Segment and joint angles of hind limb during bipedal and quadrupedal walking of the bonobo (Pan paniscus)

We describe segment angles (trunk, thigh, shank, and foot) and joint angles (hip, knee, and ankle) for the hind limbs of bonobos walking bipedally ("bent-hip bent-knee walking," 17 sequences) and quadrupedally (33 sequences). Data were based on video recordings (50 Hz) of nine subjects in a lateral view, walking at voluntary speed. The major differences between bipedal and quadrupedal walking are found in the trunk, thigh, and hip angles. During bipedal walking, the trunk is approximately 33-41 degrees more erect than during quadrupedal locomotion, although it is considerably more bent forward than in normal human locomotion. Moreover, during bipedal walking, the hip has a smaller range of motion (by 12 degrees ) and is more extended (by 20-35 degrees ) than during quadrupedal walking. In general, angle profiles in bonobos are much more variable than in humans. Intralimb phase relationships of subsequent joint angles show that hip-knee coordination is similar for bipedal and quadrupedal walking, and resembles the human pattern. The coordination between knee and ankle differs much more from the human pattern. Based on joint angles observed throughout stance phase and on the estimation of functional leg length, an efficient inverted pendulum mechanism is not expected in bonobos.     

Variations in blood supply allocations for quadrupedal and for bipedal posture and locomotion

Hemodynamics and orthodynamics were investigated in quadrupeds (dogs) and in bipeds (humans). The subjects were investigated at rest in supine or lateral posture, in quadrupedal and then in bipedal posture, and during locomotion. Quadrupedalism in humans was with subjects on their hands and knees. Bipedalism in dogs was on hindlimbs with the forelimbs held by a technician. Blood flow in the main arteries of the body (aorta, external and internal carotid, subclavian, and femoral) was measured by sonography. Positional variations between the main bones of the body were determined from X-rays. This study investigated the reallocation of blood supply to different regions of the body when it switches from quadrupedal to bipedal posture and locomotion. Compared with resting posture, the principal findings are 1) cardiac output shows a minimal increase for humans in bipedal stance and a noticeable increase for dogs as well as humans in quadrupedal stance; 2) quadrupedal stance in humans and dogs and bipedal stance in dogs require increased blood supply to the muscles of the neck, back, and limbs, while human bipedal stance requires none of these; 3) cerebral blood flow (internal carotid) in humans did not change as a result of bipedal posture or locomotion, but showed a noticeable drop in quadrupedal posture and an even further drop in quadrupedal locomotion. The conclusion is that erect posture and encephalization produced a noticeable readjustment and reallocation of blood flow among the different regions of the body: This consisted in shifting a large volume of blood supply from the musculature to the human brain.     

Limb morphology,bipedal gait,and the energetics of hominid locomotion

How viable is the argument that increased locomotor efficiency was an important agent in the origin of hominid bipedalism? This study reviews data from the literature on the cost of human bipedal walking and running and compares it to data on quadrupedal mammals including several non-human primate species. Literature data comparing the cost of bipedal and quadrupedal locomotion in trained capuchin monkeys and chimpanzees are also considered. It is concluded that increased energetic efficiency would not have accrued to early bipeds. Presumably, however, selection for improved efficiency in the bipedal stance would have occurred once the transition was made. Would such a process have included selection for increased limb length? Data on the cost of locomotion vs. limb length reveal no significant relationship between these variables in 21 species of mammals or in human walking or running. © 1996 Wiley-Liss, Inc.     

Spatio-temporal gait characteristics of the hind-limb cycles during voluntary bipedal and quadrupedal walking in bonobos (Pan paniscus)

Spatio-temporal gait characteristics (step and stride length, stride frequency, duty factor) were determined for the hind-limb cycles of nine bonobos (Pan paniscus) walking quadrupedally and bipedally at a range of speeds. The data were recalculated to dimensionless quantities according to the principle of dynamic similarity. Lower leg length was used as the reference length. Interindividual variability in speed modulation strategy of bonobos appears to be low. Compared to quadrupedal walking, bipedal bonobos use smaller steps to attain a given speed (differences increase with speed), resulting in shorter strides at a higher frequency. In the context of the ("hybrid") dynamic pattern approach to locomotion (Latach, 1998) we argue that, despite these absolute differences, intended walking speed is the basic control variable which elicits both quadrupedal and bipedal walking kinematics in a similar way. Differences in the initial status of the dynamic system may be responsible for the differences in step length between both gaits. Comparison with data deduced from the literature shows that the effects of walking speed on stride length and frequency are similar in bonobos, common chimpanzees, and humans. This suggests that (at least) within extant homininae, spatio-temporal gait characteristics are highly comparable, and this in spite of obvious differences in mass distribution and bipedal posture.     

Dynamic plantar pressure distribution during terrestrial locomotion of bonobos (Pan paniscus)

We collected high-resolution plantar pressure distributions of seven bonobos during terrestrial bipedal and quadrupedal locomotion (N = 146). Functional foot length, degree of hallux abduction, and total contact time were determined, and plots, showing pressure as a function of time for six different foot regions, were generated. We also studied five adult humans for comparison (N = 13). Both locomotion types of the bonobo show a large variation in plantar pressure distributions, which could be due to the interference of instantaneous behavior with locomotion and differences in walking speed and body dimensions. The heel and the lateral midfoot typically touch down simultaneously at initial ground contact in bipedal and quadrupedal walking of bonobos, in contrast with the typical heel-strike of human bipedalism. The center of pressure follows a curved course during quadrupedalism, as a consequence of the medial weight transfer during mid-stance. Bipedal locomotion of bonobos is characterized by a more plantar positioning of the feet and by a shorter contact time than during quadrupedal walking, according to a smaller stride and step length at a higher frequency. We observed a varus position of the foot with an abducted hallux, which likely possesses an important sustaining and stabilizing function during terrestrial locomotion.     

Development of chimpanzee locomotion on level surfaces

The objective of this study was to investigate kinesiologically the development of the unique characteristics of the level locomotion of the chimpanzee. The data were obtained semi-longitudinally from six chimpanzees eleven weeks through nineteen years of age. The posture, footfall order, phase duration, speed and foot force (including the hand force) in level locomotion were observed by means of foot contact switches, a 16 mm cine-camera or a video tape recorder and a force plate. The speed or the pattern of locomotion was not particularly controlled. The infants moved freely without any attachments on the body. The age change in locomotion is described. The particular characteristics of the infant chimpanzees compared with those of the adults were: 1) long stance phase duration, 2) wide variety in the difference in the cycle duration between forward movement of the limbs one after another, 3) wide variety in phase duration, speed and foot force, and 4) the forelimbs of the infant just started to stand quadrupedally to carry the larger part of the body weight than the hindlimbs. The dominance of the hindlimbs in locomotor and weight-bearing characteristics becomes clearly fixed at about one year of age. The wide variety of the locomotion pattern will be one of the characteristics of the chimpanzees of all age groups. The human acquisition of bipedal walking is discussed in connection with chimpanzee locomotion.     

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.     

First evidence on foot preference during locomotion in Old World monkeys: a study of quadrupedal and bipedal actions in Sichuan snub-nosed monkeys (Rhinopithecus roxellana)

This is the first report of foot preference during locomotion in Old World monkeys. Foot preferences during the quadrupedal walking action and the bipedal shifting action of a naturalistic group of Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in Zhouzhi National Nature Reserve in the Qinling Mountains of China were investigated. Twelve of 21 individuals tested on quadrupedal action and all 21 individuals tested on bipedal action exhibited a significant foot preference. Both significant right- and left-footed preferences were observed; sex affected neither direction nor strength of foot preference in both actions. The finding that 61.90% of focal R. roxellana showed a right-foot preference, both in quadrupedal action based on the footed index and in bipedal action based on the z-score, is in partial agreement with the postural origin hypothesis on footedness. Foot preference was significantly stronger in bipedal action than in quadrupedal action, supporting the view that posture could be a crucial factor influencing foot preference as well as hand preference in this species.     

Form in the context of function: Fundamentals of an energy effective striding walk,the role of the plantigrade foot and its expected size

What morphological and functional factors allow for the unique and characteristic upright striding walk of the hominin lineage? Predictive models of locomotion that arise from considering mechanisms of energy loss indicate that collision-like losses at the transition between stance limbs are important determinants of bipedal gait. Theoretical predictions argue that these collisional losses can be reduced by having “functional extra legs” which are physically the heel and the toe part of a single anatomical foot. The ideal spacing for these “functional legs” are up to a quarter of a stride length, depending on the model employed. We evaluate the foot in the context of the dynamics of a bipedal system and compare predictions of optimal foot size against empirical data from modern humans, the Laetoli footprint trackways, and chimpanzees walking bipedally. The dynamics-based modeling approach provides substantial insight into how, and why, walking works as it does, even though current models are too simple to make predictions at a level adequate to anticipate specific morphology except at the most general level.     

Ground-reaction-force profiles of bipedal walking in bipedally trained Japanese monkeys

Ground-reaction-force (GRF) profiles of bipedal locomotion in bipedally trained Japanese macaques (performing monkeys) were analyzed in order to clarify the dynamic characteristics of their locomotion. Five trained and two ordinary monkeys participated in the experiment. They walked on a wooden walkway at a self-selected speed, and three components of the GRF vector were measured using a force platform. Our measurements reveal that trained monkeys exhibited vertical-GRF profiles that were single-peaked, similar to those of ordinary monkeys; they did not generate the double-peaked force curve that is seen in humans, despite their extensive training. However, in the trained monkeys, the peak appeared relatively earlier in the stance phase, and overall shape was more triangular than that of the more parabolic profile generated by ordinary monkeys. Comparisons of vertical fluctuation of the center of body mass calculated from the measured profiles suggest that this was larger in the trained monkeys, indicating that storage and release of potential energy actually took place in their bipedal walking. This energetic advantage seems limited, however, because efficient exchange of potential and kinetic energy during walking were not completely out of phase as in human walking. We suggest that anatomically restricted range of hip-joint motion impedes the inherently quadrupedal monkeys from generating humanlike bipedal locomotion, and that morphological rearrangement of the hip joint was an essential precondition for protohominids to acquire humanlike bipedalism.     

Bioenergetics and the origin of hominid bipedalism

Compared to most quadrupedal mammals, humans are energetically inefficient when running at high speeds. This fact can be taken to mean that human bipedalism evolved for reasons other than to reduce relative energy cost during locomotion. Recalculation of the energy expended during human walking at normal speeds shows that (1) human bipedalism is at least as efficient as typical mammalian quadrupedalism and (2) human gait is much more efficient than bipedal or quadrupedal locomotion in the chimpanzee. We conclude that bipedalism bestowed an energetic advantage on the Miocene hominoid ancestors of the Hominidae.     

Compliant bipedal model with the center of pressure excursion associated with oscillatory behavior of the center of mass reproduces the human gait dynamics

Although the compliant bipedal model could reproduce qualitative ground reaction force (GRF) of human walking, the model with a fixed pivot showed overestimations in stance leg rotation and the ratio of horizontal to vertical GRF. The human walking data showed a continuous forward progression of the center of pressure (CoP) during the stance phase and the suspension of the CoP near the forefoot before the onset of step transition. To better describe human gait dynamics with a minimal expense of model complexity, we proposed a compliant bipedal model with the accelerated pivot which associated the CoP excursion with the oscillatory behavior of the center of mass (CoM) with the existing simulation parameter and leg stiffness. Owing to the pivot acceleration defined to emulate human CoP profile, the arrival of the CoP at the limit of the stance foot over the single stance duration initiated the step-to-step transition. The proposed model showed an improved match of walking data. As the forward motion of CoM during single stance was partly accounted by forward pivot translation, the previously overestimated rotation of the stance leg was reduced and the corresponding horizontal GRF became closer to human data. The walking solutions of the model ranged over higher speed ranges (~1.7 m/s) than those of the fixed pivoted compliant bipedal model (~1.5 m/s) and exhibited other gait parameters, such as touchdown angle, step length and step frequency, comparable to the experimental observations. The good matches between the model and experimental GRF data imply that the continuous pivot acceleration associated with CoM oscillatory behavior could serve as a useful framework of bipedal model.     

Effect of posture and locomotion on energy expenditure

Energy expenditure for human adults and infants and for dogs was measured in resting (supine or lateral) posture, in bipedal posture and locomotion, and in quadrupedal posture and locomotion. Variations in respiratory and heart rate and in body temperature were utilized in this comparative study. Oxygen consumption was also measured in human adults. In human adults, bipedal posture and locomotion were shown to be much less energy-consuming than corresponding quadrupedal posture and locomotion. The opposite was observed in adult dogs, where bipedalism was shown to be much more energy-consuming than quadrupedalism. In addition, this study demonstrated, for human adults in their natural erect posture, an energy expenditure barely higher than in supine or lateral resting posture, while the dogs in their natural quadrupedal stance, the energy expenditure is much higher than in their resting posture. With respect to energy, therefore, humans are more adapted to bipedalism than dogs to quadrupedalism. Human children, at the transitional stage between quadrupedalism and bipedalism, have high and almost equal requirements for all postures and locomotions. This demonstrates, in term of energy, their incomplete adaptation to erect behavior.     

The advantage of standing up to fight and the evolution of habitual bipedalism in hominins

Background

Many quadrupedal species stand bipedally on their hindlimbs to fight. This posture may provide a performance advantage by allowing the forelimbs to strike an opponent with the range of motion that is intrinsic to high-speed running, jumping, rapid braking and turning; the range of motion over which peak force and power can be produced.

Methodology/Principal Findings

To test the hypothesis that bipedal (i.e., orthograde) posture provides a performance advantage when striking with the forelimbs, I measured the force and energy produced when human subjects struck from “quadrupedal” (i.e., pronograde) and bipedal postures. Downward and upward directed striking energy was measured with a custom designed pendulum transducer. Side and forward strikes were measured with a punching bag instrumented with an accelerometer. When subjects struck downward from a bipedal posture the work was 43.70±12.59% (mean ± S.E.) greater than when they struck from a quadrupedal posture. Similarly, 47.49±17.95% more work was produced when subjects struck upward from a bipedal stance compared to a quadrupedal stance. Importantly, subjects did 229.69±44.19% more work in downward than upward directed strikes. During side and forward strikes the force impulses were 30.12±3.68 and 43.04±9.00% greater from a bipedal posture than a quadrupedal posture, respectively.

Conclusions/Significance

These results indicate that bipedal posture does provide a performance advantage for striking with the forelimbs. The mating systems of great apes are characterized by intense male-male competition in which conflict is resolved through force or the threat of force. Great apes often fight from bipedal posture, striking with both the fore- and hindlimbs. These observations, plus the findings of this study, suggest that sexual selection contributed to the evolution of habitual bipedalism in hominins.     

A bipedal compliant walking model generates periodic gait cycles with realistic swing dynamics

A simple spring mechanics model can capture the dynamics of the center of mass (CoM) during human walking, which is coordinated by multiple joints. This simple spring model, however, only describes the CoM during the stance phase, and the mechanics involved in the bipedality of the human gait are limited. In this study, a bipedal spring walking model was proposed to demonstrate the dynamics of bipedal walking, including swing dynamics followed by the step-to-step transition. The model consists of two springs with different stiffnesses and rest lengths representing the stance leg and swing leg. One end of each spring has a foot mass, and the other end is attached to the body mass. To induce a forward swing that matches the gait phase, a torsional hip joint spring was introduced at each leg. To reflect the active knee flexion for foot clearance, the rest length of the swing leg was set shorter than that of the stance leg, generating a discrete elastic restoring force. The number of model parameters was reduced by introducing dependencies among stiffness parameters. The proposed model generates periodic gaits with dynamics-driven step-to-step transitions and realistic swing dynamics. While preserving the mimicry of the CoM and ground reaction force (GRF) data at various gait speeds, the proposed model emulated the kinematics of the swing leg. This result implies that the dynamics of human walking generated by the actuations of multiple body segments is describable by a simple spring mechanics.     

Cross-Sectional Morphology of the Femoral Neck of Wild Chimpanzees

To understand the mechanical effects of different modes of locomotion on the femoral neck of chimpanzees, we investigated the cross-sectional morphology of the femoral neck of 4 chimpanzees (Pan troglodytes schweinfurthii) collected from the Mahale Mountains, Tanzania. We performed serial computed tomography (CT) scans of the neck from the femoral head to the base of the neck perpendicular to the long axis of the neck. We measured the cortical thickness of the serial 5 cross sections of the neck region every 45° around the circumference, i.e., 8 points per section, and examined the cross-sectional properties of the mid-section. When we compared the superior and inferior parts of the cortical thickness of the femoral neck, the inferior part exhibited the greatest cortical thickness whereas the superior part had the smallest values in every specimen. Researchers have also observed such regional differences between superior and inferior cortical thicknesses in bipedal humans and other primates, although these differences are not as large in the chimpanzee as in bipedal hominini. The present study differed from the past study on hominini and chimpanzees in that the superior anterior (SA) part exhibited greater cortical thickness in chimpanzees. We believe these observations reflect the structural strengthening of parts of the chimpanzee femoral neck that is needed to accommodate the mechanical loads imposed by arboreal vertical climbing and terrestrial quadrupedal and bipedal locomotion.     

Optimum walking techniques for quadrupeds and bipeds

A new theory is presented which describes quadrupedal as well as bipedal walking. It avoids errors which occurred in previous theories by evaluating separately the work done by each leg instead of deriving net work from mechanical energy fluctuations. It takes particular account of two parameters, the duty factor β (the fraction of the stride for which each foot is on the ground) and a parameter q which defines the time course of the force on each foot. It shows that for any given speed there is an optimum (β, q ) which minimizes the energy cost of locomotion. These (β, q ) are only a little different for bipeds and quadrupeds except near the critical speed at which the optimum moves abruptly from walking (high β) to running (low β). Walking men use (β, q ) close to the theoretical optima, but with slightly higher q. Walking dogs and sheep use q which are lower than the optimum values except at very low speeds. Some of the energy which would otherwise be required for locomotion may be saved by storage of elastic strain energy in tendons etc. This mechanism is more effective in running than in fast walking, which may be why men change from walking to running at lower speeds than the inelastic theory suggests.     

Optimum walking techniques for idealized animals

The vertical component of the force exerted by a foot on the ground, in the course of a step, may rise to a single maximum and decline again (as in human running) or may show two distinct maxima (as in human walking). A foot may remain on the ground for a large or small fraction of the duration of a stride. Mathematical models are used to investigate the effects of these differences of technique on the energy cost of locomotion. The optimum technique for a biped at a given speed is different from the optimum for a hypothetical many-legged animal. The optima for quadrupedal walking are likely to lie between these extremes.
The walking techniques adopted by men at different speeds are close to the optima indicated by the bipedal model. The two maxima of the force exerted by a foot are higher, and have a lower minimum between them, at higher speeds of walking. The techniques adopted by a sheep are close to the optima indicated by the many-legged model but dogs use techniques rather closer to the optima for bipeds.
The limitations of the models are discussed.     

Energetic costs of bipedal and quadrupedal walking in Japanese macaques

We investigated the energetic costs of quadrupedal and bipedal walking in two Japanese macaques. The subjects were engaged in traditional bipedal performance for years, and are extremely adept bipeds. The experiment was conducted in an airtight chamber with a gas analyzer. The subjects walked quadrupedally and bipedally at fixed velocities (<5 km/hr) on a treadmill in the chamber for 2.5-6 min. We estimated energy consumption from carbon dioxide (CO2) production. While walking bipedally, energetic expenditure increased by 30% relative to quadrupedalism in one subject, and by 20% in another younger subject. Energetic costs increased linearly with velocity in quadrupedalism and bipedalism, with bipedal/quadrupedal ratios remaining almost constant. Our experiments were relatively short in duration, and thus the observed locomotor costs may include presteady-state high values. However, there was no difference in experimental duration between bipedal and quadrupedal trials. Thus, the issue of steady state cannot cancel the difference in energetic costs. Furthermore, we observed that switching of locomotor mode (quadrupedalism to bipedalism) during a session resulted in a significant increase of CO2 production. Taylor and Rowntree ([1973] Science 179:186-187) noted that the energetic costs for bipedal and quadrupedal walking were the same in chimpanzees and capuchin monkeys. Although the reason for this inconsistency is not clear, species-specific differences should be considered regarding bipedal locomotor energetics among nonhuman primates. Extra costs for bipedalism may not be great in these macaques. Indeed, it is known that suspensory locomotion in Ateles consumes 1.3-1.4 times as much energy relative to quadrupedal progression. This excess ratio surpasses the bipedal/quadrupedal energetic ratios in these macaques.