Morphological affinities of the Australopithecus afarensis hand on the basis of manual proportions and relative thumb length

The hands of apes and humans differ considerably with regard to proportions between several bones. Of critical significance is the long thumb relative to other fingers, which is the basis for human-like pad-to-pad precision grip capability, and has been considered by some as evidence of tool-making. The nature and timing of the evolutionary transition from ape-like to human-like manual proportions, however, have remained unclear as a result of the lack of appropriate fossil material. In this article, the manual proportions of Australopithecus afarensis from locality AL 333/333w (Hadar, Ethiopia) are investigated by means of bivariate and multivariate morphometric analyses, in order to test the hypothesis that human-like proportions, including an enhanced thumb/hand relationship, originally evolved as an adaptation to stone tool-making. Although some evidence for human-like manual proportions had been previously proposed for this taxon, conclusive evidence was lacking. Our results indicate that A. afarensis possessed overall manual proportions, including an increased thumb/hand relationship that, contrary to previous reports, is fully human and would have permitted pad-to-pad human-like precision grip capability. We show that these human-like proportions in A. afarensis mainly result from hand shortening, as in modern humans, and that these conclusions are robust enough as to be non-dependent on whether the bones belong to a single individual or not. Since A. afarensis predates the appearance of stone tools in the archeological record, the above-mentioned conclusions permit a confident refutation of the null hypothesis that human-like manual proportions are an adaptation to stone tool-making, and thus alternative explanations must be therefore sought. One hypothesis would consider manipulative behaviors (including tool-use and/or non-lithic tool-making) in early hominines exceeding those reported among extant non-human primates. Alternatively, on the basis of the many adaptations to committed bipedalism in A. afarensis, we propose the hypothesis that once arboreal behaviors became adaptively insignificant and forelimb-dominated locomotor selection pressures were relaxed with the adoption of terrestrial bipedalism, human-like manual proportions could have merely evolved as a result of the complex manipulation selection pressures already present in extant non-human primates.Both hypotheses are not mutually exclusive, and even other factors such as pleiotropy cannot be currently discarded.     

Substrate alters forelimb to hindlimb peak force ratios in primates

It is often claimed that the walking gaits of primates are unusual because, unlike most other mammals, primates appear to have higher vertical peak ground reaction forces on their hindlimbs than on their forelimbs. Many researchers have argued that this pattern of ground reaction force distribution is part of a general adaptation to arboreal locomotion. This argument is frequently used to support models of primate locomotor evolution. Unfortunately, little is known about the force distribution patterns of primates walking on arboreal supports, nor do we completely understand the mechanisms that regulate weight distribution in primates. We collected vertical peak force data for seven species of primates walking quadrupedally on instrumented terrestrial and arboreal supports. Our results show that, when walking on arboreal vs. terrestrial substrates, primates generally have lower vertical peak forces on both limbs but the difference is most extreme for the forelimb. We found that force reduction occurs primarily by decreasing forelimb and, to a lesser extent, hindlimb stiffness. As a result, on arboreal supports, primates experience significantly greater functional differentiation of the forelimb and hindlimb than on the ground. These data support long-standing theories that arboreal locomotion was a critical factor in the differentiation of the forelimbs and hindlimbs in primates. This change in functional role of the forelimb may have played a critical role in the origin of primates and facilitated the evolution of more specialized locomotor behaviors.     

Intrinsic hand proportions of euarchontans and other mammals: implications for the locomotor behavior of plesiadapiforms

Arboreal primates have distinctive intrinsic hand proportions compared with many other mammals. Within Euarchonta, platyrrhines and strepsirrhines have longer manual proximal phalanges relative to metacarpal length than colugos and terrestrial tree shrews. This trait is part of a complex of features allowing primates to grasp small-diameter arboreal substrates. In addition to many living and Eocene primates, relative elongation of proximal manual phalanges is also present in most plesiadapiforms. In order to evaluate the functional and evolutionary implications of manual similarities between crown primates and plesiadapiforms, we measured the lengths of the metacarpal, proximal phalanx, and intermediate phalanx of manual ray III for 132 extant mammal species (n=702 individuals). These data were compared with measurements of hands in six plesiadapiform species using ternary diagrams and phalangeal indices. Our analyses reveal that many arboreal mammals (including some tree shrews, rodents, marsupials, and carnivorans) have manual ray III proportions similar to those of various arboreal primates. By contrast, terrestrial tree shrews have hand proportions most similar to those of other terrestrial mammals, and colugos are highly derived in having relatively long intermediate phalanges. Phalangeal indices of arboreal species are significantly greater than those of the terrestrial species in our sample, reflecting the utility of having relatively long digits in an arboreal context. Although mammals known to be capable of prehensile grips demonstrate long digits relative to palm length, this feature is not uniquely associated with manual prehension and should be interpreted with caution in fossil taxa. Among plesiadapiforms, Carpolestes, Nannodectes, Ignacius, and Dryomomys have manual ray III proportions that are unlike those of most terrestrial species and most similar to those of various arboreal species of primates, tree shrews, and rodents. Within Euarchonta, Ignacius and Carpolestes have intrinsic hand proportions most comparable to those of living arboreal primates, while Nannodectes is very similar to the arboreal tree shrew Tupaia minor. These results provide additional evidence that plesiadapiforms were arboreal and support the hypothesis that Euarchonta originated in an arboreal milieu.     

A comparison of primate, carnivoran and rodent limb bone cross-sectional properties: are primates really unique?

The cross-sectional properties of mammalian limb bones provide an important source of information about their loading history and locomotor adaptations. It has been suggested, for instance, that the cross-sectional strength of primate limb bones differs from that of other mammals as a consequence of living in a complex arboreal environment (Kimura, 1991, 1995). In order to test this hypothesis more rigorously, we have investigated cross-sectional properties in samples of humeri and femora of 71 primate species, 30 carnivorans and 59 rodents. Primates differ from carnivorans and rodents in having limb bones with greater cross-sectional strength than mammals of similar mass. This might imply that primates have stronger bones than carnivorans and rodents. However, primates also have longer proximal limb bones than other mammals. When cross-sectional dimensions are regressed against bone length, primates appear to have more gracile bones than other mammals. These two seemingly contradictory findings can be reconciled by recognizing that most limb bones experience bending as a predominant loading regime. After regressing cross-sectional strength against the product of body mass and bone length, a product which should be proportional to the bending moments applied to the limb, primates are found to overlap considerably with carnivorans and rodents. Consequently, primate humeri and femora are similar to those of nonprimates in their resistance to bending. Comparisons between arboreal and terrestrial species within the orders show that the bones of arboreal carnivorans have greater cross-sectional properties than those of terrestrial carnivorans, thus supporting Kimura's general notion. However, no differences were found between arboreal and terrestrial rodents. Among primates, the only significant difference was in humeral bending rigidity, which is higher in the terrestrial species. In summary, arboreal and terrestrial species do not show consistent differences in long bone reinforcement, and Kimura's conclusions must be modified to take into account the interaction of bone length and cross-sectional geometry.     

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.     

Mantled Howler (<Emphasis Type="Italic">Alouatta palliata</Emphasis>) Arboreal Pathway Networks: Relative Impacts of Resource Availability and Forest Structure

Numerous studies have concluded that primates move about their environments in a nonrandom manner, frequently traveling between consecutive foraging sites along relatively straight-line paths. However, primates do not always take the most direct path between resources, and a number of species have been observed to travel repeatedly along a network of the same arboreal pathways. In this study, I used spatially explicit techniques to examine quantitatively what mantled howler monkey groups on Barro Colorado Island, Panama, accomplish by selecting nonlinear paths between resources and by repeatedly using the same paths within an arboreal network. Results show that chosen arboreal paths between sites where foraging occurred have higher levels of resource availability and canopy connectivity than comparable straight-line paths between the same sites. When comparing the relative importance of these factors, autologistic models of pathway choice indicate that though canopy connectivity is related to the location of repeatedly used arboreal pathway networks, the most statistically significant predictor is resource availability (both on a path and within a visual detection distance of a path). These results provide support for the hypothesis that repeated use of arboreal pathway networks aids in resource monitoring and acquisition. In addition, statistical models developed from 1 primary focal group’s travel patterns had high predictive value when employed to generate likely locations for arboreal pathways in the home ranges of 3 neighboring groups. This finding has important implications for studies of primate habitat use and seed dispersal, as it suggests that different groups consistently use similar characteristics when deciding on travel paths.     

Comparative histomorphology of intrinsic vibrissa musculature among primates: implications for the evolution of sensory ecology and “face touch”

Macrovibrissae are specialized tactile sensory hairs present in most mammalian orders, used in maxillary mechanoreception or “face touch.” Some mammals have highly organized vibrissae and are able to “whisk” them. Movement of vibrissae is influenced by intrinsic vibrissa musculature, striated muscle bands that attach directly to the vibrissa capsule. It is unclear if primates have organized vibrissae or intrinsic vibrissa musculature and it is uncertain if they can move their vibrissae. The present study used histomorphological techniques to compare vibrissae among 19 primates and seven non‐primate mammalian taxa. Upper lips of these mammals were sectioned and processed for histochemical analysis. While controlling for phylogenetic effects the following hypotheses were tested: 1) mammals with well‐organized vibrissae possess intrinsic vibrissa musculature and 2) intrinsic vibrissa musculature is best developed in nocturnal, arboreal taxa. Our qualitative analyses show that only arboreal, nocturnal prosimians possess intrinsic musculature. Not all taxa that possessed organized vibrissae had intrinsic vibrissa musculature. Phylogenetic comparative analyses revealed a 70% probability that stem mammals, primates, and haplorhines possessed intrinsic vibrissa musculature and well‐organized vibrissae. These two traits most likely coevolved according to a discrete phylogenetic analysis. These results indicate that nocturnal, arboreal primates have the potential to more actively use their vibrissae in spatial recognition and navigation tasks than diurnal, more terrestrial species, but there is a clear phylogenetic signal involved in the evolution of primate vibrissae and “face touch.” Am J Phys Anthropol, 2013. © 2012 Wiley Periodicals, Inc.     

Predation on primates: Ecological patterns and evolutionary consequences

It has long been thought that predation has had important ecological and evolutionary effects on primates as prey. Predation has been theorized to have been a major selective force in the evolution of hominids.¹ In modern primates, behaviors such as active defense, concealment, vigilance, flight, and alarm calls have been attributed to the selective pressures of predation, as has group living itself. It is clear that primates, like other animals, have evolved ways to minimize their risk of predation. However, the extent to which they have been able to do so, given other constraints of living such as their own need to acquire food, has not yet been resolved. Perhaps most hotly debated is whether predation has been the primary selective force favoring the evolution of group living in primates. Part of the difficulty in resolving the debate lies in a paucity of direct evidence of predation. This is regrettable yet understandable since primatologists, by definition, focus on the study of primates, not predators of primates (unless these are also primates). Systematic direct evidence of the effects of predation can best be obtained by studying predators that are as habituated to observers as are their primate prey. Until this is done, we must continue to rely on opportunistic accounts of predation and predation attempts, and on systematically obtained indirect evidence. Such data reveal several interesting patterns: (1) although smaller primates may have greater predation rates than larger primates, even the largest primates are not invulnerable to predation; (2) the use by primates of unfamiliar areas can result in higher predation rates, which might be one pressure favoring philopatry, or site fidelity; (3) arboreal primates are at greater risk of predation when they are more exposed (at forest edges and tops of canopies) than in more concealed locations; (4) predation by mammalian carnivores may often be episodic; and (5) terrestrial primates may not experience greater predation than arboreal primates.     

Arboreal tropical forest vertebrates: current knowledge and research trends

We review the ecology and specialized methods required for studying arboreal mammals, birds, reptiles and amphibians, and use faunal checklists from 12 tropical wet forest sites and an analysis of all articles published during the past ten years in 14 major journals to assess current knowledge and general research trends for these groups. The percentage of arboreal vertebrates was remarkably similar at the different sites (76.2 ± 3.9%). Birds were the most arboreal group and amphibians and reptiles the least. The review of journals showed that primates were overwhelmingly the most studied group (336 papers), followed by bats (105), passeriform birds (73) and rodents (55). Judging by their portion of the arboreal vertebrate community and the number of papers surveyed, birds and amphibians and reptiles are vastly understudied compared to mammals, but this is largely due to the great number of primate studies. The number of publications on arboreal vertebrates has remained relatively stable over the last 10 years for all taxa except primates, which have seen a growth in publications. Canopy vertebrates from Brazil had by far the most publications (120), followed by Madagascar (61), Costa Rica (55) and Indonesia (42). We conclude by highlighting the priorities we see for future studies on tropical canopy vertebrates.     

Locomotor energetics in primates: gait mechanics and their relationship to the energetics of vertical and horizontal locomotion

All primates regularly move within three-dimensional arboreal environments and must often climb, but little is known about the energetic costs of this critical activity. Limited previous work on the energetics of incline locomotion suggests that there may be differential selective pressures for large compared to small primates in choosing to exploit a complex arboreal environment. Necessary metabolic and gait data have never been collected to examine this possibility and biomechanical mechanisms that might explain size-based differences in the cost of arboreal movement. Energetics and kinematics were collected for five species of primate during climbing and horizontal locomotion. Subjects moved on a treadmill with a narrow vertical substrate and one with a narrow horizontal substrate at their maximum sustainable speed for 10–20 min while oxygen consumption was monitored. Data during climbing were compared to those during horizontal locomotion and across size. Results show that climbing energetic costs were similar to horizontal costs for small primates (<0.5 kg) but were nearly double for larger species. Spatio-temporal gait characteristics suggest that the relationship between the cost of locomotion and the rate of force production changes between the two locomotor modes. Thus, the main determinants of climbing costs are fundamentally different from those during horizontal locomotion. These new results combining spatiotemporal and energetic data confirm and expand on our previous argument (Hanna et al.: Science 320 (2008) 898) that similar costs of horizontal and vertical locomotion in small primates facilitated the successful occupation of a fine-branch arboreal milieu by the earliest primates.     

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.     

Mediolateral reaction forces and forelimb anatomy in quadrupedal primates: implications for interpreting locomotor behavior in fossil primates

The forelimb joints of terrestrial primate quadrupeds appear better able to resist mediolateral (ML) shear forces than those of arboreal quadrupedal monkeys. These differences in forelimb morphology have been used extensively to infer locomotor behavior in extinct primate quadrupeds. However, the nature of ML substrate reaction forces (SRF) during arboreal and terrestrial quadrupedalism in primates is not known. This study documents ML-SRF magnitude and orientation and forelimb joint angles in six quadrupedal anthropoid species walking across a force platform attached to terrestrial (wooden runway) and arboreal supports (raised horizontal poles). On the ground all subjects applied a lateral force in more than 50% of the steps collected. On horizontal poles, in contrast, all subjects applied a medially directed force to the substrate in more than 75% of the steps collected. In addition, all subjects on arboreal supports combined a lower magnitude peak ML-SRF with a change in the timing of the ML-SRF peak force. As a result, during quadrupedalism on the poles the overall SRF resultant was relatively lower than it was on the runway. Most subjects in this study adduct their humerus while on the poles. The kinetic and kinematic variables combine to minimize the tendency to collapse or translate forelimbs joints in an ML plane in primarily arboreal quadrupedal primates compared to primarily terrestrial quadrupedal ones. These data allow for a more complete understanding of the anatomy of the forelimb in terrestrial vs. arboreal quadrupedal primates. A better understanding of the mechanical basis of morphological differences allows greater confidence in inferences concerning the locomotion of extinct primate quadrupeds.     

Kinematic adjustments to arboreal locomotion in Japanese macaques (Macaca fuscata)

Primates - Although biomechanical adaptations to arboreal locomotion have been well investigated in primates and other mammals in laboratory settings, the results are not consistent, and more...     

The Fayum primate forest: Did it exist?

The primates have the reputation of being essentially arboreal, forest-adapted animals. Yet there are many genera and species that inhabit an extremely wide array of non-forest habitats. Nevertheless, palaeoprimatologists often tend to depict fossil primate habitats as being more arboreal and more forest-like than is justified by the facts. It is worthwhile, therefore, to reconsider some current interpretations. In this paper, evidence of the Fayum Oligocene primate deposits are reviewed and discussed. The following conclusions emerge:(1) The large number of primate species indicates that the Fayum ecosystem was an optimum or near-optimum habitat for primates. (2) The lithological characteristics point to a sahélien type of climate. (3) The calcified and silicified root systems, having diameters up to 4 cm, suggest a sahélien type of shrub, bushland and/or small-tree vegetation. (4) The large fossilized logs cannot have grown on the spot and apparently represent driftwood from a more humid climatic belt in the south, as is indicated by damage resulting from fluvial transportation and by palaeobotanical data. (5) There may have been some minor patches or strips of medium-height forests and/or wood-lands in the Fayum delta, but there is no evidence of these.Thus the tall forest in which the earliest known African primates are currently supposed to have lived probably never existed. Grounds for this conclusion were presented by Unger 121 years ago, by Beadnell 75 years ago and by Kräusel 41 years ago, but sank into oblivion. The classic image of the primates as arboreal specialists seems to have interfered with seeing the facts. However, more extensive verification of the evidence by means of palaeobotanical research is still required. The fossil material to do so is readily available.     

Use of forest canopy by European red squirrelsSciurus vulgaris in Northern Greece: claws and the small branch niche

Moving and standing in trees impose multiple problems to arboreal mammals. Among them, the major ones are the negotiation of slender terminal branches and of large vertical supports. Both microhabitats are important as they have been linked alternatively to the evolutionary loss of claws in early primates. Therefore, rates of use of these different supports by claw-bearing arboreal mammals may offer insights to their actual significance in the adaptive evolution of early primates. In this context, canopy, tree crown, branch size, inclination, and texture use were recorded on four adult free ranging European red squirrelsSciurus vulgaris Linnaeus, 1758 in a mixed coniferous forest in northern Greece.S. vulgaris was mainly arboreal, exploiting the terminal branch zone, using frequently oblique and intermediately textured supports<5 cm and moderately large vertical branches. Furthermore, comparative data from other sciurid species and clawed primates showed positive correlations of small and horizontal support use, and negative ones of vertical support use to body mass. These findings show that keeled functional claws do not impede habitual use of slender branches and may not facilitate efficient climbing on large vertical trunks. These observations partly question the association between habitual use of the small branch niche and primate adaptations and lend support to alternative hypotheses, underscoring the importance of inquiring for more complex mechanisms that lead to the evolution of the unique set of primate morphological adaptations.     

Plantigrady and foot adaptation in African apes: implications for hominid origins.

In living primates, except the great apes and humans, the foot is placed in a heel-elevated or semi-plantigrade position when these animals move upon arboreal or terrestrial substrates. Heel placement and bone positions in the non-great ape primate foot are designed to increase mobility and flexibility in the arboreal environment. Orangutans have further enhanced foot mobility by adapting their feet for suspension and thus similarly utilize foot positions where the heel does not touch the substrate. Chimpanzees and gorillas represent an alternative pattern (plantigrady), in which the heel contacts the surface of the support at the end of swing phase, especially during terrestrial locomotion. Thus, chimpanzees and gorillas possess feet adapted for both arboreal and terrestrial substrates. African apes also share several osteological features related to plantigrady and terrestrial locomotion with early hominids. From this analysis, it is apparent that hominid locomotor evolution passed through a quadrupedal terrestrial phase.     

Frequent predation on primates by crowned eagles (Stephanoaetus coronatus) in Mahale Mountains National Park,Tanzania

Primates - The significance of raptor predation has been repeatedly emphasized in studies on arboreal primates; however, there are few studies on the predation of primates by raptors in...     

Scapular position in primates

Scapular position affects shoulder mobility, which plays an important role in the upper limb adaptations in primates. However, currently available data on scapular position are unsatisfactory because of the failure to simultaneously consider the relative dimensions of all the three skeletal elements of the shoulder girdle, i.e. the clavicle, the scapula and the thorax. In the present study, the clavicular length and the scapular spine length were measured on preserved cadavers, and the dorsoventral thoracic diameter was measured on scaled radiographs of a wide range of primates, permitting a quantitative comparison of scapular position among primates. It was found that arboreal monkeys have a more dorsally situated scapula than terrestrial ones, but the same difference was not found between terrestrial and arboreal prosimians. Hominoids were found to have the most dorsally situated scapula. Contrary to the slow climbing theory of hominoid evolution, which tries to explain most postcranial specializations of hominoids as adaptations for slow climbing, the scapulae of slow-climbing lorines and Alouatta are much less dorsal than those of the hominoids.     

Leaf chemistry and the biomass of folivorous primates in tropical forests

Summary Recent results have suggested that the biomass of folivorous arboreal primates per unit area in Africa and Asia is positively correlated with the average quality of leaves, expressed as the ratio of protein to fiber concentrations in a given forest. This hypothesis has been tested in different forests of Madagascar. Leaf selection of all folivorous femus species was studied in relation to leaf chemistry. Except for two populations ofLepilemur subspecies all other folivorous lemur species (including two other subspecies ofLepilemur) select leaves with high concentrations of easily extractable protein or low concentrations of fiber, or both. This confirms the prominent role of these two components in leaf selection by folivorous lemurs. The average quality of mature leaves in a given forest, expressed as the ratio of protein to fiber concentrations, is positively correlated with the biomass of folivorous lemurs. This confirms the hypothesis tested and suggests rather uniform selection processes for arboreal folivorous primates across the world.