Subchondral Bone Apparent Density and Locomotor Behavior in Extant Primates and Subfossil Lemurs <Emphasis Type="Italic">Hadropithecus</Emphasis> and <Emphasis Type="Italic">Pachylemur</Emphasis>

We analyze patterns of subchondral bone apparent density in the distal femur of extant primates to reconstruct differences in knee posture, discriminate among extant species with different locomotor preferences, and investigate the knee postures used by subfossil lemur species Hadropithecus stenognathus and Pachylemur insignis. We obtained computed tomographic scans for 164 femora belonging to 39 primate species. We grouped species by locomotor preference into knuckle-walking, arboreal quadruped, terrestrial quadruped, quadrupedal leaper, suspensory and vertical clinging, and leaping categories. We reconstructed knee posture using an experimentally validated procedure of determining the anterior extent of the region of maximal subchondral bone apparent density on a median slice through the medial femoral condyle. We compared subchondral apparent density magnitudes between subfossil and extant specimens to ensure that fossils did not display substantial mineralization or degradation. Subfossil and extant specimens were found to have similar magnitudes of subchondral apparent density, thereby permitting comparisons of the density patterns. We observed significant differences in the position of maximum subchondral apparent density between leaping and nonleaping extant primates, with leaping primates appearing to use much more flexed knee postures than nonleaping species. The anterior placement of the regions of maximum subchondral bone apparent density in the subfossil specimens of Hadropithecus and Pachylemur suggests that both species differed from leaping primates and included in their broad range of knee postures rather extended postures. For Hadropithecus, this result is consistent with other evidence for terrestrial locomotion. Pachylemur, reconstructed on the basis of other evidence as a committed arboreal quadruped, likely employed extended knee postures in other activities such as hindlimb suspension, in addition to occasional terrestrial locomotion.     

The Emergence of an Endangered Species: Evolution and Phylogeny of the <Emphasis Type="Italic">Trachypithecus geei</Emphasis> of Bhutan

Golden langurs (Trachypithecus geei) are an endangered primate species in Bhutan. We discuss their evolution in terms of phylogeny, ecology, and biogeography. We test the hypothesis that rivers and mountains in Bhutan isolated a population of capped langurs (Trachypithecus pileatus) that later speciated into the morphologically distinct T. geei. Trachypithecus, the genus to which both capped and golden langurs belong, spread north from a paleorefuge in south China, and Semnopithecus (gray langurs) spread east and northward from a refuge in south India. We show that the 2 genera both arrived in Bhutan and were separated from each other by the Sunkosh River and Black Mountains. Likewise, a population of capped langurs isolated from parental populations by rivers speciated into the distinct golden langurs. We conducted field surveys covering the entire range of langurs in Bhutan. The Sunkosh River and Black Mountain range in west Bhutan isolate gray langurs and golden langurs from each other. In the east, the Manas River system (Manas-Mangde) served as a barrier between golden and capped langurs. However, it is an imperfect barrier and a contact zone between the 2 species occurred on the banks of the Mangde River. Second, we reconstructed the evolutionary history of the langurs of Bhutan via molecular phylogenetic tools. We sequenced the cytochrome b region (cyt b) of the mitochondrial DNA (mtDNA) to model a phylogeny. It revealed the distinct evolutionary paths of the golden, capped, and gray langurs. As predicted, golden and capped langurs are closely related to each other and to other species in Trachypithecus from Southeast Asia. The gray langur of Bhutan grouped into a distinct clade with conspecifics in Semnopithecus from India and Nepal. The south Indian clade of gray langurs is more ancient, with the Bhutan and Nepal gray langurs having diverged later, which fits with the glacial models of ice sheet retreats and colonization of South Asia by gray langurs from south India north toward the Himalayas. Likewise, the golden and capped langur clade are the most derived and divergent from the older groups of Trachypithecus in Southeast Asia, which also fits with paleorefuge models of recolonization by Trachypithecus into the rest of Southeast Asia and north toward the Himalayas from paleorefuges in Southeast Asia. As predicted, golden and capped langurs are closely related to each other and gray langurs are only distantly related to them. The divergence between capped and golden langurs is more recent, while the split between Trachypithecus and Semnopithecus is more ancient and took place before the Pliocene.     

Locomotor adaptations within the Cercopithecus Genus: a multivariate approach.

Multivariate analysis as a technique for investigating locomotor differentiation among primates has proven its power and usefulness in many studies on various skeletal dimensions. In these analyses primate genera were distributed and sometimes clustered in a manner that was interpretable based on current knowledge of gross locomotor differences. In an effort to advance our understanding of arboreality and terrestriality in primates, the present research involves a careful look for the most subtle morphological differences in locomotor behavior. It is believed that by looking at such subtle shape differences an understanding of what it means morphologically for a primate to be either more or less arboreal may be achieved. The species within the primate genus Cercopithecus were analyzed. This genus includes species which may be placed along a habitat (ground-living to tree-dwelling) or activity spectrum. The different habitats or activity patterns clearly require slight variations in patterns of movement, which in turn may require subtle structural adaptations. Multivariate analyses of 67 postcranial variables on seven species within the genus allowed detection of slight degrees of morphological variation. However, when morphological differences are small, size variance among specimens may take on an inflated importance. A substantial amount of work was devoted to finding the least biased method of removing size variance from the variables while incorporating a discrete size variable into the study. Using these transformed skeletal variables, interspecific groupings were discovered. Much of this infrastructure is then related to differing locomotor behavior and provides an insight into the fine structure of primate locomotor adaptation in an arboreal habitat.     

Raptors and primate evolution

Most scholars agree that avoiding predators is a central concern of lemurs, monkeys, and apes. However, given uncertainties about the frequency with which primates actually become prey, the selective importance of predation in primate evolution continues to be debated. 1 - 9 Some argue that primates are often killed by predators, 5 , 6 while others maintain that such events are relatively rare. 2 , 7 , 9 Some authors have contended that predation's influence on primate sociality has been trivial 10 , 11 ; others counter that predation need not occur often to be a powerful selective force. 12 - 14 Given the challenges of documenting events that can be ephemeral and irregular, we are unlikely ever to amass the volume of systematic, comparative data we have on such topics as feeding, social dynamics, or locomotor behavior. Nevertheless, a steady accumulation of field observations, insight gained from natural experiments, and novel taphonomic analyses have enhanced understanding of how primates interact with several predators, especially raptors, the subject of this review.     

Evolutionary aspects of primate locomotion

Both neontological and phylogenetic studies are necessary to interpret primate locomotion. Reference to palaeoprimatology and palaeocology, for instance, will lead to a fuller understanding of the roots of such gaits as the vertical clinging and leaping of Tarsius, Indri and Propithecus. Evolutionary trends in posture and locomotion are discussed. The postural trend has been towards maintenance of trunk verticality and the locomotor trend towards an increasing dependence on the forelimbs among arboreal primates. Three stages are recognized in the phylogenetic course of arboreal locomotor adaptation: Stage A. Vertical clinging and leaping; Stage B. Quadrupedalism; Stage C. Brachiation. The role of prehensility of the hand in the evolution of locomotor types is discussed in relation to forest morphology and, in particular, to stratification. Finally a scheme of evolution, set in the framework of ecology, for Old World Monkey groups is presented.     

Evolution of Primate Social Systems

We review evolutionary processes and mechanisms that gave rise to the diversity of primate social systems. We define social organization, social structure and mating system as distinct components of a social system. For each component, we summarize levels and patterns of variation among primates and discuss evolutionary determinants of this variation. We conclude that conclusive explanations for a solitary life and pair-living are still lacking. We then focus on interactions among the 3 components in order to identify main targets of selection and potential constraints for social evolution. Social organization and mating system are more closely linked to each other than either one is to social structure. Further, we conclude that it is important to seek a priori measures for the effects of presumed selective factors and that the genetic contribution to social systems is still poorly examined. Finally, we examine the role of primate socio-ecology in current evolutionary biology and conclude that primates are not prominently represented because the main questions asked in behavioral ecology are often irrelevant for primate behavior. For the future, we see a rapprochement of these areas as the role of disease and life-history theory are integrated more fully into primate socio-ecology.     

Patterns and Trends in Primate Pair Bonds

Pair-bonding may be a significant feature of the social repertoire of some primate species. However, discerning inter- and intraspecific pair bonds is problematic. I present an overview of the general behavior and ecology of species reported to occur in two-adult, pair-bonded groups. There is no two-adult grouped nonhuman primate species in Africa and only two types in Asia. Behavioral and ecological data suggest that the two-adult group or pair-bonding or both may have evolved separately 4–7 times. I propose that two pair-bond components—social pair bond and sexual pair bond—occur and can be defined and described in such a manner that facilitates comparative analysis across primate taxa. The evolution of grouping patterns in many two-adult grouped primates may be best modeled via evolutionary scenarios relying on direct dietary/energetic constraints, predation, and possibly mate-guarding. There is little support for the infanticide prevention and bodyguard hypotheses of female-choice models.     

Gut microbiome,diet, and conservation of endangered langurs in Sri Lanka

Understanding the mechanisms by which organisms respond to environmental change is critical to conservation biology. Recent research indicates that the gut microbiome may mediate mammalian responses to the environment and can be used as a biomarker to understand host ecological strategies. Here, we explore the relationship between the gut microbiome, host dietary niche, and potential resilience to habitat alteration using two closely related, sympatric non-human primate species: the tufted gray langur (Semnopithecus priam) and the purple-faced langur (Semnopithecus vetulus). The gray langur is suspected to be a habitat generalist less perturbed by anthropogenic disturbance, while the purple-faced langur is suspected to be a specialist more sensitive to disturbance. To test these characterizations, we assessed the gut microbiome using 16S rRNA gene amplicon sequencing of fecal samples collected from Kaludiyapokuna Forest Reserve, Sri Lanka (gray langur n = 50 samples, purple-faced langur n = 7 samples). Our results demonstrate that despite strong gut microbial similarities, gray langurs had a more diverse gut microbiome that harbored Prevotella and Akkermansia, taxa involved in starch degradation, while the purple-faced langur gut microbiome harbored Roseburia, Clostridium, and Ruminococcus, taxa involved in processing plant structural carbohydrates. Compared to related species in other locations, both Sri Lankan langurs harbored more pathogenic bacteria. These differences suggest that gray langurs have more generalist diets, making them more resilient to anthropogenic change, but also indicate that they are not impervious to human encroachment. Our findings suggest that microbiome analyses are an important tool for langur ecology and conservation, and should be integrated into ongoing studies.     

Major features in the evolution of early hominoid locomotion

Evolution of hominoid locomotion is a traditional topic in primate evolution. Views have changed during the last decade because a number of crucial differences between early and advanced hominoid morphologies have been demonstrated. Increasing evidence on primate behaviour and ecology show that any direct analogies between living and fossil hominoids must be made extremely carefully. The necessity of synthesizing data on primate behaviour, locomotion, morphology and ecology and simultaneously defining the framework in which the data should be interpreted are explained. Results of our studies of ontogeny of locomotor and behavioural patterns (LBP) are presented that could help identify the main features of early hominoid locomotor patterns (LP) and the mechanisms of their changes. The early hominoid LP was different from those of pronograde monkeys and specialized antipronograde living apes. Some similar features could be expected between early hominoid LP and the LP of ceboid monkeys. Analogous mechanisms of change of LBP exist in all groups of living higher primates. Crucial early mechanisms of change are the ontogenetic shifts in LBP connected with ethoecological changes. Analysis of fossil evidence has shown that Miocene hominoids differ morphologically from any group of living primates. Certain features present in Miocene hominoids could be found in Atelinae and living Asian apes but they are limited to some functional regions of the postcrania only. Consequently the early hominoid general LP can not be strictly analogous either to that of any monkey group or to the LP of apes. We suppose that certain pronograde adaptations, such as climbing, bipedality, limited suspensory activity and sitting constituted the main part of their LP.     

Differences in terrestrial velocity in Macaca and Presbytis

Over 150 sequences of terrestrial movement were timed and measured in the toque macaque, the gray langur, and the purple-faced langur to determine the relation between velocity, gait, and psychosocial context. Species differences were found in mean velocity, “favored” gait, and surface preference. All three species used the walk and the gallop at the slowest and fastest speeds respectively. The macaques and gray langurs walked frequently, but the purple-faced langurs were never seen to do so. At intermediate speeds, the macaques used either the “fast” walk or the “slow” gallop, whereas the gray langurs used irregular patterns of walk-gallop-walk-gallop. The purple-faced langurs were faster (about 20 fps) and less variable than the other species, regardless of distance. These data suggest that motor expression varies among the Cercopithecoid monkeys: the correlation between locomotion and anatomy is not as close as it is among wholly terrestrial or arboreal forms; slowness in the macaque is an expression of social confidence, not of biomechanical inability; high speed in the purple-faced langur is due to psychosocial factors rather than to “terrestrial” adaptability.     

Distribution and Population Densities of Diurnal Primates in the Karst Forests of Phong Nha – Ke Bang National Park,Quang Binh Province,Central Vietnam

We studied the status and distribution of the diurnal primates in the Phong Nha – Ke Bang National Park (PNKB NP) from April to August 2007. In the past, researchers reported 9 primate species and subspecies for the karst forests of PNKB NP, which constitutes the most important protected area for the endangered Hatinh langur (Trachypithecus hatinhensis) in Vietnam. All 9 primate taxa are threatened due to hunting pressure and habitat loss. We applied line transect sampling in 4 areas. During a total of 117 transect inspections along 12 different transect routes, we confirmed 5 primate taxa and the analysis of population densities resulted in 2143 (±467) Hatinh langurs, 1316 (±871) red-shanked douc langurs (Pygathrix nemaeus), 930 (±489) stump-tailed macaques (Macaca arctoides), 986 (±883) eastern Assamese macaques (M. a. assamensis), and 18 (±18) southern white-cheeked crested gibbons (Nomascus siki) in the whole PNKB NP, which covers an area of ca. 85,000 ha. We could not detect the 2 nocturnal lorises, Bengal slow lorises (Nycticebus bengalensis) and pygmy slow lorises (N. pygmaeus), as well as rhesus macaques (Macaca mulatta) and northern pig-tail macaques (M. leonina). The distribution of the primates predominantly depended on human impact. We could not recognize a correlation between habitat constitution and abundance of primates. The population density estimates showed a much higher density of the Hatinh langur than previously assumed. Thus the importance of the PNKB NP for the conservation of this endangered langur increased significantly.     

Interpreting the Role of Climbing in Primate Locomotor Evolution: Are the Biomechanics of Climbing Influenced by Habitual Substrate Use and Anatomy?

Vertical climbing is widely accepted to have played an important role in the origins of both primate locomotion and of human bipedalism. Yet, only a few researchers have compared climbing mechanics in quadrupedal primates that vary in their degree of arboreality. It is assumed that primates using vertical climbing with a relatively high frequency will have morphological and behavioral specializations that facilitate efficient climbing mechanics. We test this assumption by examining whether time spent habitually engaged in climbing influences locomotor parameters such as footfall sequence, peak forces, and joint excursions during vertical climbing. Previous studies have shown that during climbing, the pronograde and semiterrestrial Macaca fuscata differs in these parameters compared to the more arboreal and highly specialized, antipronograde Ateles geoffroyi. Here, we examine whether a fully arboreal, quadrupedal primate that does not regularly arm-swing will exhibit gait and force distribution patterns intermediate between those of Macaca fuscata and Ateles geoffroyi. We collected footfall sequence, limb peak vertical forces, and 3D hindlimb excursion data for Macaca fascicularis during climbing on a stationary pole instrumented with a force transducer. Results show that footfall sequences are similar between macaque species, whereas peak force distributions and hindlimb excursions for Macaca fascicularis are intermediate between values reported for M. fuscata and Ateles geoffroyi. These results support the notion that time spent climbing is reflected in climbing mechanics, even though morphology may not provide for efficient mechanics, and highlight the important role of arboreal locomotor activity in determining the pathways of primate locomotor evolution.     

Led by the nose: Olfaction in primate feeding ecology

Olfaction, the sense of smell, was a latecomer to the systematic investigation of primate sensory ecology after long years in which it was considered to be of minor importance. 1 This view shifted with the growing understanding of its role in social behavior 2 and the accumulation of physiological studies demonstrating that the olfactory abilities of some primates are on a par with those of olfactory‐dependent mammals such as dogs and rodents. 3 , 4 Recent years have seen a proliferation of physiological, behavioral, anatomical, and genetic investigations of primate olfaction. These investigations have begun to shed light on the importance of olfaction in the process of food acquisition. However, integration of these works has been limited. It is therefore still difficult to pinpoint large‐scale evolutionary scenarios, namely the functions that the sense of smell fulfills in primates’ feeding ecology and the ecological niches that favor heavier reliance on olfaction. Here, we review available behavioral and physiological studies of primates in the field or captivity and try to elucidate how and when the sense of smell can help them acquire food.     

Parasite community structure in sympatric Bornean primates

Parasites are important components of ecosystems, influencing trophic networks, competitive interactions and biodiversity patterns. Nonetheless, we are not nearly close to disentangling their complex roles in natural systems. Southeast Asia falls within global areas targeted as most likely to source parasites with zoonotic potential, where high rates of land conversion and fragmentation have altered the circulation of wildlife species and their parasites, potentially resulting in altered host-parasite systems. Although the overall biodiversity in the region predicts equally high, or even higher, parasite diversity, we know surprisingly little about wild primate parasites, even though this constitutes the first step towards a more comprehensive understanding of parasite transmission processes. Here, we characterise the gastrointestinal helminth parasite assemblages of a community of Bornean primates living along the Kinabatangan floodplain in Sabah (Malaysian Borneo), including two species endemic to the island. Through parasitological analyses, and by using several measures of parasite infection as proxies for parasite diversity and distribution, we show that (i) most parasite taxonomic groups are not limited to a single host, suggesting a greater flexibility for habitat disturbance, (ii) parasite infracommunities of nocturnal primates differ from their diurnal counterparts, reflecting both phylogenetic and ecological constraints, and (iii) soil-transmitted helminths such as whipworm, threadworm and nodule worm are widespread across the primate community. This study also provides new parasite records for southern pig-tailed macaques (Macaca nemestrina), silvered langurs (Trachypithecus cristatus) and Western tarsiers (Cephalopachus bancanus) in the wild, while adding to the limited records for the other primate species in the community. Given the information gap regarding primate-parasite associations in the region, the information presented here should prove relevant for future studies of parasite biodiversity and infectious disease ecology in Asia and elsewhere.     

Locomotion and Posture During Terminal Branch Feeding

We investigated locomotor and postural behavior during terminal branch feeding in order to gain a better understanding of the motor capabilities of primates. We videotaped wild, juvenile bonnet macaques (Macaca radiata) in India as they fed on flower nectar in a simal tree (Bombax malabaricum). Kinematic analysis revealed that they select specific support surfaces and movements that, for their body design and postures, maximize lateral stability and minimize the chances of falling. These choices are made even though the distance and duration of travel to a selected target are frequently increased. Our discussion focuses on particular concepts of how primates contend with balance problems arboreally, potential reasons for changes in footfall patterns, and how the tail contributes to arboreal locomotion and posture. We concluded that balance problems due to the ratio of body size to branch size are usually avoided, at least among juvenile bonnet macaques, by placing the hands and feet on branches extending laterally from the central support branch and not on the central branch itself. The lateral branches permit a wide base of support, which increases lateral stability. Second, juvenile bonnet macaques have a striking ability to rapidly and repeatedly adapt their gait patterns to changing substrate design with minimal interruption to overall progression. Third, primate tails that are not morphologically specialized for prehension nevertheless have important prehensile and sensory functions in arboreal locomotion and posture.     

中国石山叶猴生态学研究进展

喀斯特石山是一类特殊环境,生存在喀斯特石山的动物形成特殊的行为机制以适应这一特殊的环境.石山叶猴是仅分布于喀斯特石山地区的珍稀濒危灵长类动物,属疣猴亚科乌叶猴属的一个种组,包括黑叶猴(Trachypithecus francoisi)、白头叶猴(T.leucocephalus)、德氏叶猴(T.delacouri)、金头...     

Apparent density of the primate calcaneo‐cuboid joint and its association with locomotor mode,foot posture,and the “midtarsal break”

Primates use a range of locomotor modes during which they incorporate various foot postures. Humans are unique compared with other primates in that humans lack a mobile fore‐ and midfoot. Rigidity in the human foot is often attributed to increased propulsive and stability requirements during bipedalism. Conversely, fore‐ and midfoot mobility in nonhuman primates facilitates locomotion in arboreal settings. Here, we evaluated apparent density (AD) in the subchondral bone of human, ape, and monkey calcanei exhibiting different types of foot loading. We used computed tomography osteoabsorptiometry and maximum intensity projection (MIP) maps to visualize AD in subchondral bone at the cuboid articular surface of calcanei. MIPs represent 3D volumes (of subchondral bone) condensed into 2D images by extracting AD maxima from columns of voxels comprising the volumes. False‐color maps are assigned to MIPs by binning pixels in the 2D images according to brightness values. We compared quantities and distributions of AD pixels in the highest bin to test predictions relating AD patterns to habitual locomotor modes and foot posture categories of humans and several nonhuman primates. Nonhuman primates exhibit dorsally positioned high AD concentrations, where maximum compressive loading between the calcaneus and cuboid likely occurs during “midtarsal break” of support. Humans exhibit less widespread areas of high AD, which could reflect reduced fore‐ and midfoot mobility. Analysis of the internal morphology of the tarsus, such as subchondral bone AD, potentially offers new insights for evaluating primate foot function during locomotion. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

Electromyography of back muscles during quadrupedal and bipedal walking in primates

Despite the extensive electromyographic research that has addressed limb muscle function during primate quadrupedalism, the role of the back muscles in this locomotor behavior has remained undocumented. We report here the results of an electromyographic (EMG) analysis of three intrinsic back muscles (multifidus, longissimus, and iliocostalis) in the baboon (Papio anubis), chimpanzee (Pan troglodytes), and orangutan (Pongo pygmaeus) during quadrupedal walking. The recruitment patterns of these three back muscles are compared to those reported for the same muscles during nonprimate quadrupedalism. In addition, the function of the back muscles during quadrupedalism and bipedalism in the two hominoids is compared. Results indicate that the back muscles restrict trunk movements during quadrupedalism by contracting with the touchdown of one or both feet, with more consistent activity associated with touchdown of the contralateral foot. Moreover, despite reported differences in their gait preferences and forelimb muscle EMG patterns, primates and nonprimate mammals recruit their back muscles in an essentially similar fashion during quadrupedal walking. These quadrupedal EMG patterns also resemble those reported for chimpanzees, gibbons and humans (but not orangutans) walking bipedally. The fundamental similarity in back muscle function across species and locomotor behaviors is consistent with other data pointing to conservatism in the evolution of the neural control of tetrapod limb movement, but does not preclude the suggestion (based on forelimb muscle EMG and spinal lesion studies) that some aspects of primate neural circuitry are unique. © 1994 Wiley-Liss, Inc.     

Comparison of locomotor behaviour between white-headed langurs Trachypithecus leucocephalus and Francois' langurs T.fran(c)oisi in Fusui, China

We studied the locomotor behaviour of white-headed langurs Trachypithecus leucocephalus and Fran(c)ois' langurs T.fran(c)oisi to test two hypotheses: (1) these monkeys have evolved locomotor ability to support their activities on limestone hills,and (2) Fran(c)ois' langurs have evolved more diverse locomotor skills than white-headed langurs. Data were collected from 1996 - 1998 and in 2005 in Fusui Nature Reserve,Guangxi,and showed that the two species had similar locomotor types,but Francois' langurs had more locomotor modes (26) than white-headed langurs (12). Quadrupedal walking and leaping were two major types,and white-headed langurs were more arboreal than Fran(c)ois' langurs. We suggest that,while keeping their ancestral locomotor types,the two species have evolved new types allowing them to live on limestone cliffs. Compared to white-headed langurs,Francois' langurs have more diverse locomotor modes that probably have allowed them to live in more habitat types. As an evolutionary outcome,Fran(c)ois' langurs have a larger distribution range.