study investigates biomechanically relevant attributes of the lumbar vertebral morphology of 20 species of extant strepsirrhines. With this extensive sample, our goal is to address the influence of positional behavior on lumbar vertebral form while also assessing the effects of body size and phylogenetic history. The results reveal distinctions in lumbar vertebral morphology among strepsirrhines in functional association with their habitual postures and primary locomotor behaviors. In general, strepsirrhines that emphasize pronograde posture and quadrupedal locomotion combined with leaping (from a pronograde position) have the relatively longest lumbar regions and lumbar vertebral bodies, features promoting sagittal spinal flexibility. Indrids and galagonids that rely primarily on vertical clinging and leaping with orthograde posture share a relatively short (i.e., stable and resistant to bending) lumbar region, although the length of individual lumbar vertebral bodies varies phylogenetically and possibly allometrically. The other two vertical clingers and leapers, Hapalemur and Lepilemur, more closely resemble the pronograde, quadrupedal taxa. The specialized, suspensory lorids have relatively short lumbar regions as well, but the lengths of their lumbar regions are influenced by body size, and Arctocebus has dramatically longer vertebral bodies than do the other lorids. Lumbar morphology among galagonids appears to reflect a strong phylogenetic signal superimposed on a functional one. In general, relative length of the spinous processes follows a positively allometric trend, although lorids (especially the larger-bodied forms) have relatively short spinous processes for their body size, in accordance with their positional repertoire. The results of the study broaden our understanding of postcranial adaptation in primates, while providing an extensive comparative database for interpreting vertebral morphology in fossil primates.     

Additional postcranial elements of Teilhardina belgica: The oldest European primate

Teilhardina belgica is one of the earliest fossil primates ever recovered and the oldest fossil primate from Europe. As such, this taxon has often been hypothesized as a basal tarsiiform on the basis of its primitive dental formula with four premolars and a simplified molar cusp pattern. Until recently [see Rose et al.: Am J Phys Anthropol 146 (2011) 281–305; Gebo et al.: J Hum Evol 63 (2012) 205–218], little was known concerning its postcranial anatomy with the exception of its well‐known tarsals. In this article, we describe additional postcranial elements for T. belgica and compare these with other tarsiiforms and with primitive adapiforms. The forelimb of T. belgica indicates an arboreal primate with prominent forearm musculature, good elbow rotational mobility, and a horizontal, rather than a vertical body posture. The lateral hand positions imply grasps adaptive for relatively large diameter supports given its small body size. The hand is long with very long fingers, especially the middle phalanges. The hindlimb indicates foot inversion capabilities, frequent leaping, arboreal quadrupedalism, climbing, and grasping. The long and well‐muscled hallux can be coupled with long lateral phalanges to reconstruct a foot with long grasping digits. Our phyletic analysis indicates that we can identify several postcranial characteristics shared in common for stem primates as well as note several derived postcranial characters for Tarsiiformes. Am J Phys Anthropol 156:388–406, 2015. © 2014 Wiley Periodicals, Inc.     

Functional morphology of the postcranium and locomotor behavior of Neosaimiri fieldsi,a Saimiri-like Middle Miocene platyrrhine

A number of postcranial specimens of Neosaimiri fieldsi, a Middle Miocene platyrrhine, were discovered in 1988, 1989, and 1990 at La Venta, Colombia. Until recently only three postcranial specimens of this species had been discovered and the present material adds further information about this taxon's postcranial morphology. In overall skeletal dimensions and in postcranial features, Neosaimiri is most similar to Saimiri among extant medium-sized platyrrhines, but differs from Saimiri in having more rugose surface markings, a longer olecranon, 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 shorter distal calcaneus relative to the calcaneal tuberosity. These differences suggest that Neosaimiri was relatively heavily built, possessed a more dominant forelimb in quadrupedal progression, and utilized a less stabilized upper ankle joint, and a shorter power arm for plantarflexion. Neosaimiri is interpreted as an arboreal quadruped with frequent leaping across arboreal gaps, as in extant Saimiri, with perhaps less frequent running and leaping than in Saimiri. As with the dentition, the postcranial specimens suggest the close relationship between Neosaimiri and extant Saimiri. Am J Phys Anthropol 102:515–544, 1997. © 1997 Wiley-Liss, Inc.     

The petrosal of Omomys carteri and the evolution of the primate basicranium

The first omomyine petrosals, those of Omomys carteri, are described. Omomys probably had a tympanic bulla and canals for the intratympanic carotid circulation derived from the petrosal bone. The stapedial and promontory canals were complete, large and subequal. The posterior carotid foramen entered the bulla posteromedially. The intratympanic portion of the facial nerve was fully enclosed in bone, the stapedius fossa is extrabullar and the parotic fissure is patent. The mastoid was pneumatized from the epitympanic recess and a supracochlear cavity may have been present. The Omomys petrosals exhibit a generic omomyiform morphology, exhibiting no features that can be interpreted as autapomorphies and only one feature shared with adapiforms. The monophyly of Omomyiformes is based on other cranial characters, dental and postcranial characters assessed elsewhere. The similarity of the Shanghuang petrosal to the petrosals of omomyiforms, as well as the ambiguous evidence of its association, suggest that an omomyiform affinity for that petrosal cannot be ruled out.     

Postcranial adaptations for climbing in Loridae (Primates)

The Loridae are an arboreal family of small primates that are specialized for slow and quiet climbing. This paper examines the relationship between lorid locomotory behaviour and postcranial skeletal morphology. Lorid humeral and femoral diaphyseal geometric cross-sectional properties, articular surface areas, and lengths are compared to those properties in other small primates with less specialized locomotory behaviour. The comparative sample includes both closely related prosimians and more distantly related platyrrhines.
Results indicate that lorids have greater humeral and femoral diaphyseal rigidity than other quadrupedal primates of similar body size, suggesting that lorid limbs are subjected to greater forces. Lorids also have relatively larger humeral and femoral articulations, corresponding to field and laboratory observations which indicate that lorid joints are highly mobilc. In addition, lorids have long humeri relative to femoral length, and compared to humeral length in less specialized prosimians of similar body mass. Long humeral length relative to femoral length is interpreted as a climbing adaptation because similar limb proportions are also seen in many non-primate climbers. Altogether, humeral and femoral diaphyseal cross-sectional properties, articular surface areas, and lengths comprise a suite of characters which have potential for identifying climbing specialists in the fossil record.     

Postcranial functional morphology of Morotopithecus bishopi, with implications for the evolution of modern ape locomotion

The large-bodied hominoid from Moroto, Uganda has until recently been known only from proconsulid like craniodental remains and some vertebrae with modern ape like features. The discovery of two partial femora and the glenoid portion of a scapula demonstrates that the functional anatomy of Morotopithecus differed markedly from other early and middle Miocene hominoids. Previous studies have consistently associated the vertebral remains with a short, stiff back and with orthograde postures. Although the proximal femur more closely resembles the femora of monkeys than of apes and suggests a moderate degree of hip abduction, the distal femur resembles those of extant large bodied apes and suggests a varied loading regime and an arboreal repertoire that may have included substantial vertical climbing. The femoral shaft displays uniformly thick cortical bone, beyond the range of thickness seen in extant primates, and signifies higher axial loading than is typical of most extant primates. The glenoid fossa is broad and uniformly curved as in extant suspensory primates. Overall, Morotopithecus is reconstructed as an arboreal species that probably relied on forelimb-dominated, deliberate and vertical climbing, suspension and quadrupedalism. Morotopithecus thus marks the first appearance of certain aspects of the modern hominoid body plan by at least 20 Ma. If the suspensory and orthograde adaptations linking Morotopithecus to extant apes are synapomorphies, Morotopithecus may be the only well-documented African Miocene hominoid with a close relationship to living apes and humans.     

Comparative postcranial body shape and locomotion in Chlorocebus aethiops and Cercopithecus mitis

Body weight and length, chest girth, and seven postcranial limb segment lengths are compared between two guenon species, Chlorocebus (Cercopithecus) aethiops (vervets) and Cercopithecus mitis (blue monkeys), exhibiting different habitual locomotor preferences. The subjects, all adults, were wild caught for a non-related research project (Turner et al. [1986] Genetic and morphological studies on two species of Kenyan monkeys, C. aethiops and C. mitis. In: Else JG, Lee PC, editors. Primate evolution, proceedings of the Xth International Congress of Primatology, Cambridge. London). The morphological results are interpreted within the context of previously published observations of primate locomotion and social organization. The sample is unique in that the body weight of each individual is known, allowing the effects of body-size scaling to be assessed in interspecific and intersexual comparisons. C. mitis has a significantly (P < 0.05) greater body weight and trunk length than C. aethiops. A shorter trunk may function to reduce spinal flexibility for ground-running in the latter. Proximal limb segments (arm and thigh) are significantly greater in C. mitis, reflecting known adaptations to committed arboreal quadrupedal locomotion. By contrast, relative distal limb segments (forearm, crus, and foot) are significantly longer in C. aethiops, concordant with a locomotor repertoire that includes substantial terrestrial quadrupedalism, in addition to arboreal agility, and also the requisite transition between ground and canopy. Although normally associated with arboreal monkeys, greater relative tail length occurs in the more terrestrial vervets. However, because vervets exploit both arboreal and terrestrial habitats, a longer tail may compensate for diminished balance during arboreal quadrupedalism resulting from the greater "brachial" and "crural" indices that enhance their ground quadrupedalism. Most interspecific differences in body proportions are explicable by differences in locomotor modalities. Some results, however, contradict commonly held "tenets" that relate body size and morphology exclusively to locomotion. Generally associated with terrestriality, sexual dimorphism (male/female) is greater in the more arboreal blue monkeys. A more intense, seasonal mating competition may account for this incongruity.     

Comparative locomotion of six sympatric primates in Ecuador

Primates exhibit a great variety of arboreal locomotor modes associated with their size and postcranial morphology. The study of sympatric primates is interesting in that it may reveal how primates of different sizes and anatomies move and select for forest structure. This study reports on preliminary data on the locomotion of six non-ateline platyrrhines found in the Yasuni National Park, Napo Province, Ecuador. Pygmy marmosets are confined to the understory using scansorial locomotion and quadrupedalism, preferring large vertical supports. Golden-mantled tamarins, common squirrel monkeys and dusky titis also range in the understory, moving by quadrupedal walk and leap, mainly on small horizontal supports. Monk sakis are found in the main canopy and use quadrupedal walk and less leap on medium-sized horizontal supports. Whitefronted capuchins use the understory and the main canopy equally often, walking quadrupedally and leaping on small and medium-sized oblique supports. In general, smaller species occupy lower strata while larger species tend to spend more time in the upper strata. Small tegulae-bearing monkeys showed the highest proportions of large vertical support use. For all species, leaping was the main gap-crossing mode, though decreasing in proportion with a higher use of the upper forest layers.     

Positional behavior of long-tailed macaques (Macaca fascicularis) in northern Sumatra

Although the majority of extant primates are described as "quadrupedal," there is little information available from natural habitats on the locomotor and postural behavior of arboreal primate quadrupeds that are not specialized for leaping. To clarify varieties of quadrupedal movement, a quantitative field study of the positional behavior of a highly arboreal cercopithecine, Macaca fascicularis, was conducted in northern Sumatra. At least 70% of locomotion in travel, foraging, and feeding was movement along continuous substrates by quadrupedalism and vertical climbing. Another 14-25% of locomotion was across substrates by pronograde clambering and vertical clambering. The highest frequency of clambering occurred in foraging for insects, and on the average smaller substrates were used in clambering than during quadrupedal movement. All postural behavior during foraging and feeding was above-substrate, largely sitting. Locomotion across substrates requires grasping branches of diverse orientations, sometimes displaced away from the animal's body. The relatively low frequency of across-substrate locomotion appears consistent with published analyses of cercopithecoid postcranial morphology, indicating specialization for stability of limb joints and use of limbs in parasagittal movements, but confirmation of this association awaits interspecific comparisons that make the distinction between along- and across-substrate forms of locomotion. It is suggested that pronograde clambering as defined in this study was likely a positional mode of considerable importance in the repertoire of Proconsul africanus and is a plausible early stage in the evolution of later hominoid morphology and locomotor behavior.     

The relationship between locomotor behavior and limb morphology in brown (Cebus apella) and weeper (Cebus olivaceus) capuchins

This study is a comparison of locomotor behavior and postcranial form in two species of capuchin monkey, the brown capuchin (Cebus apella), and the weeper capuchin (Cebus olivaceus). Behavioral data from groups of wild C. apella and C. olivaceus in Guyana were collected during the period of December 1999 through November 2000. Postcranial variables including 40 measurements and three indices were taken from 43 adult and subadult specimens of C. apella and 14 adult and subadult specimens of C. olivaceus housed in American museums, as well as two wild-caught adult specimens of C. olivaceus from the Georgetown Zoo in Guyana. The results of this study indicate that these two capuchins exhibit similar patterns of locomotor behavior, but that there are important differences in how they move through their homerange, particularly with respect to quadrupedalism. These differences in behavior are reflected in their postcranial morphology and can be related to differences in foraging strategies. This study provides an example of the importance of using more exclusive categories of quadrupedal behaviors when comparing closely related arboreal quadrupeds, as well as an alternative explanation for some of the postcranial features of C. apella that may relate to foraging postures and foraging strategy rather than traditionally categorized patterns of locomotor behavior.     

Hindlimb adaptations in Ourayia and Chipetaia, relatively large-bodied omomyine primates from the Middle Eocene of Utah

North American omomyids represent a tremendous Eocene radiation of primates exhibiting a wide range of body sizes and dietary patterns. Despite this adaptive diversity, relatively little is known of the postcranial specializations of the group. Here we describe hindlimb and foot bones of Ourayia uintensis and Chipetaia lamporea that were recovered from the Uinta B member (early Uintan Land Mammal Age), Uinta Formation, Utah. These specimens provide insights into the evolution of postcranial adaptations across different body sizes and dietary guilds within the Eocene primate radiation. Body mass estimates based on talar measurements indicate that Ourayia uintensis and Chipetaia lamporea weighed about 1,500-2,000 g and 500-700 g, respectively. Skeletal elements recovered for Ourayia include the talus, navicular, entocuneiform, first metatarsal, and proximal tibia; bones of Chipetaia include the talus, navicular, entocuneiform, and proximal femur. Both genera had opposable grasping big toes, as indicated by the saddle-shaped joint between the entocuneiform and first metatarsal. Both taxa were arboreal leapers, as indicated by a consistent assemblage of characters in all represented bones, most notably the somewhat elongated naviculars, the high and distinct trochlear crests of the talus, the posteriorly oriented tibial plateau (Ourayia), and the cylindrical head of the femur (Chipetaia). The closest resemblances to Ourayia and Chipetaia are found among the Bridger omomyines, Omomys and Hemiacodon. The results of our comparisons suggest that the later, larger, more herbivorous omomyines from Utah retained a skeletal structure characteristic of earlier, smaller North American omomyids.     

Taxonomic affinities of the Eppelsheim femur

The taxonomic affinities of the Eppelsheim femur, known as Paidopithex, have been unclear for more than a century. Over the years, due to similarities with Pliopithecus, some authors have considered it a large pliopithecid, while others refer to it as Dryopithecus. The issue could not be resolved, because no definitive Dryopithecus femora were available. With the discovery of the Dryopithecus laietanus skeleton from Can Llobateres (CLl 18800), it has become possible to test the attribution of the Eppelsheim femur to Dryopithecus on the basis of direct morphological and metrical comparisons. By means of allometric techniques, we show that the Eppelsheim and D. laietanus femora fit different hindlimb morphologies with regard to relative length and relative head/neck size, with Paidopithex significantly differing from Dryopithecus, but more closely resembling Pliopithecus. Paidopithex also differs from Dryopithecus in other important aspects, such as its lower neck/shaft angle, lack of elevation of the femoral head above the greater trochanter, more posteriorly oriented lesser trochanter, and proximal shaft diameter thicker anteroposteriorly than mediolaterally. In these features, Paidopithex most closely resembles Pliopithecus in spite of differences in body mass (ca. 22 kg vs. ca. 10 kg, respectively). These features suggest that Paidopithex used a primitive locomotor pattern associated with arboreal quadrupedalism, instead of the more derived pattern displayed by Dryopithecus. Currently available evidence confirms that the attribution of Paidopithex to Dryopithecus can be rejected. Paidopithex could be a large and otherwise unknown pliopithecid, but the possibility cannot be ruled out that it represents a third kind of catarrhine.     

Knuckle-walking in Sivapithecus? The combined effects of homology and homoplasy with possible implications for pongine dispersals

Sivapithecus is a Miocene great ape from South Asia that is orangutan-like cranially but is distinctive postcranially. Work by others shows that the humerus resembles large terrestrial cercopithecoids proximally and suspensory hominoids distally, but most functional interpretations nevertheless situate Sivapithecus in an arboreal setting. We present a new quantitative analysis of the Sivapithecus capitate and hamate. Though the functional morphology of both bones suggests some degree of arboreality, the overall morphology is most similar to knuckle-walking African apes. Other features of the Sivapithecus humerus and hind limb are also functionally consistent with knuckle-walking, and we suggest that this locomotor behavior is a valid alternative functional interpretation of the postcranial morphology. We speculate that knuckle-walking in Sivapithecus would have evolved independently from African apes, perhaps for similar ecological reasons. The discovery of a possible pongine knuckle-walker challenges the hypotheses that (1) knuckle-walking evolved only once in hominoids and (2) knuckle-walking is too highly specialized to be the positional behavior from which human bipedalism evolved. The possibility of knuckle-walking in Sivapithecus may help to explain not only the curious combination of characters that typify the postcranium but also the unique postcranial morphology of extant Pongo. Furthermore, it may clarify the distribution of fossil pongines across many ecological zones in Eurasia in the Miocene and Pleistocene, as well as, independently, the spread of African apes across a diversity of environments in equatorial Africa.     

Postcranial adaptation and evolution in lorisidae

With the exception of leaping, lorises and galagos move in many similar ways although frequencies and styles differ. This peculiar locomotor distinction in two closely related subfamilies has profoundly altered their respective postcranial anatomies from their common ancestor. A comparison of postcranial adaptation in extant forms shows that lorises and galagos differ somewhat in forelimb mobility, but are more fundamentally disparate in hindlimb adaptation. Inferences concerning locomotor adaptation in the lorisid fossil record indicate a more generalized locomotor pattern which is more like that of extant cheirogaleids than either living galagos or lorises. Thus, vertical clinging and leaping in galagines and the slow-climbing and suspensory movements of lorisines appear to be evolutionarily recent innovations from a more generalized locomotor past.