Jumping performance in tree squirrels: Insights into primate evolution.

Morphological traits suggesting powerful jumping abilities are characteristic of early crown primate fossils. Because tree squirrels lack certain 'primatelike' grasping features but frequently travel on the narrow terminal branches of trees, they make a viable extant model for an early stage of primate evolution. Here, we explore biomechanical determinants of jumping performance in the arboreal Eastern gray squirrel (Sciurus carolinensis, n = 3) as a greater understanding of the biomechanical strategies that squirrels use to modulate jumping performance could inform theories of selection for increased jumping ability during early primate evolution. We assessed vertical jumping performance by using instrumented force platforms upon which were mounted launching supports of various sizes, allowing us to test the influence of substrate diameter on jumping kinetics and performance. We used standard ergometric methods to quantify jumping parameters (e.g., takeoff velocity, total displacement, peak mechanical power) from force platform data during push-off. We found that tree squirrels display divergent mechanical strategies according to the type of substrate, prioritizing force production on flat ground versus center of mass displacement on narrower poles. As jumping represents a significant part of the locomotor behavior of most primates, we suggest that jumping from small arboreal substrates may have acted as a potential driver of the selection for elongated hindlimb segments in primates, allowing the center of mass to be accelerated over a longer distance-and thereby reducing the need for high substrate reaction forces.

Ontogenetic changes to metacarpal trabecular bone structure in mountain and western lowland gorillas.

The trabecular bone morphology of adult extant primates has been shown to reflect mechanical loading related to locomotion. However, ontogenetic studies of humans and other mammals suggest an adaptive lag between trabecular bone response and current mechanical loading patterns that could result in adult trabecular bone morphology reflecting juvenile behaviours. This study investigates ontogenetic changes in the trabecular bone structure of the third metacarpal of mountain gorillas (Gorilla beringei beringei; n = 26) and western lowland gorillas (Gorilla gorilla gorilla; n = 26) and its relationship to expected changes in locomotor loading patterns. Results show that trabecular bone reflects predicted mechanical loading throughout ontogeny. Bone volume fraction, trabecular thickness and trabecular number are low at birth and increase with age, although degree of anisotropy remains relatively stable throughout ontogeny. A high concentration of bone volume fraction can be observed in the distopalmar region of the third metacarpal epiphysis in early ontogeny, consistent with the high frequency of climbing, suspensory and other grasping behaviours in young gorillas. High trabecular bone concentration increases dorsally in the epiphysis during the juvenile period as terrestrial knuckle-walking becomes the primary form of locomotion. However, fusion of the epiphysis does not take place until 10-11 years of age, and overall trabecular structure does not fully reflect the adult pattern until 12 years of age, indicating a lag between adult-like behaviours and adult-like trabecular morphology. We found minimal differences in trabecular ontogeny between mountain and western lowland gorillas, despite presumed variation in the frequencies of arboreal locomotor behaviours. Altogether, ontogenetic changes in Gorilla metacarpal trabecular structure reflect overall genus-level changes in locomotor behaviours throughout development, but with some ontogenetic lag that should be considered when drawing functional conclusions from bone structure in extant or fossil adolescent specimens.

Effects of human variation on foot and ankle pain in rural Madagascar.

OBJECTIVES: Foot and ankle dysfunction in barefoot/minimally shod populations remains understudied. Although factors affecting musculoskeletal pain in Western populations are well-studied, little is known about how types of work, gender, and body shape influence bone and joint health in non-Western and minimally shod communities. This study examines the effect of human variation on locomotor disability in an agrarian community in Madagascar. MATERIALS AND METHODS: Foot measurements were collected along with height, weight, age, and self-report data on daily activity and foot and ankle pain from 41 male and 48 female adults. A short form revised foot function index (FFI-R), that measures functional disability related to foot pain, was calculated. Raw and normalized foot measurements were compared by gender and used in a multiple linear regression model to determine predictors of FFI-R. RESULTS: Compared to men, women reported higher FFI-R scores (p = 0.014), spent more time on their feet (p = 0.019), and had higher BMIs (p = 0.0001). For their weight, women had significantly smaller and narrower feet than men. Bimalleolar breadth (p = 0.0005) and foot length (p = 0.0223) standardized by height, time spent on feet (p = 0.0102), ankle circumference standardized by weight (p = 0.0316), and age (p = 0.0090) were significant predictors of FFI-R score. DISCUSSION: Our findings suggest that human variation in anatomical and behavioral patterns serve as significant explanations for increased foot and ankle pain in women in this non-Western rural population. Foot and ankle pain were prevalent at similar levels to those in industrialized populations, indicating that research should continue to examine its effect on similar barefoot/minimally shod communities.

Mechanics of heel-strike plantigrady in African apes.

The initiation of a walking step with a heel strike is a defining characteristic of humans and great apes but is rarely found in other mammals. Despite the considerable importance of heel strike to an understanding of human locomotor evolution, no one has explicitly tested the fundamental mechanical question of why great apes use a heel strike. In this report, we test two hypotheses (1) that heel strike is a function of hip protraction and/or knee extension and (2) that short-legged apes with a midfoot that dorsiflexes at heel lift and long digits for whom digitigrady is not an option use heel-strike plantigrady. This strategy increases hip translation while potentially moderating the cost of redirecting the center of mass ('collisional costs') during stance via rollover along the full foot from the heel to toes. We quantified hind limb kinematics and relative hip translation in ten species of primates, including lemurs, terrestrial and arboreal monkeys, chimpanzees, and gorillas. Chimpanzees and gorillas walked with relatively extended knees but only with moderately protracted hips or hind limbs, partially rejecting the first hypothesis. Nonetheless, chimpanzees attained relative hip translations comparable with those of digitigrade primates. Heel-strike plantigrady may be a natural result of a need for increased hip translations when forelimbs are relatively long and digitigrady is morphologically restricted. In addition, foot rollover from the heel to toe in large, short-legged apes may reduce energetic costs of redirecting the center of mass at the step-to-step transition as it appears to do in humans. Heel strike appears to have been an important mechanism for increasing hip translation, and possibly reducing energetic costs, in early hominins and was fundamental to the evolution of the modern human foot and human bipedalism.

Mechanisms for the functional differentiation of the propulsive and braking roles of the forelimbs and hindlimbs during quadrupedal walking in primates and felines.

During quadrupedal walking in most animals, the forelimbs play a net braking role, whereas the hindlimbs are net propulsive. However, the mechanism by which this differentiation occurs remains unclear. Here, we test two models to explain this pattern using primates and felines: (1) the horizontal strut effect (in which limbs are modeled as independent struts), and (2) the linked strut model (in which limbs are modeled as linked struts with a center of mass in between). Video recordings were used to determine point of contact, timing of mid-stance, and limb protraction/retraction duration. Single-limb forces were used to calculate contact time, impulses and the proportion of the stride at which the braking-to-propulsive transition (BP) occurred for each limb. We found no association between the occurrence of the BP and mid-stance, little influence of protraction and retraction duration on the braking-propulsive function of a limb, and a causative relationship between vertical force distribution between limbs and the patterns of horizontal forces. These findings reject the horizontal strut effect, and provide some support for the linked strut model, although predictions were not perfectly matched. We suggest that the position of the center of mass relative to limb contact points is a very important, but not the only, factor driving functional differentiation of the braking and propulsive roles of the limbs in quadrupeds. It was also found that primates have greater differences in horizontal impulse between their limbs compared with felines, a pattern that may reflect a fundamental arboreal adaptation in primates.

Ontogenetic changes in limb postures and their impact on effective limb length in baboons (Papio cynocephalus).

OBJECTIVES: Digitigrade hand and foot postures and extended elbows and knees are considered adaptations to running in cursorial mammals because they increase effective limb lengths (ELLs). However, the relationship between digitigrady and ELL in primates is not well understood. We documented the ontogeny of limb postures in baboons to better understand the function of digitigrady during walking. We hypothesized that the hand and foot would become more elevated and the elbow and knee more extended, leading to increased relative ELLs throughout ontogeny. MATERIALS AND METHODS: Longitudinal kinematic data were collected on four infant yellow baboons (Papio cynocephalus) as they aged from two to nine months, and again at two to three years. Hand/foot postures, elbow/knee angles, relative fore/hind limb ELLs, and dimensionless velocity were measured for 404 symmetrical walking strides. RESULTS: Digitigrade hand and foot postures were preferred at all ages. The elbow extended slightly and the knee flexed slightly with age. Elevated proximal hands, extended elbows, and extended knees were associated with long relative ELLs. For a given age, relative hind limb ELL was longer than relative forelimb ELL. DISCUSSION: In the forelimb, digitigrade hand postures and extended elbows function to increase relative ELL at slow walking velocity. Increased forelimb ELL may be an attempt to equalize forelimb and hind limb ELLs in baboons with an absolutely longer hind limb. Pedal digitigrady is not a main contributing factor to hind limb ELL. Results suggest that manual and pedal digitigrady in terrestrial cercopithecoids does not function to increase velocity.

Trabecular architecture in the StW 352 fossil hominin calcaneus.

Australopithecus africanus has been interpreted as having a rigid lateral foot. One mechanism contributing to a rigid foot during push-off in humans is a calcaneocuboid joint (CCJ) with limited dorsiflexion and a "close-packed" talocalcaneal joint (TCJ). In contrast, apes likely have a greater CCJ range of motion and lack a close-packed TCJ. Differences in tarsal arthrokinematics may result in different joint loading environments. In Homo sapiens, we tested the hypothesis that dorsal and plantar CCJ and the TCJ show evidence of predictable habitual loading. In Pan troglodytes, Gorilla gorilla, Gorilla beringei, and Papio ursinus, we tested the hypothesis that only the dorsal CCJ shows evidence of predictable loading. Specifically, we predicted similarity in trabecular properties across the dorsal and plantar CCJ in H. sapiens, but dissimilarity in non-humans. Additionally, we investigated trabecular properties of an A. africanus calcaneus (StW 352) to evaluate joint loading patterns in this hominin and ultimately address the evolution of these properties in H. sapiens. Contrary to predictions, the H. sapiens dorsal CCJ has a significantly higher elongation index, bone volume fraction, trabecular thickness, and trabecular number than the plantar CCJ, while trabecular properties in non-humans do not always differ as predicted between regions. H. sapiens exhibits trabecular morphology indicative of less variable TCJ loading than other groups, having the most anisotropic and rod-like struts oriented in line with predicted principal loads. Multivariate analysis shows that the StW 352 dorsal CCJ matches P. ursinus best, while the plantar CCJ matches G. beringei best and the TCJ matches that of G. gorilla best. Overall patterns suggest that the StW 352 calcaneus experienced more variable loading than H. sapiens, but less variable loading than P. troglodytes, G. gorilla, G. beringei, and P. ursinus, consistent with a large range of foot movements, probably reflecting locomotor kinematics that are unlike those of living humans or apes.

Ontogenetic scaling of fore limb and hind limb joint posture and limb bone cross-sectional geometry in vervets and baboons.

OBJECTIVES: Previous studies suggest that the postures habitually adopted by an animal influence the mechanical loading of its long bones. Relatively extended limb postures in larger animals should preferentially reduce anteroposterior (A-P) relative to mediolateral (M-L) bending of the limb bones and therefore decrease A-P/M-L rigidity. We test this hypothesis by examining growth-related changes in limb bone structure in two primate taxa that differ in ontogenetic patterns of joint posture. MATERIALS AND METHODS: Knee and elbow angles of adult and immature vervets (Chlorocebus aethiops, n = 16) were compared to published data for baboons (Papio hamadryas ursinus, n = 33, Patel et al., ). Ontogenetic changes in ratios of A-P/M-L bending rigidity in the femur and humerus were compared in skeletal samples (C. aethiops, n = 28; P. cynocephalus, n = 39). Size changes were assessed with linear regression, and age group differences tested with ANOVA. RESULTS: Only the knee of baboons shows significant postural change, becoming more extended with age and mass. A-P/M-L bending rigidity of the femur decreases during ontogeny in immature and adult female baboons only. Trends in the humerus are less marked. Adult male baboons have higher A-P/M-L bending rigidity of the femur than females. CONCLUSIONS: The hypothesized relationship between more extended joints and reduced A-P/M-L bending rigidity is supported by our results for immature and adult female baboon hind limbs, and the lack of significant age changes in either parameter in forelimbs and vervets. Adult males of both species depart from general ontogenetic trends, possibly due to socially mediated behavioral differences between sexes. Am J Phys Anthropol 161:72-83, 2016. © 2016 Wiley Periodicals, Inc.

Metacarpal head biomechanics: a comparative backscattered electron image analysis of trabecular bone mineral density in Pan troglodytes, Pongo pygmaeus, and Homo sapiens.

Great apes and humans use their hands in fundamentally different ways, but little is known about joint biomechanics and internal bone variation. This study examines the distribution of mineral density in the third metacarpal heads in three hominoid species that differ in their habitual joint postures and loading histories. We test the hypothesis that micro-architectural properties relating to bone mineral density reflect habitual joint use. The third metacarpal heads of Pan troglodytes, Pongo pygmaeus, and Homo sapiens were sectioned in a sagittal plane and imaged using backscattered electron microscopy (BSE-SEM). For each individual, 72 areas of subarticular cortical (subchondral) and trabecular bone were sampled from within 12 consecutive regions of the BSE-SEM images. In each area, gray levels (representing relative mineralization density) were quantified. Results show that chimpanzee, orangutan, and human metacarpal III heads have different gray level distributions. Weighted mean gray levels (WMGLs) in the chimpanzee showed a distinct pattern in which the 'knuckle-walking' regions (dorsal) and 'climbing' regions (palmar) are less mineralized, interpreted to reflect elevated remodeling rates, than the distal regions. Pongo pygmaeus exhibited the lowest WMGLs in the distal region, suggesting elevated remodeling rates in this region, which is loaded during hook grip hand postures associated with suspension and climbing. Differences among regions within metacarpal heads of the chimpanzee and orangutan specimens are significant (Kruskal-Wallis, p < 0.001). In humans, whose hands are used for manipulation as opposed to locomotion, mineralization density is much more uniform throughout the metacarpal head. WMGLs were significantly (p < 0.05) lower in subchondral compared to trabecular regions in all samples except humans. This micro-architectural approach offers a means of investigating joint loading patterns in primates and shows significant differences in metacarpal joint biomechanics among great apes and humans.

Trabecular structure of the elbow reveals divergence in knuckle-walking biomechanical strategies of African apes.

African apes engage in a distinct form of locomotion called knuckle-walking, but there is much ambiguity as to when and how this locomotor behavior evolved. This study aims to elucidate potential differences in knuckle-walking elbow posture and loading in African apes through the study of trabecular bone. Using a whole-epiphysis approach, we quantified variation in the trabecular structure of the distal humerus of chimpanzees, western lowland gorillas, and mountain gorillas in comparison to orang-utans, siamangs, and a sample of Old and New World monkeys. Results demonstrate differences in the distribution of trabecular bone within the distal humerus that are consistent across taxa that habitually use a flexed-elbow posture in comparison to those that use an extended elbow during locomotion. Western lowland gorillas show an extended-elbow pattern consistent with the straight forelimb position during knuckle-walking, whereas chimpanzees show a flexed-elbow pattern. Unexpectedly, mountain gorillas show an intermediate pattern between their western counterparts and chimpanzees. The differences found in elbow joint posture between chimpanzees and gorillas, and between gorilla species, point to diversification in the knuckle-walking biomechanical strategies among African apes, which has implications in the debate regarding the locomotor behavior from which human bipedalism arose.

The effect of ankle osteoarthritis and total ankle arthroplasty on center of pressure position.

Total ankle arthroplasty (TAA) is a common surgical approach for patients with end-stage ankle osteoarthritis (OA). However, very little is known about the path of the center of pressure (COP) of the foot, and thus important aspects of load transfer, muscle mechanical advantage, and balance, in patients before or after surgery. The objective of this study was to trace the pathway of the COP under the foot in patients with symptomatic ankle OA, comparing asymmetry between affected and unaffected limbs. From force plate data, proximodistal and mediolateral positions of the COP beneath the foot were calculated and compared for the affected and unaffected foot in patients with unilateral ankle OA (N = 93) before and after TAA. Gender and age at surgery had little or no effect in this study. Patients with ankle OA had minimal COP position asymmetry before surgery, and this asymmetry was reduced following surgery. Before surgery, patients had a slower walking speed and a shorter path of the COP which began relatively distal to the heel and ended relatively proximal to the hallux. TAA increased the proximodistal distance the COP traveled under both the unaffected and affected foot, a pattern that was maintained for over 2-year postsurgery. TAA allows patients with ankle OA to maintain a longer COP path than they had before surgery on both sides that is closer to that reported for unaffected individuals, extending effectively from the heel to the hallux, potentially improving pedal mechanics.

Ontogenetic changes in foot strike pattern and calcaneal loading during walking in young children.

The assumption that the morphology of the human calcaneus reflects high and cyclical impact forces at heel strike during adult human walking has never been experimentally tested. Since a walking step with a heel strike is an emergent behavior in children, an ontogenetic study provides a natural experiment to begin testing the relationship between the mechanics of heel strike and calcaneal anatomy. This study examined the ground reaction forces (GRFs) of stepping in children to determine the location of the center of pressure (COP) relative to the calcaneus and the orientation and magnitude of ground reaction forces during foot contact. Three-dimensional kinematic and kinetic data were analyzed for 18 children ranging in age from 11.5 to 43.1 months. Early steppers used a flat foot contact (FFC) and experienced relatively high vertical and resultant GRFs with COP often anterior to the calcaneus. More experienced walkers used an initial heel contact (IHC) in which GRFs were significantly lower but the center of pressure remained under the heel a greater proportion of time. Thus, during FFC the foot experienced higher loading, but the heel itself was relatively wider and the load was distributed more evenly. In IHC walkers load was concentrated on the anterior calcaneus and a narrower heel, suggesting a need for increased calcaneal robusticity during development to mitigate injury. These results provide new insight into foot loading outside of typical mature contact patterns, inform structure-function relationships during development, and illuminate potential causes of heel injury in young walkers.