Quantitative Analysis of the Deltoid and Rotator Cuff Muscles in Humans and Great Apes

The shoulder is one of the anatomic regions differentiating orthograde primates (gibbons, orangutans, gorillas, chimpanzees, bonobos, and humans) from the rest of the pronograde primates. Orthograde primates are characterized by a dorsal position of the scapula and a more lateral orientation of the glenoid cavity. This anatomic pattern, together with adaptations in related osteological structures and muscles, serves to facilitate the elevation of the upper extremity in the scapular plane. We quantified the proportions of the muscles comprising the principal functional and stabilizing components of the glenohumeral joint —deltoid, subscapularis, supraspinatus, infraspinatus, and teres minor— in 3 species of orthograde primates: Pongo pygmaeus, Pan troglodytes, and Homo sapiens. Our objective was to determine whether quantifiable differences in these muscles relate to the functional requirements of the types of locomotion used by these 3 species: suspension/vertical climbing, knuckle-walking, and bipedalism. We observed a close similarity between the proportional mass of these muscles in Homo sapiens and Pongo pygmaeus, whereas Pan troglodytes displayed a unique anatomic pattern, particularly in the subscapularis, which may be due to differences in how the glenohumeral joint is stabilized in a great ape knuckle-walker. Our findings may help explain the high incidence of subacromial impingement syndrome in humans.     

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.     

The development of grooming,sociosexual behavior,play and aggression in captive baboons in their first two years

This paper focuses on the development of behavior in a mixed-longitudinal sample of 77 baboons (Papio sp. — 46 males and 31 females) from birth to 2 years of age. Eleven behaviors measured as frequency of performance and frequency of reception were used to test null hypotheses of gender and rearing differences among thePapio sp. subjects. The behaviors measured included: groom, mount, present, open-mouth threat, hard bite, displace, avoid, grapple, play bite, charge and chase. The data indicate that gender differences exist in the development of grooming, sociosexual behavior and aggression and play. The data also indicate that subjects raised in the nursery environment were behaviorally indistinguishable from mother-reared peers on the basis of the 11 behavioral criteria.     

Intestinal parasites of sympatric Pan troglodytes and Papio Spp. at two sites: Gombe (Tanzania) and Mt. Assirik (Senegal)

Experimental and clinical parasitology need natural baselines or “controls”. We present normative data intestinal parasite loads in two genera of African primates. Wild Pan troglodytes and Papio spp. were studied at two sites: Gombe in Tanzania (P. anubis) and Mt. Assirik in Senegal (P. papio). Presence or absence of parasites, especially nematodes, was recorded from fecal specimens. Gombe's primates were more often infected than were Mt. Assirik's. At Gombe, but not at Mt. Assirik, chimpanzees seemed to have a higher incidence of infection than baboons. Comparison of three baboon troops yielded apparent differences in prevalence of infection. No differences in infection were found between the wet and dry seasons in Mt. Assirik's chimpanzees.     

Gc subtypes identified by isoelectric focusing in Baboons (Papio hamadryas)

Summary Phenotyping for Gc variants by conventional electrophoresis in 835 Papio hamadryas baboons demonstrated a monomorphic population. Gc subtyping by polyacrylamide IEF gels, pH 4–6, on 394 of these baboons revealed the existence of two common alleles which we named Gc _Papio ¹ and Gc _Papio ² . Pedigree data confirmed the inheritance of a single locus, two allele system and the observed gene frequencies were 0.593 for Gc _Papio ¹ and 0.407 for Gc _Papio ² .     

Activity budget,home range and diet of the Colombian night monkey (Aotus lemurinus) in peri-urban forest fragments

Forest fragmentation and deforestation are major threats to primates at a global scale. The survival of primates in forest fragments largely depends on their behavioral and dietary flexibility, as well as their ability to use a modified matrix in anthropogenic landscapes, hence the importance of determining these ecological parameters in habitats with strong anthropic interventions. This paper aims to describe the activity budget and diet of two groups of the Colombian night monkey (Aotus lemurinus) and to estimate their home range in two peri-urban forest fragments in the city of Manizales, Colombia. We combined scan sampling and handheld GPS fixes in order to determine the behavioral, dietary and spatial patterns of the study groups. Night monkeys spent most of their time resting and traveling and were mainly frugivorous relying on at least 26 plant species in their diet. The most consumed plants included Persea americana, Cecropia angustifolia, Musa x paradisiaca, Cecropia telenitida, and Croton cf. mutisianus. Two of these plants are cultivated species and can provide important resources for populations in small forest fragments. Home range sizes were estimated at 1.7 to 1.8 hectares, using a grid count method. Our results suggest the potential adaptability that these primates have when exposed to anthropogenic habitat disturbances and habitat degradation. Nonetheless, future studies should evaluate the influence of demographic factors and resource availability on the behavioral, dietary and spatial patterns of A. lemurinus in peri-urban forests, in order to further understand their ability to cope with the pervasive processes of habitat fragmentation in the northern Andes.

     

Comparative 3D quantitative analyses of trapeziometacarpal joint surface curvatures among living catarrhines and fossil hominins

Comparisons of joint surface curvature at the base of the thumb have long been made to discern differences among living and fossil primates in functional capabilities of the hand. However, the complex shape of this joint makes it difficult to quantify differences among taxa. The purpose of this study is to determine whether significant differences in curvature exist among selected catarrhine genera and to compare these genera with hominin¹ fossils in trapeziometacarpal curvature. Two 3D approaches are used to quantify curvatures of the trapezial and metacarpal joint surfaces: (1) stereophotogrammetry with nonuniform rational B‐spline (NURBS) calculation of joint curvature to compare modern humans with captive chimpanzees and (2) laser scanning with a quadric‐based calculation of curvature to compare modern humans and wild‐caught Pan, Gorilla, Pongo, and Papio. Both approaches show that Homo has significantly lower curvature of the joint surfaces than does Pan. The second approach shows that Gorilla has significantly more curvature than modern humans, while Pongo overlaps with humans and African apes. The surfaces in Papio are more cylindrical and flatter than in Homo. Australopithecus afarensis resembles African apes more than modern humans in curvatures, whereas the Homo habilis trapezial metacarpal surface is flatter than in all genera except Papio. Neandertals fall at one end of the modern human range of variation, with smaller dorsovolar curvature. Modern human topography appears to be derived relative to great apes and Australopithecus and contributes to the distinctive human morphology that facilitates forceful precision and power gripping, fundamental to human manipulative activities. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc. ¹ The term “hominin” refers to members of the tribe Hominini, which includes modern humans and fossil species that are related more closely to modern humans than to extant species of chimpanzees, Wood and Lonergan (2008). Hominins are in the family Hominidae with great apes.     

Individual and social behavior in a captive troop of mandrills (mandrillus sphinx)

Little is known about the behavior of mandrills in the wild, and few captive studies have been conducted. Individual and social behaviors of six captive mandrills were categorized and quantified. The captive troop consisted of one adult male, two adult females and three infants. Behavioral categories were constructed during 150 hr of preliminary observations. One hundred and sixty-seven hours of quantitative data were collected over an eight-month period. Although much of the mandrill's behavioral repertoire is similar toPapio, some facial expressions, body postures and various social behaviors were found to be unique.     

A reassessment of the taxonomic status and phyletic relationships of Papio baringensis and Papio quadratirostris (Primates: Cercopithecidae)

Comparison of the skulls of Papio baringensis Leakey 1969 from the Chemeron Formation and P. quadratirostris Iwamoto 1982 from the Usno Formation with those of Theropithecus gelada, T. brumpti, T. darti, T. oswaldi, and several species of Papio indicate that the species from Chemeron and Usno exhibit all, or most, respectively, of the shared derived characters of Theropithecus. We propose that they be removed from Papio and placed in Theropithecus as T. baringensis and T. quadratirostris. Comparison of the specimens of T. baringensis and T. quadratirostris with those of T. brumpti indicate that the former two species have some of the derived characters of T. brumpti but are primitive in others. We propose that the three species form the following phyletic lineage: T. baringensis-T. quadratirostris-T. brumpti. With these referrals, there are now six species of the genus Theropithecus. Based on geologic grounds, the specimens from Chemeron are about 4.0 million years (m.y.), that from Usno between 3.3 and 3.4 m.y., and those of T. brumpti between 2.0 and 2.8 m.y. in age. We also show that the most complete specimen of Papio sp. nov. from Olduval Gorge belongs to T. oswaldi. With the removal of these specimens from Papio, the East African fossil record of this genus, apart from isolated teeth, comprises only 21 specimens, while that of Theropithecus comprises at least 300 specimens.     

Cercopithecoid primate postcranial fossils from Cooper's D,South Africa

Among several highly fossiliferous localities in the Bloubank Valley (Gauteng, South Africa), the Cooper's Cave System has been known since 1938 and has produced a rich fossil assemblage, including some remains of the early hominin Paranthropus robustus. In 2001, excavations began at a new locality, Cooper's D, which dates to ～1.4-1.5 Ma. Although hominins are relatively rare in the assemblage, remains of cercopithecoid primates are much more common. Craniodental fossils currently indicate the possible presence of at least three large-bodied cercopithecoid primate genera at Cooper's D: Gorgopithecus, Papio, and Theropithecus. In this study, we identify and describe > 100 cercopithecoid primate postcranial fossils representing all regions of the appendicular skeleton. The specimens come from several age classes and size morphs; more than one third of the fossils described are from sub-adult and juvenile individuals. The adult postcranial fossils vary substantially in size, with body masses estimated between 30 and 60 kg (from 16 of the better preserved specimens). The functional morphology of the postcranial remains indicate that these elements come from animals that likely utilized terrestrial substrates, but they remain difficult to definitively attribute to Gorgopithecus, Theropithecus, or Papio given the absence of associated skeletons. The smaller specimens likely belong to Papio while the larger ones can be attributed to the other two genera. Because Cooper's D has also yielded fossils of the early hominin Paranthropus robustus, this raises the question of how these four large-bodied, mostly terrestrial primates sympatrically utilized the landscape.     

Ontogeny and homoplasy in the papionin monkey face

SUMMARY Recent molecular research has provided a consistent estimate of phylogeny for the living papionin monkeys (Cercocebus, Lophocebus, Macaca, Mandrillus, Papio, and Theropithecus). This phylogeny differs from morphological phylogenies regarding the relationships of the mangabeys (Cercocebus and Lophocebus) and baboons (Mandrillus, Papio, and Theropithecus). Under the likely assumption that the molecular estimate is correct, the incongruence between the molecular and morphological data sets indicates that the latter include numerous homoplasies. Knowledge of how these homoplasies emerge through development is important for understanding the morphological evolution of the living papionins, and also for reconstructing the phylogenetic relationships and adaptations of their fossil relatives. Accordingly, we have used geometric morphometric techniques and the molecular phylogeny to investigate the ontogeny of a key area of morphological homoplasy in papionins, the face. Two analyses were carried out. The first compared allometric vectors of Cercocebus, Lophocebus, Macaca, Mandrillus, and Papio to determine which of the facial resemblances among the genera are homoplasic and which are plesiomorphic. The second analysis focused on early post‐natal facial form in order to establish whether the facial homoplasies exhibited by the adult papionins are to some degree present early in the post‐natal period or whether they develop only later in ontogeny. The results of our analyses go some way to resolving the debate over which papionin genera display homoplasic facial similarities. They strongly suggest that the homoplasic facial similarities are exhibited by Mandrillus and Papio and not by Cercocebus and Lophocebus, which share the putative primitive state with Macaca. Our results also indicate that Mandrillus and Papio achieve their homoplasic similarities in facial form not through simple extension of the ancestral allometric trajectory but through a combination of an extension of allometry into larger size ranges and a change in direction of allometry away from the ancestral trajectory. Thus, the face of Mandrillus is not simply a hypermorphic version of the face of its sister taxon, Cercocebus, and the face of Papio is not merely a scaled‐up version of the face of its sister taxon, Lophocebus. Lastly, our results show that facial homoplasy is not restricted to adult papionins; it is also manifest in infant and juvenile papionins. This suggests that the homoplasic facial similarities between Mandrillus and Papio are unlikely to be a result of sexual selection.     

Ecological niche differences betweenAlouatta palliata andCebus capucinus comparing feeding modes,branch use,and diet

During the wet season, two sympatric species of primates,Alouatta palliata (mantled howlers) andCebus capucinus (white-faced capuchins), were assayed for feeding niche differences through behavioral and habitat use patterns at Refugio de Fauna Silvestre Curu in Costa Rica. Differences in the use of relative diameter and thickness of branches and five different modes of feeding were compared between the species. White-faced capuchins used more manipulative modes of obtaining food, a wider range of arboreal habitat, and had a more diverse diet than mantled howlers. Mantled howlers may be more restricted than white-faced capuchins in arboreal microhabitat use due to their possible need for large support branches during feeding bouts and resting periods. We report that differences in feeding behaviors, diet, and arboreal habitat use seem to play a large role in separating these species niches.     

Fossil papio cranium from !Ncumtsa (Koanaka) Hills, western Ngamiland, Botswana

Three fossils, a cranium of Papio, a cercopithecid frontal bone, and a mandible of juvenile Papio, have been recovered from cave deposits in the !Ncumtsa (Koanaka) Hills of western Ngamiland, Botswana. These specimens are significant because well‐preserved crania of Papio are extremely rare in the fossil record outside of South Africa and because this is the first report of fossil primate cranial remains from Botswana. Thermoluminescence dating of surrounding cave matrix indicates an age of ≥317 ± 114 ka, within the Middle Pleistocene, although it may be older. Based on univariate and multivariate analyses, the adult !Ncumtsa specimen falls within the range of variation seen in extant forms of Papio, yet is distinct from any living species/subspecies and represents a new taxon, named here as a new subspecies of Papio hamadryas—Papio hamadryas botswanae. Am J Phys Anthropol, 2012. © 2012 Wiley Periodicals, Inc.     

Sociosexual behavioral patterns involving nulliparous female orangutans (Pongo sp.) reflect unique challenges during the adolescent period

The primate adolescent period is characterized by a series of changes in physiology, behavior, and social relationships. Orangutans have the slowest life history and the longest period of dependency of all primates. As members of a semisolitary species with high levels of sexual coercion, adolescent female orangutans face a unique combination of challenges when achieving independence from their mother. This study examined the mating behavior of adolescent female orangutans and compared it with that of adult females to assess whether mating behavior reflects distinct strategies at these different points in the life cycle. Data were collected in Gunung Palung National Park on the island of Borneo over 20 years. Mating events from adolescent (n = 19) and adult females (n = 26) were scored and compared. Adolescent female mating events had significantly higher mating scores (indicating more proceptivity) than those of adult females (β = 1.948, p = .001). Adolescent females also engaged in elaborate sociosexual interactions with different flanged males, behaviors that were never observed during mating events of adult females. These interactions involved characteristic behavior on the part of both the adolescent females and the flanged males. Given these findings and the documentation of similar accounts of adolescent female–flanged male mating from the island of Sumatra, we propose that adolescent female orangutans display distinctive behavioral repertoires throughout the genus Pongo which serves to overcome male ambivalence toward nulliparous females, establish familiarity, and evaluate coercive tendencies in flanged males. We suggest that these behavioral patterns are an integral part of female social development in a female philopatric, but highly dispersed species where consistent social support is absent after ranging independence is achieved.     

Expression of Myosin Heavy Chain Isoforms in the Supraspinatus Muscle of Different Primate Species: Implications for the Study of the Adaptation of Primate Shoulder Muscles to Different Locomotor Modes

The supraspinatus muscle is a key component of the soft tissues of the shoulder. In pronograde primates, its main function, in combination with the other rotator cuff muscles (subscapularis, infraspinatus, and teres minor), is to stabilize the glenohumeral joint, whereas in orthograde primates it functions together with the deltoid, to elevate the upper extremity in the scapular plane. To determine whether these functional differences are also reflected in the molecular biochemistry of the supraspinatus muscles involved in these different locomotor modes, we used real-time polymerase chain reaction (RT-PCR) to analyze the expression of the myosin heavy chain (MHC) isoforms in supraspinatus muscles from modern humans and 12 species of pronograde and orthograde primates. The MHC expression pattern in the supraspinatus muscle of pronograde primates was consistent with its function as a tonic and postural muscle, whereas the MHC expression pattern observed in the supraspinatus muscle of nonhuman orthograde primates was that of a muscle that emphasizes speed, strength, and less resistance to fatigue. These findings are consistent with the role of the supraspinatus in the posture and locomotor modes of these groups of nonhuman primates. The humans included in the study had an expression pattern similar to that of the nonhuman orthograde primates. In conclusion, molecular analysis of skeletal muscles via RT-PCR can contribute to a better understanding of the morphological and functional characteristics of the primate musculoskeletal system.     

Myxomatous neoplasms in the perineal region of baboons

Background In baboons, Papio sp. neoplasms tend to affect the hematopoietic system most commonly, with rare documentation of myxomatous neoplasms. In contrast, women can develop myxomatous masses within deep peripelvic tissues with some frequency during their reproductive years. Methods We have identified and examined, retrospectively, myxomatous perineal masses in twelve female baboons within one research facility and compared their histopathologic, immunohistochemical and electron microscopic features to their human variants. Results Our results indicate that these myxomatous neoplasms, in humans and non‐human primates, share common features. Conclusion Further research, particularly molecular genetic analysis, may be needed to identify the baboon as a true animal model for myxomatous perineal neoplasms.     

Ectocranial suture fusion in primates: pattern and phylogeny

Patterns of ectocranial suture fusion among Primates are subject to species‐specific variation. In this study, we used Guttman Scaling to compare modal progression of ectocranial suture fusion among Hominidae (Homo, Pan, Gorilla, and Pongo), Hylobates, and Cercopithecidae (Macaca and Papio) groups. Our hypothesis is that suture fusion patterns should reflect their evolutionary relationship. For the lateral‐anterior suture sites there appear to be three major patterns of fusion, one shared by Homo‐Pan‐Gorilla, anterior to posterior; one shared by Pongo and Hylobates, superior to inferior; and one shared by Cercopithecidae, posterior to anterior. For the vault suture pattern, the Hominidae groups reflect the known phylogeny. The data for Hylobates and Cercopithecidae groups is less clear. The vault suture site termination pattern of Papio is similar to that reported for Gorilla and Pongo. Thus, it may be that some suture sites are under larger genetic influence for patterns of fusion, while others are influenced by environmental/biomechanic influences. J. Morphol. 275:342–347, 2014. © 2013 Wiley Periodicals, Inc.     

Metatarsal robusticity in primates and a few other plantigrade mammals

By using a new technique for determining relative metatarsal robusticity, the distribution of the 1+5 pattern (in which M5 is the second most robust metatarsal after M1) and 15 pattern (in which M5 is the least robust of all metatarsals) was established in primates and a few other plantigrade mammals. The first pattern is associated with a terrestrial and the second with an arboreal substrate. Robusticity formulae are not connected with specific locomotor patterns, but a total robusticity quotient is associated with these patterns and substrate preference as well. Changes in substrate preference are accompanied by changes of total robusticity, an increased number of permutations and ultimately a change of the robusticity pattern. Intermetatarsal robusticity gradients are related to the direction and intensity of muscular activity. A combined analysis of all factors can reveal a great deal of the locomotor history of a taxon.Also ofThe Institute of Applied Biology, New York.     

Positional Behavior of Cercopithecus petaurista

I studied the positional behavior and habitat use of Cercopithecus petaurista, the lesser spot-nosed monkey, in the Ivory Coast's Taï Forest for 15 months. I compare these data with similar information collected on sympatric groups of Cercopithecus diana and C. campbelli in order to examine further the relationships between locomotion, posture, support use, stratal use, body size, diet, activity patterns and foraging behavior. Spot-nosed monkeys are predominantly quadrupedal primates that frequent the top layer of the understory during all maintenance activities. Locomotion is characteristically slow and cautious; travel takes place on branches and boughs while foraging occurs on twigs and branches. Postural behavior of Cercopithecus petaurista reflects their reliance on more ubiquitously distributed, less mobile food items. The relationship between body size, climbing, leaping and support use among Taï guenons is weak; interspecific differences are more likely functions of strata use and overall behavioral characteristics, e.g. crypticity. I also compare the locomotion and support use of Cercopithecus petaurista with that of C. ascanius from Uganda's Kibale Forest (Gebo and Chapman, 1995a) in order to assess the behavioral similarity of members of the same superspecies. Although overall support use is quite similar, the monkeys differ significantly in frequencies of quadrupedism, leaping and climbing. I present possible reasons for and implications of these differences.