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.     

Primate limb bones and locomotor types in arboreal or terrestrial environments

Postcranial limb bones were compared among primates of different locomotor types. Seventy-one primate species, in which all families of primates were included, were grouped into nine locomotor types. Osteometrical data on long bones and data on the cross-sectional geometry of the humerus and the femur were studied by means of allometric analysis and principal component analysis. Relatively robust forelimb bones were observed in the primate group which adopted the relatively terrestrial locomotor type compared with the group that adopted the arboreal locomotor type. The difference resembled the previously reported comparison between terrestrial and arboreal groups among all quadrupedal mammals. The degree of arboreality in daily life is connected with the degree of hindlimb dominance, or the ratio of force applied to the fore- and hindlimb in positional behaviour and also with the shape, size and robusticity of limb bones.     

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.     

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.     

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.     

Differential habitat use byCebus apella andSaimiri sciureus in central surinam

Cebus apella, the black-capped or tufted capuchin, andSaimiri sciureus, the squirrel monkey, are frequently found in mixed species feeding and foraging groups throughout tropical South America and have been reported previously to show marked differences in techniques of insect foraging. Individuals of these taxa observed in central Surinam show numerous additional species-specific differences in other aspects of habitat utilization including gross dietary preferences, utilization of forest strata, locomotor behavior and arboreal support preferences.Cebus apella is more frugivorous, frequents the middle and lower levels of the main canopy, is predominantly quadrupedal and moves on medium-sized arboreal supports. By contrast, the smallerSaimiri sciureus is more insectivorous, frequents the lower strata of the forest, is more saltatory and moves on the smallest arboreal supports. Many of these differences in habitat use are interrelated and accord with patterns of habitat use seen in other primate taxa. The differences betweenCebus apella andSaimiri sciureus also accord with the types of behavioral differences frequently associated with differences in body size.     

Brain size and ecology in small mammals

Relative brain size (measured as gross brain size after body size effects are removed) differs systematically between families of rodents, insectivores and lagomorphs. The Sciuridae have the largest relative brain size, the Soricidae and Bathyergidae the smallest.
These results are discussed and compared with previous analyses of relative brain sizes among primates and bats. These differences complicate comparisons between relative brain size across phylogenetically diverse species and attempts to relate differences in relative brain size to ecological variables. To overcome these problems, best fit relationships were estimated for each family , and values for each genus were expressed as deviations from the lines of best fit. We refer to these values as Comparative Brain Size (CBS).
Differences in CBS are related to differences in habitat type (forest-dwelling genera have larger CBS' than grassland forms), in diet (folivores have smaller CBS' than generalists or insectivores, frugivores and granivores), in zonation (arboreal genera have larger CBS' than terrestrial ones) and in activity timing (nocturnal genera have larger CBS' than dirurnal ones). However, these ecological categories are interrelated and, when the effects of other ecological differences are taken into account using analyses of variance, only the differences associated with diet, and possibly habitat remain.     

Osteological postcranial traits in hylid anurans indicate a morphological continuum between swimming and jumping locomotor modes

Anurans exhibit a particularly wide range of locomotor modes that result in wide variations in their skeletal structure. This article investigates the possible correlation between morphological aspects of the hylid postcranial skeleton and their different locomotor modes and habitat use. To do so, we analyzed 18 morphometric postcranial variables in 19 different anuran species representative of a variety of locomotor modes (jumper, hopper, walker, and swimmer) and habitat uses (arboreal, bush, terrestrial, and aquatic). Our results show that the evolution of the postcranial hylid skeleton cannot be explained by one single model, as for example, the girdles suggest modular evolution while the vertebral column suggests other evolutionary modules. In conjunction with data from several other studies, we were able to show a relationship between hylid morphology and habitat use; offering further evidence that the jumper/swimmer and walker/hopper locomotor modes exhibit quite similar morphological architecture. This allowed us to infer that new locomotor modalities are, in fact, generated along a morphological continuum. J. Morphol. 278:403–417, 2017. © 2017 Wiley Periodicals, Inc.     

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.     

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.     

A reappraisal of the locomotion and habitat preference of Theropithecus oswaldi

The one modern member of the genus Theropithecus, T. gelada (Primates, Cercopithecidae), inhabits grassland and is highly terrestrial. It is often supposed that Theropithecus oswaldi, one of the most common primates of the Plio-Pleistocene of East and southern Africa, was also a highly terrestrial open habitat species. Ecomorphic analysis was used to assess the locomotor strategy and habitat preference of T. oswaldi, and it was found that this species was unlikely to have had a locomotor strategy and habitat preference identical to that of T. gelada, with T. oswaldi possibly using arboreal substrates in a manner similar to some modern baboon groups. Thus, it appears that there has been considerable ecological diversity in the genus Theropithecus over the course of its evolution, mirroring the diversity evident in the hominin fossil record.     

Allometric scaling and locomotor function in the primate pelvis

Identification of positional behavior adaptation in the pelvis of primates is complicated by possible confounding effects of body size and phylogeny. Previous work on primate pelvic allometry has focused primarily on sexual dimorphism and its relationship to obstetric constraints in species with large fetal size relative to maternal size. This study investigates patterns of pelvic scaling with a specific aim to understand how pelvic scaling relates to locomotor function. Patterns of scaling of nine pelvic dimensions were examined in a broad comparative sample of 40 species of primates, covering both haplorhines and strepsirrhines, while accounting for phylogenetic nonindependence. Phylogenetic reduced major axis regressions on pelvic scaling patterns suggest that primate-wide patterns are reflected in haplorhine- and strepsirrhine-specific analyses. Many measures scale isometrically with pelvis size, but notably, features of the ilium tend to scale allometrically. As predicted, ilium width and lower ilium cross-sectional area scale with positive allometry, while lower iliac height scales with negative allometry. Further regression analyses by locomotor group suggest that these ilium measures, as well as pubic symphysis and ischium lengths, differ in their scaling patterns according to locomotor mode. These results suggest that scaling differences within primates, when present, are related to functional differences in locomotor behavior and mechanics. This study supports recent work that identifies adaptations to locomotor loading in the ilium and highlights the need for a better understanding of the relationship between pelvic structural mechanics and the mechanical requirements of primate locomotion. Am J Phys Anthropol 156:511–530, 2015. © 2015 Wiley Periodicals, Inc.     

The correspondence between proximal phalanx morphology and locomotion: implications for inferring the locomotor behavior of fossil catarrhines

Phalanges are considered to be highly informative in the reconstruction of extinct primate locomotor behavior since these skeletal elements directly interact with the substrate during locomotion. Variation in shaft curvature and relative phalangeal length has been linked to differences in the degree of suspension and overall arboreal locomotor activities. Building on previous work, this study investigated these two skeletal characters in a comparative context to analyze function, while taking evolutionary relationships into account. This study examined the correspondence between proportions of suspension and overall substrate usage observed in 17 extant taxa and included angle of curvature and relative phalangeal length. Predictive models based on these traits are reported. Published proportions of different locomotor behaviors were regressed against each phalangeal measurement and a size proxy. The relationship between each behavior and skeletal trait was investigated using ordinary least-squares, phylogenetic generalized least-squares (pGLS), and two pGLS transformation methods to determine the model of best-fit. Phalangeal curvature and relative length had significant positive relationships with both suspension and overall arboreal locomotion. Cross-validation analyses demonstrated that relative length and curvature provide accurate predictions of relative suspensory behavior and substrate usage in a range of extant species when used together in predictive models. These regression equations provide a refined method to assess the amount of suspensory and overall arboreal locomotion characterizing species in the catarrhine fossil record.     

Morphometry and allometry of the primate humerus

The primate distal humerus has been used both in phylogenetic reconstruction and in assessing locomotor and postural adaptations. This study uses an allometric approach to predict locomotor patterns of extant primates regardless of phylogenetic position. By showing the relationship between form and function in living primate taxa it will be possible to use this data set to predict locomotor behavior of extinct primates. Several linear measurements were taken from the distal humerus of 71 extant primate species (anthropoids and prosimians). Allometric regressions of each measurement were performed with mandibular M₂ area as a surrogate for body size. These measurements were used to determine if significant differences in distal humerus morphology exist among locomotor groups. The results were then used to test several hypotheses about the relationship between humeral form and function. For example, the hypothesis that suspensory primates have a large medial epicondyle is confirmed; the hypothesis that terrestrial quadrupeds have a deep olecranon fossa could not be confirmed with quantitative data. In addition to this hypothesis testing, the residuals from the allometric regressions of the humeral measurements were used in a discriminant functions analysis to estimate locomotor behavior from distal humerus morphology. The discriminant functions analysis correctly reclassified 64/71 (90%) species.     

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.     

Primate longevity: Its place in the mammalian scheme

Data on captive longevity in 587 mammalian species were analyzed in order to evaluate primate longevity in the context of general mammalian life history patterns. Contrary to some recurrent claims in the literature, we found that 1) primates are not the longest-lived mammalian order, either by absolute longevity, longevity corrected for body size, or metabolic expenditure per lifetime; 2) although relative brain size is highly correlated with longevity in primates, this is an aberrant trend for mammals in general, and other body organs account for an even greater amount of variation in longevity; and 3) there has been no progressive evolution of increased longevity among the primate superfamilies. The exceptional magnitude of primate longevity may, in keeping with evolutionary senescence theory, be due to an evolutionary history of low vulnerability to environmentally imposed death due to their body size, arboreal habit, and propensity to live in social groups. © 1992 Wiley-Liss, Inc.     

Sex differences in adult chimpanzee positional behavior: The influence of body size on locomotion and posture

Focal animal instantaneous sampling of adult male and female chimpanzee positional behavior was conducted during a 7-month study in the Tai Forest, Ivory Coast, in order to determine whether there are sex differences in the locomotion, posture, substrate use, and height preference of sexually dimorphic adult chimpanzees, and if so, whether these differences support predictions based on body size differences. Results indicate that as predicted, adult male and female chimpanzees differ in their arboreal locomotor behavior, with the larger males using less quadrupedalism and more climbing, scrambling, and aided bipedalism than females during feeding locomotion. There is a sex difference in height preference as well, with female chimpanzees consistently using more arboreal behavior than males, primarily during resting. Although it has been previously demonstrated that separate primate species of differing body size differ in locomotor and postural activities (Fleagle and Mittermeier, 1980; Crompton, 1984), this study clearly demonstrates that body size differences within a species can also be correlated with differences in locomotor behavior. These findings may influence how we interpret sex differences in body size of extinct species. © 1993 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.     

Ecological distinctions between sympatric species of Saguinus and Sciurus

Tamarins are small New World monkeys that have been described as "squirrellike." Squirrels, along with bats and birds, are the taxa most likely to utilize resources similar to those used by primates in the tropical forest canopy. In this paper we compare differences in ecology, diet, locomotion, and habitat utilization between sympatric populations of tamarins (Saguinus oedipus) and tree squirrels (Sciurus granatensis) in Panama. Data presented indicate that although there is some degree of resource overlap, patterns of habitat utilization differ significantly. Rather than being "squirrellike," the Panamanian tamarin exhibits a pattern of locomotor and feeding behavior consistent with that found in other arboreal primates.     

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

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