Convergence of forelimb and hindlimb Natural Pendular Period in baboons (Papio cynocephalus) and its implication for the evolution of primate quadrupedalism

The patterns of muscle mass distribution along the lengths of limbs may have important effects on the mechanics and energetics of quadrupedalism. Specifically, Myers and Steudel (J. Morphol. 234 (1997) 183) have shown that fore- and hindlimb Natural Pendular Periods (NPPs) may affect quadrupedal kinematics and must converge to reduce locomotor energetic costs. This study quantifies patterns of limb mass distribution in a live sample of Papio cynocephalus using limb inertial properties (mass, center of mass, mass moment of inertia, and radius of gyration). These inertial properties are calculated using a geometric modeling technique similar to that of Crompton et al. (Am. J. phys. Anthrop. 99 (1996) 547). The inertial properties in Papio are compared to those of Canis from Myers and Steudel (J. Morphol. 234 (1997) 183). The Papio sample has convergent fore- and hindlimb NPPs. Additionally, these limb NPPs are relatively large compared to those of Canis due to the relatively distally distributed limb mass in the Papio sample (relatively large limb masses, relatively distal centers of mass and radii of gyration, and relatively large limb mass moments of inertia). This relatively distal limb mass appears related to the grasping abilities of their hands and feet. Causal links are explored between limb shape adaptations for grasping hands and feet and the kinematics of primate quadrupedalism. In particular, if primates in general follow Papio's limb mass distribution pattern, then relatively large limb NPPs may lead to the relatively low stride frequencies already documented for primates. The kinematics of primate quadrupedalism appears to have been strongly influenced by both selection for grasping hands and feet and selection for reduced locomotor energetic costs.     

Ontogeny of limb mass distribution in infant baboons (Papio cynocephalus)

Primates have more distally distributed limb muscle mass compared to most nonprimate mammals. The heavy distal limbs of primates are likely related to their strong manual and pedal grasping abilities, and interspecific differences in limb mass distributions among primates are correlated with the amount of time spent on arboreal supports. Within primate species, individuals at different developmental stages appear to differ in limb mass distribution patterns. For example infant macaques have more distally distributed limb mass at young ages. A shift from distal to proximal limb mass concentrations coincides with a shift from dependent travel (grasping their mother's hair) to independent locomotion. Because the functional demands placed on limbs may differ between taxa, understanding the ontogeny of limb mass distribution patterns is likely an essential element in interpreting the diversity of limb mass distribution patterns present in adult primates. This study examines changes in limb inertial properties during ontogeny in a longitudinal sample of infant baboons (Papio cynocephalus). The results of this study show that infant baboons undergo a transition from distal to proximal limb mass distribution patterns. This transition in limb mass distribution coincides with the transition from dependent to independent locomotion during infant development. Compared to more arboreal macaques, infant baboons undergo a faster transition to more proximal limb mass distribution patterns. These results suggest that functional demands placed on the limbs during ontogeny have a strong impact on the development of limb mass distribution patterns.     

Understanding hind limb weight support in chimpanzees with implications for the evolution of primate locomotion

Most quadrupedal mammals support a larger amount of body weight on their forelimbs compared with their hind limbs during locomotion, whereas most primates support more of their body weight on their hind limbs. Increased hind limb weight support is generally interpreted as an adaptation that reduces stress on primates' highly mobile forelimb joints. Thus, increased hind limb weight support was likely vital for the evolution of primate arboreality. Despite its evolutionary importance, the mechanism used by primates to achieve this important kinetic pattern remains unclear. Here, we examine weight support patterns in a sample of chimpanzees (Pan troglodytes) to test the hypothesis that limb position, combined with whole body center of mass position (COM), explains increased hind limb weight support in this taxon. Chimpanzees have a COM midway between their shoulders and hips and walk with a relatively protracted hind limb and a relatively vertical forelimb, averaged over a step. Thus, the limb kinematics of chimpanzees brings their feet closer to the COM than their hands, generating greater hind limb weight support. Comparative data suggest that these same factors likely explain weight support patterns for a broader sample of primates. It remains unclear whether primates use these limb kinematics to increase hind limb weight support, or whether they are byproducts of other gait characteristics. The latter hypothesis raises the intriguing possibility that primate weight support patterns actually evolved as byproducts of other traits, or spandrels, rather than as adaptations to increase forelimb mobility. Am J Phys Anthropol, 2009. © 2008 Wiley‐Liss, Inc.     

Stride length and its determinants in humans, early hominids, primates, and mammals

Primate stride lengths during quadrupedal locomotion are very long when compared to those of nonprimate quadrupedal mammals at the speed of trot/gallop transition. These exceptional lengths are a consequence of the relatively long limbs of primates and the large angular excursions of their limbs during quadrupedalism. When quadrupedal primates employ bipedal gaits they exhibit much lower angular excursions. Consequently their bipedal stride lengths do not appear to be exceptional in length when compared to other mammals. Angular excursions of the lower limbs of modern humans are not exceptionally large. However, when running, humans exhibit relatively long periods of flight (i.e., they have low duty factors) when compared to other mammals including primates. Because of these long periods of flight and their relative long lower limbs, humans have running stride lengths that are at the lower end of the range of stride lengths of quadrupedal primates. The stride length of the Laetoli hominid trails are evaluated in this context.     

Uniqueness of primate forelimb posture during quadrupedal locomotion

Among the characteristics that are thought to set primate quadrupedal locomotion apart from that of nonprimate mammals are a more protracted limb posture and larger limb angular excursion. However, kinematic aspects of primate or nonprimate quadrupedal locomotion have been documented in only a handful of species, and more widely for the hind than the forelimb. This study presents data on arm (humerus) and forelimb posture during walking for 102 species of mammals, including 53 nonhuman primates and 49 nonprimate mammals. The results demonstrate that primates uniformly display a more protracted arm and forelimb at hand touchdown of a step than nearly all other mammals. Although primates tend to end a step with a less retracted humerus, their total humeral or forelimb angular excursion exceeds that of other mammals. It is suggested that these features are components of functional adaptations to locomotion in an arboreal habitat, using clawless, grasping extremities.     

Ontogenetic Scaling of Fore- and Hind Limb Posture in Wild Chacma Baboons (Papio hamadryas ursinus)

Large-scale interspecific studies of mammals ranging between 0.04–280 kg have shown that larger animals walk with more extended limb joints. Within a taxon or clade, however, the relationship between body size and joint posture is less straightforward. Factors that may affect the lack of congruence between broad and narrow phylogenetic analyses of limb kinematics include limited sampling of (1) ranges of body size, and/or (2) numbers of individuals. Unfortunately, both issues are inherent in laboratory-based or zoo locomotion research. In this study, we examined the relationship between body mass and elbow and knee joint angles (our proxies of fore- and hind limb posture, respectively) in a cross-sectional ontogenetic sample of wild chacma baboons (Papio hamadryas ursinus) habituated in the De Hoop Nature Reserve, South Africa. Videos were obtained from 33 individuals of known age (12 to ≥108 months) and body mass (2–29.5 kg) during walking trials. Results show that older, heavier baboons walk with significantly more extended knee joints but not elbow joints. This pattern is consistent when examining only males, but not within the female sample. Heavier, older baboons also display significantly less variation in their hind limb posture compared to lighter, young animals. Thus, within this ontogenetic sample of a single primate species spanning an order of magnitude in body mass, hind limb posture exhibited a postural scaling phenomenon while the forelimbs did not. These findings may further help explain 1) why younger mammals (including baboons) tend to have relatively stronger bones than adults, and 2) why humeri appear relatively weaker than femora (in at least baboons). Finally, this study demonstrates how field-acquired kinematics can help answer fundamental biomechanical questions usually addressed only in animal gait laboratories.     

Lateral sequence walking in infant Papio cynocephalus: implications for the evolution of diagonal sequence walking in primates

One of the most distinctive aspects of primate quadrupedal walking is the use of diagonal sequence footfalls in combination with diagonal-couplets interlimb timing. Numerous hypotheses have been offered to explain why primates might have evolved this type of gait, yet this important question remains unresolved. Because infant primates use a wider variety of quadrupedal gaits than do adults, they provide a natural experiment with which to test hypotheses about the evolution of unique aspects of primate quadrupedalism. In this study, we present kinematic data on two infant baboons (Papio cynocephalus) in order to test the recent hypothesis that diagonal sequence, diagonal couplets walking might have evolved in primates because their limb positioning provides stability in a small branch environment (Cartmill et al. [2002] Zool J Linn Soc 136:401-420). To assess hindlimb position at the moment of forelimb touchdown, we measured hindlimb angular excursion and ankle position for 84 walking strides, across three different types of gaits (diagonal sequence, diagonal couplets (DSDC); lateral sequence lateral couplets (LSLC); and lateral sequence diagonal couplets (LSDC)). Results indicate that if a forelimb were to contact an unstable substrate, LSLC walking provides as much, and perhaps more, stability when compared to DSDC walking. Therefore, it appears that this moment in a stride was unlikely to be a particularly important selective factor in the evolution of DSDC walking. Further insight into this issue will likely be gained by observations of primate quadrupedalism in natural environments, where the use of lateral sequence gaits might be more common than currently known.     

Bipedal versus Quadrupedal Hind Limb and Foot Kinematics in a Captive Sample of <Emphasis Type="Italic">Papio anubis:</Emphasis> Setup and Preliminary Results

Setups that integrate both kinematics and morpho-functional investigations of a single sample constitute recent developments in the study of nonhuman primate bipedalisms. We introduce the integrated setup built at the Primatology Station of the French National Centre for Scientific Research (CNRS), which allows analysis of both bipedal and quadrupedal locomotion in a population of 55–60 captive olive baboons. As a first comparison, we present the hind limb kinematics of both locomotor modalities in 10 individuals, focusing on the stance phase. The main results are: 1) differences in bipedal and quadrupedal kinematics at the hip, knee, and foot levels; 2) a variety of foot contacts to the ground, mainly of semiplantigrade type, but also of plantigrade type; 3) equal variations between bipedal and quadrupedal foot angles; 4) the kinematics of the foot joints act in coordinated and stereotyped manners, but are triggered differently according to whether the support is bipedal or quadrupedal. Although very occasionally realized, the bipedal walk of olive baboon appears to be a habitual and nonerratic locomotor modality.     

Kinematics of the cercopithecine foot on arboreal and terrestrial substrates with implications for the interpretation of hominid terrestrial adaptations

The stereotyped characterizations of quadrupedal foot postures were tested by examining the kinematics of the cercopithecine foot on arboreal and terrestrial supports. Strictly arboreal species were compared with semi-terrestrial species for Cercopithecus, Cercocebus, Lophocebus, and Papio, in semi-natural or experimental settings. Results indicate that the kinematics of the cercopithecine arboreal quadruped differ in degree from stereotypical expectations for an arboreal quadruped. The relatively extended, adducted limb movements of the cercopithecines and the emphasis on the central digit as the functional axis of the foot suggest convergence with terrestrial mammalian cursors, and differ from the platyrrhine or colobine arboreal quadruped. The characteristics of the quadrupedal terrestrial primate foot contrast with the very unique pattern seen in the hominid foot. These contrasts provide a new perspective from which to interpret the hominid adaptation, in which the functional axis has remained fixed between the first and second digits. This pattern differs from virtually all other terrestrial mammals. The influence of bipedalism on this functional pattern is examined.     

Lateral bending of the lumbar spine during quadrupedalism in strepsirhines

Much research has been devoted to spinal kinematics of nonmammalian vertebrates, while comparatively little is known about the locomotor role of spinal movements in mammals, especially primates. This study, conducted at the Duke University Primate Center, examines the function of lateral spinal bending during quadrupedal walking among a diverse sample of strepsirhines. The taxa studied include Loris tardigradus (1), Nycticebus coucang (1), N. pygmaeus (1), Cheirogaleus medius (2), Varecia variegata (2), Eulemur fulvus (2), and a total sample size of 261 strides. Lateral bending varies among the taxa with respect to both magnitude and effects of velocity, and does not appear to be correlated with body size. In addition, the timing of lateral bending during a stride appears to differ from that reported for other (nonmammalian) tetrapods. On average, maximum lateral flexion occurs just after ipsilateral foot touchdown, which may be functionally associated with touchdown of the contralateral forelimb during diagonal sequence gait. For some of the taxa, lateral flexion coincides more closely with foot touchdown as velocity increases, suggesting a functional role in increasing hindlimb stride length. Both of these timing patterns contrast with those reported for lizards. Finally, although lorids as a group have been described as having a "sinuous" gait, this study shows more pronounced lateral flexion in Nycticebus than in Loris.     

The hands and feet of Archaeolemur: metrical affinities and their functional significance

Recent expeditions to Madagascar have recovered abundant skeletal remains of Archaeolemur, one of the so-called "monkey lemurs" known from Holocene deposits scattered across the island. These new skeletons are sufficiently complete to permit reassembly of entire hands and feet--postcranial elements crucial to drawing inferences about substrate preferences and positional behavior. Univariate and multivariate analysis of intrinsic hand and foot proportions, phalangeal indices, relative pollex and hallux lengths, phalangeal curvature, and distal phalangeal shape reveal a highly derived and unique morphology for an extinct strepsirrhine that diverges dramatically from that of living lemurs and converges in some respects on that of Old World monkeys (e.g., mandrills, but not baboons or geladas). The hands and feet of Archaeolemur are relatively short (extremely so relative to body size); the carpus and tarsus are both "long" relative to total hand and foot lengths, respectively; phalangeal indices of both the hands and feet are low; both pollex and hallux are reduced; the apical tufts of the distal phalanges are very broad; and the proximal phalanges are slightly curved (but more so than in baboons). Overall grasping capabilities may have been compromised to some extent, and dexterous handling of small objects seems improbable. Deliberate and noncursorial quadrupedalism was most likely practiced on both the ground and in the trees. A flexible locomotor repertoire in conjunction with a eurytopic trophic adaptation allowed Archaeolemur to inhabit much of Madagascar and may explain why it was one of the latest surviving subfossil lemurs.     

Grasping primate development: Ontogeny of intrinsic hand and foot proportions in capuchin monkeys (Cebus albifrons and Sapajus apella)

Young primates have relatively large hands and feet for their body size, perhaps enhancing grasping ability. We test the hypothesis that selection for improved grasping ability is responsible for these scaling trends by examining the ontogeny of intrinsic hand and foot proportions in capuchin monkeys (Cebus albifrons and Sapajus apella). If selection for improved grasping ability is responsible for the observed patterns of hand and foot growth in primates, we predicted that fingers and toes would be longer early in life and proportionally decline with age. We measured the lengths of manual and pedal metapodials and phalanges in a mixed‐longitudinal radiographic sample. Bone lengths were (a) converted into phalangeal indices (summed non‐distal phalangeal length/metapodial length) to test for age‐related changes in intrinsic proportions and (b) fit to Gompertz models of growth to test for differences in the dynamics of phalangeal versus metapodial growth. Manual and pedal phalangeal indices nearly universally decreased with age in capuchin monkeys. Growth curve analyses revealed that metapodials generally grew at a faster rate, and for a longer duration, than corresponding phalanges. Our findings are consistent with the hypothesis that primates are under selection for increased grasping ability early in life. Relatively long digits may be functionally adaptive for growing capuchins, permitting a more secure grasp on both caregivers and arboreal supports, as well as facilitating early foraging. Additional studies of primates and other mammals, as well as tests of grasping performance, are required to fully evaluate the adaptive significance of primate hand and foot growth.     

A dynamic similarity hypothesis for the gaits of quadrupedal mammals

The dynamic similarity hypothesis postulates that different mammals move in a dynamically similar fashion whenever they travel at speeds that give them equal values of a dimensionless parameter, the Froude number. Thus, given information about one species, it could be possible to predict for others relationships between size, speed and features of gait such as stride length, duty factor, the phase relationships of the feet and the patterns of force exerted on the ground.
Data for a diverse sample of mammals have been used to test the hypothesis. It is found to be tenable in many cases when comparisons are confined to quadrupedal mammals of the type described by Jenkins (1971) as "cursorial". Most mammals of mass greater than 5 kg are of this type. Although the hypothesis applies less successfully to comparisons between cursorial and non-cursorial mammals it is shown to be a reasonable approximation even for such comparisons and for comparisons between quadrupedal mammals and bipedal mammals and birds.     

Locomotion in the quail (Coturnix japonica): the kinematics of walking and increasing speed

Hindlimb segmental kinematics and stride characteristics are quantified in several quail locomoting on a treadmill over a six-fold increase in speed. These data are used to describe the kinematics of a walking stride and to identify which limb elements are used to change stride features as speed increases. In quail, the femur does not move during locomotion and the tarsometatarsus-phalangeal joint is a major moving joint; thus, quail have lost the most proximal moving joint and added one distally. The tibiotarsus and tarsometatarsus act together as a fixed strut swinging from the knee during stance phase (the ankle angle remains constant at a given speed) and the tarsometatarsus-phalangeal joint appears to have a major role in increasing limb length during the propulsive phase of the stride. Speed is increased with greater knee extension and by lengthening the tibiotarsus/tarsometatarsus via increased ankle extension at greater speeds. Because the femur is not moved and three distal elements are, quail move the limb segments through a stride and increase speed in a way fundamentally different from other nonavian vertebrates. However, the three moving joints in quail (the knee, ankle, and tarsometatarsophangeal joint) have strikingly similar kinematics to the analogous moving joints (the hip, knee, and ankle) in other vertebrates. Comparisons to other vertebrates indicate that birds appear to have two modes of limb function (three- and four-segment modes) that vary with speed and locomotory habits.     

The Effect of Speed on the Hindlimb Kinematics of the Reeves' Butterfly Lizard,Leiolepis reevesii(Agamidae)

We recorded locomotor performance of Reeves' butterfly lizards(Leiolepis reevesii) on a racetrack and to describe hindlimb kinematic patterns and to evaluate the effect of speed on hindlimb kinematics. The studied lizards predominantly used quadrupedal locomotion at relatively low speeds, but ran bipedally with a digitigrade posture at high speeds. Speed was positively correlated with both stride length and stride frequency, and was negatively correlated with duty factor. Lizards modulated speed probably by a combination of changing frequency and amplitude of limb movements. Within the range of standardized speeds from 50 to 150 cm/s, speed effects on 28 out of a total of 56 kinematic variables were significant. The hip height at footfall increased as speed increased, whereas the amplitude of vertical oscillations of the hip did not vary with speed. The total longitudinal and dorsoventral movements relative to the hip varied with speed for all parts of the limb that were distal to the knee, whereas the lateral movements did not. The knee and ankle angle at footfall varied with speed, but did not at the end of stance. The degree of pelvis rotation during the entire stride cycle did not vary with speed. Our results suggest that pelvic rotation and femoral protraction/retraction have a minor role in modulating speed in L. reevesii.     

Kinematics and spatiotemporal parameters of infant‐carrying in olive baboons

In the field of biomechanics of quadrupedal locomotion in primates, infant‐carrying has received little attention. This study presents the first biomechanical study of infant‐carrying in captive female olive baboons (Papio anubis). We test whether females carrying infants conform 1) to the Support Polygon Model (Rollinson and Martin: Symp Zool Soc Lond 48 (1981) 377–427) of gait selection, according to which diagonality should decrease when the infant is carried cranially and increase when the infant is carried dorsally and caudally; 2) to Biewener's (Biewener: Science 245 ( 1989 ) 45–48) theory of limb postures, according to which females should extend their hind limbs more due to infant load, especially in the later stages when the infant is not fully autonomous but relatively heavy. This study focuses on the sagittal kinematics of quadrupedal gaits (joint angles and spatiotemporal parameters) of four females with and without infant loads at the CNRS Primatology Station (France). High‐speed video recordings were made using the technical platform “Motion Analysis of Primates” available in the animals' place of life. Regarding diagonality, our results do not fully conform to those predicted by the Support Polygon Model of gait selection; however, the model cannot be rejected at this stage in experiment. With regard to limb posture, our results do not support Biewener's (Biewener: Science 245 ( 1989 ) 45–48) theory: loaded females do not extend their hind limbs more as predicted; on the contrary, the hind limbs tend to be more flexed when the infant they carry is relatively heavy. Am J Phys Anthropol 155:392–404, 2014. © 2014 Wiley Periodicals, Inc.     

Ontogeny of limb force distribution in squirrel monkeys (Saimiri boliviensis): insights into the mechanical bases of primate hind limb dominance

The distribution of peak vertical forces between the forelimbs and the hind limbs is one of the key traits distinguishing primate quadrupedal locomotion from that of other mammals. Whereas most mammals generate greater peak vertical forelimb forces, primates generate greater peak vertical hind limb forces. At the ultimate level, hind limb dominance in limb force distribution is typically interpreted as an adaptation to facilitate fine-branch arboreality. However, the proximate biomechanical bases for primate limb force distribution remain controversial. Three models have been previously proposed. The Center of Mass (COM) Position model attributes primates’ unique mode of limb loading to differences in the position of the whole-body COM relative to the hands and feet. The Active Weight Shift model asserts that primates actively redistribute body weight to their hind limbs by pitching the trunk up via the activation of hind limb retractor muscles. Finally, the Limb Compliance model argues that primates selectively mitigate forelimb forces by maintaining a compliant forelimb and a flat shoulder trajectory. Here, a detailed dataset of ontogenetic changes in morphology and locomotor mechanics in Bolivian squirrel monkeys (Saimiri boliviensis) was employed as a model system to evaluate each of these proposed models in turn. Over the first 10 months of life, squirrel monkeys transitioned from forelimb dominant infants to hind limb dominant juveniles, a change that was precipitated by decreases in peak vertical forelimb forces and increases in peak vertical hind limb forces. Results provided some support for all three of the models, although the COM Position and Active Weight Shift models were most strongly supported by the data. Overall, this study suggests that primates may use a variety of biomechanical strategies to achieve hind limb dominance in limb force distribution.     

Apparent density patterns in subchondral bone of the sloth and anteater forelimb

Vertebrate morphologists often are interested in inferring limb-loading patterns in animals characterized by different locomotor repertoires. Because bone apparent density (i.e. mass per unit volume of bone inclusive of porosities) is a determinant of compressive strength, and thus indicative of compressive loading, recent comparative studies in primates have proposed a structure-function relationship between apparent density of subchondral bone and locomotor behaviours that vary in compressive loading. If such patterns are found in other mammals, then these relationships would be strengthened further. Here, we examine the distal radius of suspensory sloths that generally load their forelimbs (FLs) in tension and of quadrupedal anteaters that generally load their FLs in compression. Computed tomography osteoabsorptiometry was used to visualize the patterns in subchondral apparent density. Suspensory sloths exhibit relatively smaller areas of high apparent density than quadrupedal anteaters. This locomotor-based pattern is analogous to the pattern observed in suspensory and quadrupedal primates. Similarity between xenarthran and primate trends suggests broad-scale applicability for analysing subchondral bone apparent density and supports the idea that bone functionally alters its material properties in response to locomotor behaviours.     

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.     

Energetic benefits and adaptations in mammalian limbs: Scale effects and selective pressures

Differences in limb size and shape are fundamental to mammalian morphological diversity; however, their relevance to locomotor costs has long been subject to debate. In particular, it remains unknown if scale effects in whole limb morphology could partially underlie decreasing mass‐specific locomotor costs with increasing limb length. Whole fore‐ and hindlimb inertial properties reflecting limb size and shape—moment of inertia (MOI), mass, mass distribution, and natural frequency—were regressed against limb length for 44 species of quadrupedal mammals. Limb mass, MOI, and center of mass position are negatively allometric, having a strong potential for lowering mass‐specific locomotor costs in large terrestrial mammals. Negative allometry of limb MOI results in a 40% reduction in MOI relative to isometry's prediction for our largest sampled taxa. However, fitting regression residuals to adaptive diversification models reveals that codiversification of limb mass, limb length, and body mass likely results from selection for differing locomotor modes of running, climbing, digging, and swimming. The observed allometric scaling does not result from selection for energetically beneficial whole limb morphology with increasing size. Instead, our data suggest that it is a consequence of differing morphological adaptations and body size distributions among quadrupedal mammals, highlighting the role of differing limb functions in mammalian evolution.