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.     

Brief communication: Forelimb compliance in arboreal and terrestrial opossums

Primates display high forelimb compliance (increased elbow joint yield) compared to most other mammals. Forelimb compliance, which is especially marked among arboreal primates, moderates vertical oscillations of the body and peak vertical forces and may represent a basal adaptation of primates for locomotion on thin, flexible branches. However, Larney and Larson (Am J Phys Anthropol 125 [2004] 42–50) reported that marsupials have forelimb compliance comparable to or greater than that of most primates, but did not distinguish between arboreal and terrestrial marsupials. If forelimb compliance is functionally linked to locomotion on thin branches, then elbow yield should be highest in marsupials relying on arboreal substrates more often. To test this hypothesis, we compared forelimb compliance between two didelphid marsupials, Caluromys philander (an arboreal opossum relying heavily on thin branches) and Monodelphis domestica (an opossum that spends most of its time on the ground). Animals were videorecorded while walking on a runway or a horizontal 7‐mm pole. Caluromys showed higher elbow yield (greater changes in degrees of elbow flexion) on both substrates, similar to that reported for arboreal primates. Monodelphis was characterized by lower elbow yield that was intermediate between the values reported by Larney and Larson (Am J Phys Anthropol 125 [2004] 42–50) for more terrestrial primates and rodents. This finding adds evidence to a model suggesting a functional link between arboreality—particularly locomotion on thin, flexible branches—and forelimb compliance. These data add another convergent trait between arboreal primates, Caluromys, and other arboreal marsupials and support the argument that all primates evolved from a common ancestor that was a fine‐branch arborealist. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

Comparative locomotion and habitat use of six monkeys in the Tai Forest,Ivory Coast

The relationships between locomotion, body size, and habitat use in six sympatric Old World monkeys are examined to test whether the associations found are consistent with those demonstrated in previous studies (Fleagle and Mittermeier [1980] Am. J. Phys. Anthropol. 52:301–314; Gebo and Chapman [1995] Am. J. Phys. Anthropol. 97:49–76). Colobus polykomos, C. badius, C. verus, Cercopithecus diana, C. campbelli, and Cercocebus atys were studied for 14 months in the Ivory Coast's Tai Forest. Analyses reveal that (1) larger monkeys tend to frequent those strata containing the greatest densities of large supports while smaller monkeys are more diverse in their canopy use; (2) high frequencies of leaping are not necessarily confined to the understory, and understory specialists are not necessarily frequent leapers; (3) body size does not consistently predict leaping or climbing frequencies; (4) in general, climbing is more frequent during foraging and leaping is more common during travel; (5) larger supports are used during travel while smaller supports are used during foraging; and (6) larger monkeys do not always use larger supports than do smaller monkeys. Some of the factors contributing to the manner that locomotion, body size, and habitat use are related in cercopithecid monkeys are discussed. Am J Phys Anthropol 105:493–510, 1998. © 1998 Wiley-Liss, Inc.     

Brief communication: Swimming and diving behavior in apes (Pan troglodytes and Pongo pygmaeus): First documented report

Extant hominoids, including humans, are well known for their inability to swim instinctively. We report swimming and diving in two captive apes using visual observation and video recording. One common chimpanzee and one orangutan swam repeatedly at the water surface over a distance of 2–6 m; both individuals submerged repeatedly. We show that apes are able to overcome their negative buoyancy by deliberate swimming, using movements which deviate from the doggy‐paddle pattern observed in other primates. We suggest that apes' poor swimming ability is due to behavioral, anatomical, and neuromotor changes related to an adaptation to arboreal life in their early phylogeny. This strong adaptive focus on arboreal life led to decreased opportunities to interact with water bodies and consequently to a reduction of selective pressure to maintain innate swimming behavior. As the doggy paddle is associated with quadrupedal walking, a deviation from terrestrial locomotion might have interfered with the fixed rhythmic action patterns responsible for innate swimming. Am J Phys Anthropol 152:156–162, 2013. © 2013 Wiley Periodicals, Inc.     

Deciduous dental morphology of the prehistoric Jomon people of Japan: Comparison of nonmetric characters

Morphological variations of the deciduous dentition are as useful as those of the permanent dentition for determining the biological affinities of human populations. This paper provides material on morphological variations of deciduous teeth of the prehistoric Japanese population from the Late and the Latest Jomon Period (ca. 2000–ca. 300 B.C.). The expression of nonmetric traits of the deciduous teeth in the Jomon sample shows a closer affinity with modern Japanese and Native American samples than with American White, Asiatic Indian, and African samples. However, the frequency of shoveling in deciduous upper incisors in the Jomon sample is lower than those in modern Japanese and Native American samples. The Jomon sample also expresses a much higher frequency of cusp 6 in deciduous lower second molars than seen in modern Japanese, Ainu, and Native American samples. The frequency in the Jomon sample is equal to that in the Australian Aboriginal sample, which shows cusp 6 most frequently among the samples compared. A somewhat low incidence of incisor shoveling in the Jomon sample was also reported in the permanent dentition (Turner [1976] Science 193:911–913, [1979] Am. J. Phys. Anthropol. 51:619–635, [1987] Am. J. Phys. Anthropol. 73:305–321, [1990] Am. J. Phys. Anthropol. 82:295–317; T. Hanihara [1992] Am. J. Phys. Anthropol. 88:163–182, 88:183–196). However, the frequency of cusp 6 in the Jomon sample shows no significant difference from those of Northeast Asian or Native American samples in the permanent dentition (Turner [1987] Am. J. Phys. Anthropol. 73:305–321; T. Hanihara [1992] Am. J. Phys. Anthropol. 88:1–182, 88:183–196). Evidently, some nonmetric traits express an inter-group difference only in the deciduous dentition. © 1995 Wiley-Liss, Inc.     

Substrate determines asymmetrical gait dynamics in marmosets (Callithrix jacchus) and squirrel monkeys (Saimiri boliviensis)

Studies of skeletal pathology indicate that injury from falling accounts for most long bone trauma in free‐ranging primates, suggesting that primates should be under strong selection to manifest morphological and behavioral mechanisms that increase stability on arboreal substrates. Although previous studies have identified several kinematic and kinetic features of primate symmetrical gaits that serve to increase arboreal stability, very little work has focused on the dynamics of primate asymmetrical gaits. Nevertheless, asymmetrical gaits typify the rapid locomotion of most primates, particularly in smaller bodied taxa. This study investigated asymmetrical gait dynamics in growing marmosets and squirrel monkeys moving on terrestrial and simulated arboreal supports (i.e., an elevated pole). Results showed that monkeys used several kinematic and kinetic adjustments to increase stability on the pole, including reducing peak vertical forces, limiting center of mass movements, increasing substrate contact durations, and using shorter and more frequent strides (thus limiting disruptive whole‐body aerial phases). Marmosets generally showed greater adjustment to pole locomotion than did squirrel monkeys, perhaps as a result of their reduced grasping abilities and retreat from the fine‐branch niche. Ontogenetic increases in body size had relatively little independent influence on asymmetrical gait dynamics during pole locomotion, despite biomechanical theory suggesting that arboreal instability is exacerbated as body size increases relative to substrate diameter. Overall, this study shows that 1) symmetrical gaits are not the only stable way to travel arboreally and 2) small‐bodied primates utilize specific kinematic and kinetic adjustments to increase stability when using asymmetrical gaits on arboreal substrates. Am J Phys Anthropol, 2009. © 2008 Wiley‐Liss, Inc.     

Ontogeny of the hominoid scapula: The influence of locomotion on morphology

Primate shoulder morphology has been linked with locomotor habits, oftentimes irrespective of phylogenetic heritage. Among hominoids, juvenile African apes are known to climb more frequently than adults, while orangutans and gibbons maintain an arboreal lifestyle throughout ontogeny. This study examined if these ontogenetic locomotor differences carry a morphological signal, which should be evident in the scapulae of chimpanzees and gorillas but absent in taxa that do not display ontogenetic behavioral shifts. The scapular morphology of five hominoid primates and one catarrhine outgroup was examined throughout ontogeny to evaluate if scapular traits linked with arboreal activities are modified in response to ontogenetic behavioral shifts away from climbing. Specifically, the following questions were addressed: 1) which scapular characteristics distinguish taxa with different locomotor habits; and 2) do these traits show associated changes during development in taxa known to modify their behavioral patterns? Several traits characterized suspensory taxa from nonsuspensory forms, such as cranially oriented glenohumeral joints, obliquely oriented scapular spines, relatively narrow infraspinous fossae, and inferolaterally expanded subscapularis fossae. The relative shape of the dorsal scapular fossae changed in Pan, Gorilla, and also Macaca in line with predictions based on reported ontogenetic changes in locomotor behavior. These morphological changes were mostly distinct from those seen in Pongo, Hylobates, and Homo and imply a unique developmental pattern, possibly related to ontogenetic locomotor shifts. Accordingly, features that sorted taxa by locomotor habits and changed in concert with ontogenetic behavioral patterns should be particularly useful for reconstructing the locomotor habits of fossil forms. Am J Phys Anthropol 152:239–260, 2013. © 2013 Wiley Periodicals, Inc.     

Orangutans use compliant branches to lower the energetic cost of locomotion

Within the forest canopy, the shortest gaps between tree crowns lie between slender terminal branches. While the compliance of these supports has previously been shown to increase the energetic cost of gap crossing in arboreal animals (e.g. Alexander 1991 Z. Morphol. Anthropol. 78, 315-320; Demes et al. 1995 Am. J. Phys. Anthropol. 96, 419-429), field observations suggest that some primates may be able to use support compliance to increase the energetic efficiency of locomotion. Here, we calculate the energetic cost of alternative methods of gap crossing in orangutans (Pongo abelii). Tree sway (in which orangutans oscillate a compliant tree trunk with increasing magnitude to bridge a gap) was found to be less than half as costly as jumping, and an order of magnitude less costly than descending the tree, walking to the vine and climbing it. Observations of wild orangutans suggest that they actually use support compliance in many aspects of their locomotor behaviour. This study seems to be the first to show that elastic compliance in arboreal supports can be used to reduce the energetic cost of gap crossing.     

Hindlimb suspension and hind foot reversal in Varecia variegata and other arboreal mammals

The foot, perhaps more than any other region of the primate body, reflects the interaction of positional behaviors with the geometric properties of available supports. The ability to reverse the hind foot during hindlimb suspension while hanging from a horizontal support or descending a large diameter vertical trunk has been noted in many arboreal mammals, including primates. Observations of Varecia variegata in the wild and under seminatural conditions document hindlimb suspension in this lemurid primate. The kinematics and skeletal correlates of this behavior are examined. Analogy is made with the form and function exhibited by nonprimate mammalian taxa employing this behavior. Examples of carnivores and rodents display very similar adaptations of the tarsals while other mammals, such as the xenarthrans, accomplish a similar end by means of different morphologies. However, a suite of features is identified that is shared by mammals capable of hind foot reversal. Hindlimb suspension effectively increases the potential feeding space available to a foraging mammal and represents a significant, and often unrecognized, alternative adaptive strategy to forelimb suspension and prehensile-tail suspension in primates. Am J Phys Anthropol 103:85–102, 1997. © 1997 Wiley-Liss, Inc.     

Canine tip wear in male and female anthropoids

One component of the “dual selection hypothesis” (Greenfield [1992a] Year. Phys. Anthropol. 35:153–185) is that the tips of female canines are commonly blunted and more frequently so than those of conspecific males. Data derived from two randomly selected age-graded samples of Macaca fascicularis (n = 70) and Colobus badius (n = 59) show that at least 80% of the females exhibit tip blunting on one or both canines and that frequencies of blunting are far greater than those of conspecific males in both jaws. Sexual dimorphism in mandibular canine morphology and wear and other recently critiqued aspects of the “dual selection hypothesis” (Plavcan and Kelley [1996] Am. J. Phys. Anthropol. 99:379–387.) are also discussed. Am J Phys Anthropol 107:87–97. © 1998 Wiley-Liss, Inc.     

Femoral anatomy of Aegyptopithecus zeuxis,an early Oligocene anthropoid

Three partial femora from Quarries I and M of the early Oligocene Jebel Qatrani Formation in the Fayum of Egypt are attributed to Aegyptopithecus zeuxis on the basis of their appropriate size and anthropoid morphology. Compared with extant catarrhines, Aegyptopithecus is unusual in having a distinct gluteal tuberosity (third trochanter) and a relatively deep distal femoral articulation. In the estimated neck angle, Aegyptopithecus resembles arboreal quadrupeds rather than either leaping or suspensory primates. It seems likely that the femur of this species was relatively robust and short for its body mass. In aspects of its femoral anatomy, Aegyptopithecus is quite different from the parapithecid Apidium and more similar to Catopithecus from late Eocene deposits of the Fayum, and also to small hominoids from the Miocene of East Africa. Am J Phys Anthropol 106:413–424, 1998. © 1998 Wiley-Liss, Inc.     

Underestimating intraspecific variation: The problem with excluding Sts 19 from Australopithecus africanus

Two analyses conclude that Sts 19 cannot be accommodated within the Australopithecus africanus hypodigm (Kimbel and Rak [1993] In Kimbel and Martin [eds.]: Species, Species Concepts, and Primate Evolution. New York: Plenum, pp. 461–484; Sarmiento [1993] Am. J. Phys. Anthropol. [Suppl.] 16:173). Both studies exclude Sts 19 because it possesses synapomorphies with Homo. Furthermore, according to Kimbel and Rak (1993), including Sts 19 in A. africanus results in an unacceptably high degree of polymorphism. This study aims to refute the null hypothesis that Sts 19 belongs to A. africanus. Twelve basicranial characters, as defined and implemented in Kimbel and Rak's study, were scored for casts of seven A. africanus and seven Homo habilis basicranial specimens. These characters were also examined on specimens from a large (N = 87) sample of African pongids. Contrary to Kimbel and Rak's (1993) findings, the null hypothesis is not refuted. The degree of polymorphism among A. africanus with Sts 19 included is less than that seen in Pan troglodytes. In addition, Sts 19 shares only one apomorphy with Homo. However, when treated metrically, Sts 19's morphology for this character is not significantly divergent from other A. africanus specimens. Am J Phys Anthropol 105:461–480, 1998. © 1998 Wiley-Liss, Inc.     

Interlimb coordination,gait, and neural control of quadrupedalism in chimpanzees

Interlimb coordination is directly relevant to the understanding of the neural control of locomotion, but few studies addressing this topic for nonhuman primates are available, and no data exist for any hominoid other than humans. As a follow-up to Jungers and Anapol's ([1985] Am. J. Phys. Anthropol. 67:89–97) analysis on a lemur and talapoin monkey, we describe here the patterns of interlimb coordination in two chimpanzees as revealed by electromyography. Like the lemur and talapoin monkey, ipsilateral limb coupling in chimpanzees is characterized by variability about preferred modes within individual gaits. During symmetrical gaits, limb coupling patterns in the chimpanzee are also influenced by kinematic differences in hindlimb placement (“overstriding”). These observations reflect the neurological constraints placed on locomotion but also emphasize the overall flexibility of locomotor neural mechanisms. Interlimb coordination patterns are also species-specific, exhibiting significant differences among primate taxa and between primates and cats. Interspecific differences may be suggestive of phylogenetic divergence in the basic mechanisms for neural control of locomotion, but do not preclude morphological explanations for observed differences in interlimb coordination across species. Am J Phys Anthropol 102:177–186, 1997 © 1997 Wiley-Liss, Inc.     

Functional and adaptive significance of primate pads and claws: Evidence from New World anthropoids

This study tests predicted morphoclines in fingertip morphology among four small-bodied (<1 kg) New World monkeys (Saimiri sciureus, Leontopithecus rosalia, Callithrix jacchus, and Saguinus oedipus) in order to test previous functional and adaptive explanations for the evolution of flattened nails, expanded apical pads, and grasping extremities within the Order Primates. Small-bodied platyrrhines which frequently forage among small-diameter substrates are expected to possess 1) relatively expanded apical pads, 2) well-developed epidermal ridges, 3) distally broad terminal phalanges, and 4) reduced flexor and extensor tubercles compared to those species which use large-diameter arboreal supports more frequently for their locomotor and postural behaviors. Results show that as the frequency of small-branch foraging increases among taxa within this sample, relative distal phalanx breadth also increases but distal phalanx length, height, and flexor tubercle size decrease. Moreover, epidermal ridge development becomes more pronounced as the frequency of small-branch foraging increases. Terminal phalanx breadth and epidermal ridge complexity are both positively correlated with apical pad size. The large, flexible apical pad increases stability of the hand and foot on small-diameter arboreal supports because the pad can contact the substrate in several planes which, in turn, enables the pad to resist disruptive forces from different directions by friction and interlocking (Hildebrand, 1995). The observed morphoclines demonstrate that a gradient in form from claw- to nail-like tegulae exists among these taxa. Thus, the distinction between claw- and nail-bearing platyrrhines is essentially arbitrary. These observations corroborate Cartmill's (1972) functional and adaptive model for the loss of claws in primates: namely, expanded apical pads are required for habitual locomotor and postural behaviors on small-diameter supports whereas claws are more useful for positional behaviors on large-diameter substrates. Finally, results from this study support previous suggestions that the keeled tegulae of callitrichines represent a derived postural adaptation rather than a primitive retention from an ancestral eutherian condition. Am J Phys Anthropol 106:113–127, 1998. © 1998 Wiley-Liss, Inc.     

Angular momentum and arboreal stability in common marmosets (Callithrix jacchus)

Despite the importance that concepts of arboreal stability have in theories of primate locomotor evolution, we currently lack measures of balance performance during primate locomotion. We provide the first quantitative data on locomotor stability in an arboreal primate, the common marmoset (Callithrix jacchus), predicting that primates should maximize arboreal stability by minimizing side-to-side angular momentum about the support (i.e., L_sup). If net L_sup becomes excessive, the animal will be unable to arrest its angular movement and will fall. Using a novel, highly integrative experimental procedure we directly measured whole-body L_sup in two adult marmosets moving along narrow (2.5 cm diameter) and broad (5 cm diameter) poles. Marmosets showed a strong preference for asymmetrical gaits (e.g., gallops and bounds) over symmetrical gaits (e.g., walks and runs), with asymmetrical gaits representing >90% of all strides. Movement on the narrow support was associated with an increase in more “grounded” gaits (i.e., lacking an aerial phase) and a more even distribution of torque production between the fore- and hind limbs. These adjustments in gait dynamics significantly reduced net L_sup on the narrow support relative to the broad support. Despite their lack of a well-developed grasping apparatus, marmosets proved adept at producing muscular “grasping” torques about the support, particularly with the hind limbs. We contend that asymmetrical gaits permit small-bodied arboreal mammals, including primates, to expand “effective grasp” by gripping the substrate between left and right limbs of a girdle. This model of arboreal stability may hold important implications for understanding primate locomotor evolution. Am J Phys Anthropol 156:565–576, 2015. © 2014 Wiley Periodicals, Inc.     

Kinematic data on primate head and neck posture: Implications for the evolution of basicranial flexion and an evaluation of registration planes used in paleoanthropology

Kinematic data on primate head and neck posture were collected by filming 29 primate species during locomotion. These were used to test whether head and neck posture are significant influences on basicranial flexion and whether the Frankfurt plane can legitimately be employed in paleoanthropological studies. Three kinematic measurements were recorded as angles relative to the gravity vector, the inclination of the orbital plane, the inclination of the neck, and the inclination of the Frankfurt plane. A fourth kinematic measurement was calculated as the angle between the neck and the orbital plane (the head-neck angle [HNA]). The functional relationships of basicranial flexion were examined by calculating the correlations and partial correlations between HNA and craniometric measurements representing basicranial flexion, orbital kyphosis, and relative brain size (Ross and Ravosa [1993] Am. J. Phys. Anthropol. 91:305–324). Significant partial correlations were observed between relative brain size and basicranial flexion and between HNA and orbital kyphosis. This indicates that brain size, rather than head and neck posture, is the primary influence on flexion, while the degree of orbital kyphosis may act to reorient the visual field in response to variation in head and neck posture. Regarding registration planes, the Frankfurt plane was found to be horizontal in humans but inclined in all nonhuman primates. In contrast, nearly all primates (including humans) oriented their orbits such that they faced anteriorly and slightly inferiorly. These results suggest that for certain functional craniometric studies, the orbital plane may be a more suitable registration plane than Frankfurt “Horizontal.” Am J Phys Anthropol 108:205–222, 1999. © 1999 Wiley-Liss, Inc.     

Noninvasive molecular sexing: An evaluation and validation of the SRY‐ and amelogenin‐based method in three new lemur species

Many lemur species are arboreal, elusive, and/or nocturnal and are consequently difficult to approach, observe and catch. In addition, most of them are endangered. For these reasons, non‐invasive sampling is especially useful in primates including lemurs. A key issue in conservation and ecological studies is to identify the sex of the sampled individuals to investigate sex‐biased dispersal, parentage, social organization and population sex ratio. Several molecular tests of sex are available in apes and monkeys, but only a handful of them work in the lemuriform clade. Among these tests, the coamplification of the SRY gene with the amelogenin X gene using strepsirhine‐specific X primers seems particularly promising, but the reliability and validity of this sexing test have not been properly assessed yet. In this study, we (i) show that this molecular sexing test works on three additional lemur species (Microcebus tavaratra, Propithecus coronatus and P. verreauxi) from two previously untested genera and one previously untested family, suggesting that these markers are likely to be universal among lemurs and other strepsirrhines; (ii) provide the first evidence that this PCR‐based sexing test works on degraded DNA obtained from noninvasive samples; (iii) validate the approach using a large number of known‐sex individuals and a multiple‐tubes approach, and show that mismatches between the field sex and the final molecular consensus sex occur in less than 10% of all the samples and that most of these mismatches were likely linked to incorrect sex determinations in the field rather than genotyping errors. Am J Phys Anthropol, 2013. © 2013 Wiley Periodicals, Inc.