Adaptations for bipedal walking: Musculoskeletal structure and three-dimensional joint mechanics of humans and bipedal chimpanzees (Pan troglodytes).

Humans are unique among apes and other primates in the musculoskeletal design of their lower back, pelvis, and lower limbs. Here, we describe the three-dimensional ground reaction forces and lower/hindlimb joint mechanics of human and bipedal chimpanzees walking over a full stride and test whether: 1) the estimated limb joint work and power during the stance phase, especially the single-support period, is lower in humans than bipedal chimpanzees, 2) the limb joint work and power required for limb swing is lower in humans than in bipedal chimpanzees, and 3) the estimated total mechanical power during walking, accounting for the storage of passive elastic strain energy in humans, is lower in humans than in bipedal chimpanzees. Humans and bipedal chimpanzees were compared at matched dimensionless and dimensional velocities. Our results indicate that humans walk with significantly less work and power output in the first double-support period and the single-support period of stance, but markedly exceed chimpanzees in the second double-support period (i.e., push-off). Humans generate less work and power in limb swing, although the species difference in limb swing power was not statistically significant. We estimated that total mechanical positive 'muscle fiber' work and power were 46.9% and 35.8% lower, respectively, in humans than in bipedal chimpanzees at matched dimensionless speeds. This is due in part to mechanisms for the storage and release of elastic energy at the ankle and hip in humans. Furthermore, these results indicate distinct 'heel strike' and 'lateral balance' mechanics in humans and bipedal chimpanzees and suggest a greater dissipation of mechanical energy through soft tissue deformations in humans. Together, our results document important differences between human and bipedal chimpanzee walking mechanics over a full stride, permitting a more comprehensive understanding of the mechanics and energetics of chimpanzee bipedalism and the evolution of hominin walking.

Distinct functional roles of primate grasping hands and feet during arboreal quadrupedal locomotion.

It has long been thought that quadrupedal primates successfully occupy arboreal environments, in part, by relying on their grasping feet to control balance and propulsion, which frees their hands to test unstable branches and forage. If this interlimb decoupling of function is real, there should be discernible differences in forelimb versus hind limb musculoskeletal control, specifically in how manual and pedal digital flexor muscles are recruited to grasp during arboreal locomotion. New electromyography data from extrinsic flexor muscles in red ruffed lemurs (Varecia rubra) walking on a simulated arboreal substrate reveal that toe flexors are activated at relatively higher levels and for longer durations than finger flexors during stance phase. This demonstrates that the extremities of primates indeed have different functional roles during arboreal locomotion, with the feet emphasizing maintenance of secure grips. When this dichotomous muscle activity pattern between the forelimbs and hind limbs is coupled with other features of primate quadrupedal locomotion, including greater hind limb weight support and the use of diagonal-sequence footfall patterns, a complex suite of biomechanical characters emerges in primates that allow for the co-option of hands toward non-locomotor roles. Early selection for limb functional differentiation in primates probably aided the evolution of fine manipulation capabilities in the hands of bipedal humans.

Three-dimensional kinematics of the pelvis and hind limbs in chimpanzee (Pan troglodytes) and human bipedal walking.

The common chimpanzee (Pan troglodytes) is a facultative biped and our closest living relative. As such, the musculoskeletal anatomies of their pelvis and hind limbs have long provided a comparative context for studies of human and fossil hominin locomotion. Yet, how the chimpanzee pelvis and hind limb actually move during bipedal walking is still not well defined. Here, we describe the three-dimensional (3-D) kinematics of the pelvis, hip, knee and ankle during bipedal walking and compare those values to humans walking at the same dimensionless and dimensional velocities. The stride-to-stride and intraspecific variations in 3-D kinematics were calculated using the adjusted coefficient of multiple correlation. Our results indicate that humans walk with a more stable pelvis than chimpanzees, especially in tilt and rotation. Both species exhibit similar magnitudes of pelvis list, but with segment motion that is opposite in phasing. In the hind limb, chimpanzees walk with a more flexed and abducted limb posture, and substantially exceed humans in the magnitude of hip rotation during a stride. The average stride-to-stride variation in joint and segment motion was greater in chimpanzees than humans, while the intraspecific variation was similar on average. These results demonstrate substantial differences between human and chimpanzee bipedal walking, in both the sagittal and non-sagittal planes. These new 3-D kinematic data are fundamental to a comprehensive understanding of the mechanics, energetics and control of chimpanzee bipedalism.

Electromyography of crural and pedal muscles in tufted capuchin monkeys (Sapajus apella): Implications for hallucal grasping behavior and first metatarsal morphology in euprimates.

A hypertrophied peroneal process of the hallucal metatarsal, as seen in prosimians, has been linked to a powerful hallucal grasp via the contraction of the peroneus longus (PL) muscle causing adduction of the big toe. Electromyography (EMG) studies of lemurs and lorises, however, have concluded that PL is not substantially recruited during small branch locomotion when powerful hallucal grasping is needed most, and have suggested that there is no link between PL activity and peroneal process size. If this is correct, then we should also observe no change in PL activity when strong hallucal grasping is required in anthropoids because they have a relatively smaller peroneal process for PL to act on. This study addresses this hypothesis by evaluating EMG of crural and pedal muscles in capuchins (Sapajus apella) walking on substrates of different diameters. During locomotion on the narrow substrate (3.1 cm) that should elicit a strong hallucal grasp, we observed an intense increased recruitment of adductor hallucis, but only sustained, rather than markedly increased, PL activity. This indicates that PL is not involved in powerful hallucal grasping in capuchins, and confirms similar findings previously documented in prosimians. We continue to reject the hypothesis that a large peroneal process is an adaptation for powerful grasping and further argue that its morphology may not be related to PL's ability to adduct the hallux at all. In addition, the morphology of the peroneal process should not be used to assess hallucal grasping performance in fossils.

A three-dimensional musculoskeletal model of the chimpanzee (Pan troglodytes) pelvis and hind limb.

Musculoskeletal models have become important tools for studying a range of muscle-driven movements. However, most work has been in modern humans, with few applications in other species. Chimpanzees are facultative bipeds and our closest living relatives, and have provided numerous important insights into our own evolution. A chimpanzee musculoskeletal model would allow integration across a wide range of laboratory-based experimental data, providing new insights into the determinants of their locomotor performance capabilities, as well as the origins and evolution of human bipedalism. Here, we described a detailed three-dimensional (3D) musculoskeletal model of the chimpanzee pelvis and hind limb. The model includes geometric representations of bones and joints, as well as 35 muscle-tendon units that were represented using 44 Hill-type muscle models. Muscle architecture data, such as muscle masses, fascicle lengths and pennation angles, were drawn from literature sources. The model permits calculation of 3D muscle moment arms, muscle-tendon lengths and isometric muscle forces over a wide range of joint positions. Muscle-tendon moment arms predicted by the model were generally in good agreement with tendon-excursion estimates from cadaveric specimens. Sensitivity analyses provided information on the parameters that model predictions are most and least sensitive to, which offers important context for interpreting future results obtained with the model. Comparisons with a similar human musculoskeletal model indicate that chimpanzees are better suited for force production over a larger range of joint positions than humans. This study represents an important step in understanding the integrated function of the neuromusculoskeletal systems in chimpanzee locomotion.

Rotator cuff muscle function and its relation to scapular morphology in apes.

It is widely held that many differences among primate species in scapular morphology can be functionally related to differing demands on the shoulder associated with particular locomotor habits. This perspective is largely based on broad scale studies, while more narrow comparisons of scapular form often fail to follow predictions based on inferred differences in shoulder function. For example, the ratio of supraspinous fossa/infraspinous fossa size in apes is commonly viewed as an indicator of the importance of overhead use of the forelimb, yet paradoxically, the African apes, the most terrestrial of the great apes, have higher scapular fossa ratios than the more suspensory orangutan. The recent discovery of several nearly complete early hominin scapular specimens, and their apparent morphological affinities to scapulae of orangutans and gorillas rather than chimpanzees, has led to renewed interest in the comparative analysis of human and extant ape scapular form. To facilitate the functional interpretation of differences in ape scapulae, particularly in regard to relative scapular fossa size, we used electromyography (EMG) to document the activity patterns in all four rotator cuff muscles in orangutans and gibbons, comparing the results with previously published data for chimpanzees. The EMG results indicate that the distinctive contributions of each cuff muscle to locomotion are the same in the three ape species, failing to support inferences of differences in rotator cuff function based on relative scapular fossa size comparisons. It is also shown that relative scapular fossa size is not in fact a good predictor of either the relative masses or cross-sectional areas of the rotator cuff muscles in apes, and relative fossa size gives a false impression of the importance of individual cuff muscles to locomotor differences among apes. A possible explanation for the disparity between fossa and muscle size relates to the underappreciated role of the scapular spine in structural reinforcement of the blade.

Electromyography of wrist and finger flexor muscles in olive baboons (Papio anubis).

Some non-human primates use digitigrade hand postures when walking slowly on the ground. As a component of an extended limb, a digitigrade posture can help minimize wrist joint moments thereby requiring little force production directly from wrist flexors (and/or from the assistance of finger flexors) to maintain limb posture. As a consequence, less active muscle volume would be required from these anti-gravity muscles and overall metabolic costs associated with locomotion could be reduced. To investigate whether the use of digitigrade hand postures during walking in primates entails minimal use of anti-gravity muscles, this study examined electromyography (EMG) patterns in both the wrist and finger flexor muscles in facultatively digitigrade olive baboons (Papio anubis) across a range of speeds. The results demonstrate that baboons can adopt a digitigrade hand posture when standing and moving at slow speeds without requiring substantial EMG activity from distal anti-gravity muscles. Higher speed locomotion, however, entails increasing EMG activity and is accompanied by a dynamic shift to a more palmigrade-like limb posture. Thus, the ability to adopt a digitigrade hand posture by monkeys is an adaptation for ground living, but it was never co-opted for fast locomotion. Rather, digitigrady in primates appears to be related to energetic efficiency for walking long distances.

Hallucal grasping in Nycticebus coucang: further implications for the functional significance of a large peroneal process.

Euprimate grasping feet are characterized by a suite of morphological traits, including an enlarged peroneal process on the base of the first metatarsal, which serves as the insertion site of the peroneus longus muscle. In prosimians, a large process has typically been associated with a powerful hallucal grasp via the contraction of the peroneus longus to adduct the hallux. Recent electromyography (EMG) studies have documented that peroneus longus does not contribute substantially to hallucal grasping in lemurids (Boyer et al., 2007). However, non-lemurid prosimians have a I-V opposable grasp complex that is morphologically different and phylogenetically more primitive than the I-II adductor grasp complex of the lemurids previously studied. Therefore, it is possible that peroneus longus did function during grasping in early euprimates, but lost this function in large-bodied lemurids. The present study tests the hypothesis that a large peroneal process is related to powerful grasping ability in primates displaying the more primitive I-V grasp complex. We use EMG to evaluate the recruitment of peroneus longus, other crural muscles, and adductor hallucis in static and locomotor grasping activities of the slow loris (Nycticebus coucang). Results show that peroneus longus is active during grasping behaviors that require the subject to actively resist inversion of the foot, and likely contributes to a hallucal grasp in these activities. Peroneus longus activity level does not differ between grasping and power grasping activities, nor does it differ between grasping and non-grasping locomotor modes. Conversely, the digital flexors and hallucal adductor are recruited at higher levels during power grasping and grasping locomotor modes. Consequently, we reject the hypothesis that an enlarged peroneal process represents an adaptation specifically to enhance the power of the I-V grasp, but accept that the muscle likely plays a role in adducting the hallux during grasping behaviors that require stabilization of the ankle, and suggest that further work is necessary to determine if this role is sufficient to drive selection for a large peroneal process.

Hip extensor EMG and forelimb/hind limb weight support asymmetry in primate quadrupeds.

Higher weight support on the hind limb than forelimb is among the distinctive characteristics of primate quadrupeds. Although often assumed to be due to a more posteriorly positioned whole body center of mass, there are little data to support such a difference. Reynolds (1985. Am J Phys Anthropol 67:335-349) notes that the distribution of forces on the limbs can also be influenced by average limb posture, but suggests that this effect is too small to account for the asymmetry in weight support observed in primates. Instead, he proposes that high hind limb forces are brought about by an active process of shifting weight off the forelimbs and onto the hind limbs through use of hind limb retractors. In this study, we use video records of walking animals to explore the degree to which average limb posture in primates and other quadrupedal mammals deviates from vertical, and use electromyography to test Reynolds' model of hind limb retractor activity and posterior weight shift. The limb posture results indicate that primate forelimbs oscillate about a vertical or slightly retracted axis, and though the hind limbs are slightly protracted, the magnitude of deviation from vertical is too small to have a major effect on weight support distribution. The electromyographic results reveal higher levels of hip extensor activity in antipronograde primates that bear a higher proportion of weight on their hind limbs. This lends support to Reynolds' suggestion that some primates use muscles to actively shift weight onto hind limbs to relieve stresses on forelimbs less well structured for weight support.

Telemetered electromyography of peroneus longus in Varecia variegata and Eulemur rubriventer: implications for the functional significance of a large peroneal process.

A foot specialized for grasping small branches with a divergent opposable hallux (hallucal grasping) represents a key adaptive complex characterizing almost all arboreal non-human euprimates. Evolution of such grasping extremities probably allowed members of a lineage leading to the common ancestor of modern primates to access resources available in a small-branch niche, including angiosperm products and insects. A better understanding of the mechanisms by which euprimates use their feet to grasp will help clarify the functional significance of morphological differences between the euprimate grasp complex and features representing specialized grasping in other distantly related groups (e.g., marsupials and carnivorans) and in closely related fossil taxa (e.g., plesiadapiforms). In particular, among specialized graspers euprimates are uniquely characterized by a large peroneal process on the base of the first metatarsal, but the functional significance of this trait is poorly understood. We tested the hypothesis that the large size of the peroneal process corresponds to the pull of the attaching peroneus longus muscle recruited to adduct the hallux during grasping. Using telemetered electromyography on three individuals of Varecia variegata and two of Eulemur rubriventer, we found that peroneus longus does not generally exhibit activity consistent with an important function in hallucal grasping. Instead, extrinsic digital flexor muscles and, sometimes, the intrinsic adductor hallucis are active in ways that indicate a function in grasping with the hallux. Peroneus longus helps evert the foot and resists its inversion. We conclude that the large peroneal tuberosity that characterizes the hallucal metatarsal of prosimian euprimates does not correlate to "powerful" grasping with a divergent hallux in general, and cannot specifically be strongly linked to vertical clinging and climbing on small-diameter supports. Thus, the functional significance of this hallmark, euprimate feature remains to be determined.

Humeral retractor EMG during quadrupedal walking in primates.

The mammalian humeral retractors latissimus dorsi, teres major and caudal parts of the pectoral muscles are commonly thought to contribute to forward impulse during quadrupedal locomotion by pulling the body over the supporting forelimb. While most electromyographic studies on recruitment patterns for these muscles tend to support this functional interpretation, data on muscle use in chimpanzees and vervet monkeys have suggested that the humeral retractors of nonhuman primates are largely inactive during the support phase of quadrupedal locomotion. In the chimpanzee and vervet monkey, in contrast to what has been documented for other mammals, the contributions of latissimus dorsi, caudal pectoralis major, and teres major during quadrupedal locomotion are restricted to slowing down the swinging forelimb in preparation for hand touchdown and/or retracting the humerus to help lift the hand off the substrate at the initiation of swing phase. Based on these results, it has been proposed that unique patterns of shoulder muscle recruitment are among a set of characteristics that distinguish the form of quadrupedalism displayed by nonhuman primates from that of other nonprimate mammals. However, two primate taxa is a limited sample upon which to base such far-reaching conclusions. Here we report on the activity patterns for the humeral retractors during quadrupedal walking in an additional eight species of nonhuman primates. There is some variability in the activity patterns for latissimus dorsi, caudal pectoralis major and teres major, both between and within species, but in general the results confirm that the humeral retractors of primate quadrupeds do not contribute to forward impulse by pulling the body over the supporting forelimb.

Maintenance of above-branch balance during primate arboreal quadrupedalism: coordinated use of forearm rotators and tail motion.

Animals that live and travel in trees display a variety of morphological and behavioral adaptations to help them maintain balance on narrow flexible supports. Among these adaptations are long tails that can be used as counterweights, and freely mobile limbs in order to reach discontinuous supports. Here we describe two additional ways in which these features can contribute to balance during arboreal locomotion. Electromyographic (EMG) recordings of the forearm rotators pronator quadratus and supinator during over-ground and above-branch quadrupedal locomotion in five species of Old World monkeys revealed their contribution to shifting the weight of the body to help change the direction of travel and maintain balance on a branch. In addition, we observed a coordinated mechanism consisting of a sweeping tail rotation toward the direction of imbalance, to impart an angular momentum to the body that assists in the restoration of balance. While all five primate species utilized forearm rotators to shift their bodies toward one side or the other during quadrupedal walking along a branch, the tail-whip mechanism was most frequently used by the largest and most terrestrial species. We suggest that their large size and/or terrestrial habits have made them less adept at arboreal locomotion, and therefore most likely to utilize auxiliary balancing mechanisms. The usefulness of a long tail as a balancing aid during arboreal locomotion highlights the puzzling nature of the evolutionary loss of a tail in the ape and human lineage.