Three-dimensional kinematics of capuchin monkey bipedalism

Capuchin monkeys are known to use bipedalism when transporting food items and tools. The bipedal gait of two capuchin monkeys in the laboratory was studied with three-dimensional kinematics. Capuchins progress bipedally with a bent-hip, bent-knee gait. The knee collapses into flexion during stance and the hip drops in height. The knee is also highly flexed during swing to allow the foot which is plantarflexed to clear the ground. The forefoot makes first contact at touchdown. Stride frequency is high, and stride length and limb excursion low. Hind limb retraction is limited, presumably to reduce the pitch moment of the forward-leaning trunk. Unlike human bipedalism, the bipedal gait of capuchins is not a vaulting gait, and energy recovery from pendulum-like exchanges is unlikely. It extends into speeds at which humans and other animals run, but without a human-like gait transition. In this respect it resembles avian bipedal gaits. It remains to be tested whether energy is recovered through cyclic elastic storage and release as in bipedal birds at higher speeds. Capuchin bipedalism has many features in common with the facultative bipedalism of other primates which is further evidence for restrictions on a fully upright striding gait in primates that transition to bipedalism. It differs from the facultative bipedalism of other primates in the lack of an extended double-support phase and short aerial phases at higher speeds that make it a run by kinematic definition. This demonstrates that facultative bipedalism of quadrupedal primates need not necessarily be a walking gait.     

Forward dynamic simulation of bipedal walking in the Japanese macaque: investigation of causal relationships among limb kinematics, speed, and energetics of bipedal locomotion in a nonhuman primate

Japanese macaques that have been trained for monkey performances exhibit a remarkable ability to walk bipedally. In this study, we dynamically reconstructed bipedal walking of the Japanese macaque to investigate causal relationships among limb kinematics, speed, and energetics, with a view to understanding the mechanisms underlying the evolution of human bipedalism. We constructed a two-dimensional macaque musculoskeletal model consisting of nine rigid links and eight principal muscles. To generate locomotion, we used a trajectory-tracking control law, the reference trajectories of which were obtained experimentally. Using this framework, we evaluated the effects of changes in cycle duration and gait kinematics on locomotor efficiency. The energetic cost of locomotion was estimated based on the calculation of mechanical energy generated by muscles. Our results demonstrated that the mass-specific metabolic cost of transport decreased as speed increased in bipedal walking of the Japanese macaque. Furthermore, the cost of transport in bipedal walking was reduced when vertical displacement of the hip joint was virtually modified in the simulation to be more humanlike. Human vertical fluctuations in the body's center of mass actually contributed to energy savings via an inverted pendulum mechanism.     

Speed modulation in hylobatid bipedalism: a kinematic analysis

Gibbons are highly arboreal apes, and it is expected that their bipedal locomotion will show some particularities related to the arboreal environment. Previous research has shown that, during hylobatid bipedalism, unsupported phases are rare and stride frequencies are relatively low. This study confirms previous findings, and we suggest that low stride frequencies and the absence of unsupported phases are ways to reduce disadvantageous branch oscillations during arboreal travel. Despite these restrictions, gibbons are able to locomote at a wide range of speeds, implying that they likely exploit other mechanisms to modulate their locomotor speed. To investigate this possibility, we collected video images of a large number of spontaneous bipedal bouts of four untrained white-handed gibbons by using an instrumented walkway with four synchronized cameras. These video images were digitized to obtain a quantification of the 3D kinematics of hylobatid bipedalism. We defined a large number of spatiotemporal and kinematic gait variables, and the relationship between these gait variables and (dimensionless) speed was statistically tested. It was found that gibbons mainly increase stride length to increase their locomotor speed; the main speed-modulating mechanisms are hip and ankle excursion and coupled knee and ankle extension at toe-off. Although aerial phases are rare, gibbons generally adopt a bipedal bouncing gait at most speeds and a clear-cut gait transition, as seen in human locomotion, is absent. Comparison with human and bonobo bipedalism showed that the variability of the 3D joint angles of the hind limb are comparable during human and gibbon bipedalism, and much lower than during bonobo bipedalism. The low variability found in gibbons might be related to constraints imposed by the arboreal environment. These arboreal constraints clearly affect the bipedal gait characteristics of gibbons, but do not constrain the ability to adopt a bipedal bouncing gait during terrestrial locomotion.     

Center of mass mechanics of chimpanzee bipedal walking

Center of mass (CoM) oscillations were documented for 81 bipedal walking strides of three chimpanzees. Full‐stride ground reaction forces were recorded as well as kinematic data to synchronize force to gait events and to determine speed. Despite being a bent‐hip, bent‐knee (BHBK) gait, chimpanzee walking uses pendulum‐like motion with vertical oscillations of the CoM that are similar in pattern and relative magnitude to those of humans. Maximum height is achieved during single support and minimum height during double support. The mediolateral oscillations of the CoM are more pronounced relative to stature than in human walking when compared at the same Froude speed. Despite the pendular nature of chimpanzee bipedalism, energy recoveries from exchanges of kinetic and potential energies are low on average and highly variable. This variability is probably related to the poor phasic coordination of energy fluctuations in these facultatively bipedal animals. The work on the CoM per unit mass and distance (mechanical cost of transport) is higher than that in humans, but lower than that in bipedally walking monkeys and gibbons. The pronounced side sway is not passive, but constitutes 10% of the total work of lifting and accelerating the CoM. CoM oscillations of bipedally walking chimpanzees are distinctly different from those of BHBK gait of humans with a flat trajectory, but this is often described as “chimpanzee‐like” walking. Human BHBK gait is a poor model for chimpanzee bipedal walking and offers limited insights for reconstructing early hominin gait evolution. Am J Phys Anthropol 156:422–433, 2015. © 2014 Wiley Periodicals, Inc.     

Do highly trained monkeys walk like humans? A kinematic study of bipedal locomotion in bipedally trained Japanese macaques

In this study, we examined the kinematics of bipedal walking in macaque monkeys that have been highly trained to stand and walk bipedally, and compared them to the kinematics of bipedal walking in ordinary macaques. The results revealed that the trained macaques walked with longer and less frequent strides than ordinary subjects. In addition, they appear to have used inverted pendulum mechanics during bipedal walking, which resulted in an efficient exchange of potential and kinetic energy. These gait characteristics resulted from the relatively more extended hindlimb joints of the trained macaques. By contrast, the body of the ordinary macaques translated downward during the single-limb stance phase due to more flexed hindlimb joints. This resulted in almost in-phase fluctuations of potential and kinetic energy, which indicated that energy transformation was less efficient in the ordinary macaques. The findings provide two insights into the early stage of the evolution of human bipedalism. First, the finding that training considerably improved bipedal walking a posteriori may explain why the very first bipeds that might not yet have been morphologically adapted to bipedal walking continued to walk bipedally. The evolutionary transition from quadrupedalism to bipedalism might not be as difficult as has been envisioned. In addition, the finding that macaques, which are phylogenetically distant from humans and in which bipedal walking is unlike human walking, could develop humanlike gait characteristics with training, provides strong support for the commonly held but unproven idea that the characteristics of the human gait are advantageous to human bipedalism.     

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.     

Positional behavior and substrate use in wild adult bearded capuchin monkeys (Sapajus libidinosus)

Natural selection for positional behavior (posture and locomotion) has at least partially driven the evolution of anatomical form and function in the order Primates. Examination of bipedal behaviors associated with daily activity patterns, foraging, and terrestrial habitat use in nonhuman primates, particularly those that adopt bipedal postures and use bipedal locomotion, allows us to refine hypotheses concerning the evolution of bipedalism in humans. This study describes the positional behavior of wild bearded capuchins (Sapajus libidinosus), a species that is known for its use of terrestrial substrates and its habitual use of stones as tools. Here, we test the association of terrestrial substrate use with bipedal posture and locomotion, and the influence of sex (which co‐varies with body mass in adults of this species) on positional behavior and substrate use. Behavior and location of 16 wild adult bearded capuchins from two groups were sampled systematically at 15 s intervals for 2 min periods for 1 year (10,244 samples). Despite their different body masses, adult males (average 3.5 kg) and females (average 2.1 kg) in this study did not differ substantially in their positional behaviors, postures, or use of substrates for particular activities. The monkeys used terrestrial substrates in 27% of samples. Bipedal postures and behaviors, while not a prominent feature of their behavior, occurred in different forms on the two substrates. The monkeys crouched bipedally in trees, but did not use other bipedal postures in trees. While on terrestrial substrates, they also crouched bipedally but occasionally stood upright and moved bipedally with orthograde posture. Bearded capuchin monkeys' behavior supports the suggestion from anatomical analysis that S. libidinosus is morphologically better adapted than its congeners to adopt orthograde postures.     

Genetic assimilation in the evolution of bipedalism

The evolution of the bipedal habit and its attendant anatomical specializations constitute the hallmark of our taxonomic family, but aside from numerous adaptive (ultimate cause) scenarios, no discussion of a genetic proximate cause can be found in the literature. On the surface, the evolution of obligate bipedalism involves the inheritance of an acquired character, since the descendants of facultative bipeds who chose to walk bipedally are hypothesized to have become obligate bipeds. This paper attempts to explain the Lamarckian origin of human bipedalism in a neo-Darwinian manner, by recourse to the adaptability of organisms, and the concept of genetic assimilation.     

Chimpanzee bipedal locomotion in the Gombe National Park,East Africa

An adult male chimpanzee in the natural habitat has been observed to walk predominantly bipedally after a total forelimb paralysis in 1966. The major differences from previously described bipedal chimpanzee gait are (1) one third of the femoral extension is posterior to the hip joint in propulsion, (2) excursion of the swinging foot is close to midline, due to adduction of the lower hindlimb in swing and propulsive phases, (3) depressed pelvic tilt is on the side of the swinging limb, (4) thoracic vertebrae rotate and are vertical and erect, and (5) there is only a moderate lateral sway of the midline. This locomotory complex is interpreted as individual variability and suggests an evolutionary model for the origin of hominid bipedal locomotion.     

Foramen magnum position in bipedal mammals

The anterior position of the human foramen magnum is often explained as an adaptation for maintaining balance of the head atop the cervical vertebral column during bipedalism and the assumption of orthograde trunk postures. Accordingly, the relative placement of the foramen magnum on the basicranium has been used to infer bipedal locomotion and hominin status for a number of Mio-Pliocene fossil taxa. Nonetheless, previous studies have struggled to validate the functional link between foramen magnum position and bipedal locomotion. Here, we test the hypothesis that an anteriorly positioned foramen magnum is related to bipedalism through a comparison of basicranial anatomy between bipeds and quadrupeds from three mammalian clades: marsupials, rodents and primates. Additionally, we examine whether strepsirrhine primates that habitually assume orthograde trunk postures exhibit more anteriorly positioned foramina magna compared with non-orthograde strepsirrhines. Our comparative data reveal that bipedal marsupials and rodents have foramina magna that are more anteriorly located than those of quadrupedal close relatives. The foramen magnum is also situated more anteriorly in orthograde strepsirrhines than in pronograde or antipronograde strepsirrhines. Among the primates sampled, humans exhibit the most anteriorly positioned foramina magna. The results of this analysis support the utility of foramen magnum position as an indicator of bipedal locomotion in fossil hominins.     

Functional morphology of the lemuriform wrist joints and the relationship between wrist morphology and positional behavior in arboreal primates

A comparative study of carpal joint structure and function in six Malagasy lemuriforms was undertaken to test predicted morphoclines in carpal joint morphology between pronograde and orthograde arboreal primates. Patterns of movement at the wrist during locomotion were observed and described for the lemuriform species Lemur fulvus and Propithecus verreauxi. Lemur fulvus, which assumes a pronograde posture during locomotion, extends and pronates the wrist during the support phase of quadrupedal walking and running stride cycles. Furthermore, the forearm of this species exhibits some transverse movement across the proximal wrist joint during the support phase. In contrast, the indriid Propithecus maintains the hand and wrist in a flexed and partially supinated position during vertical clinging and suspensory postures. Habitual quadrupedal and vertical postures in Malagasy primates are in turn related to very different patterns of carpal joint morphology and articular mechanics. Those lemurs which are predominantly pronograde share a series of structural features related to stabilizing the antebrachiocarpal joint during extension and mediolateral deviation and the midcarpal joint during pronation: an intraarticular labrum is present on the inner portion of the radiocarpal ligament, the radiocarpal articular surface is quite flat dorsoventrally, the capitate-trapezoid embrasure is expanded dorsally, and development of the radial and ulnar styloids is more pronounced. The wrists of Propithecus, Avahi, and Lepilemur (vertical clingers) differ from those of quadrupedal lemuriforms in possessing a suite of morphological features related to stabilizing the wrist during antebrachiocarpal flexion and midcarpal supination: the radiocarpal articular surface is deeply curved and tilted anteriorly, the dorsal radiocarpal ligament is very broad, thick, and fibrous, the hamate's triquetral facet is directed proximodistally, and the capitate-trapezoid embrasure is dorsally constricted and expanded palmarly. These observed contrasts in carpal form and function are used to define further the morphological features related to orthograde posture in several lineages of arboreal primates. © 1996 Wiley-Liss, Inc.     

Kinematic analysis of bipedal locomotion of a Japanese macaque that lost its forearms due to congenital malformation

Spontaneously acquired bipedal locomotion of an untrained Japanese monkey (Macaca fuscata) is measured and compared with the elaborated bipedal locomotion of highly trained monkeys to assess the natural ability of a quadrupedal primate to walk bipedally. The subject acquired bipedalism by himself because of the loss of his forearms and hands due to congenital malformation. Two other subjects are performing monkeys that have been extensively trained for bipedal posture and locomotion. We videotaped their bipedal locomotion with two cameras in a lateral view and calculated joint angles (hip, knee, and ankle) and inertial angle of the trunk from the digitized joint positions. The results show that all joints are relatively more flexed in the untrained monkey. Moreover, it is noted that the ankle is less plantar flexed and the knee is more flexed in mid-to-late stance phase in the untrained monkey, suggesting that the trunk is not lifted up to store potential energy. In the trained monkeys, the joints are extended to bring the trunk as high as possible in the stance phase, and then stored potential energy is exchanged for kinetic energy to move forward. The efficient inverted pendulum mechanism seems to be absent in the untrained monkeys locomotion, implying that acquisition of such efficient bipedal locomotion is not a spontaneous ability for a Japanese monkey. Rather, it is probably a special skill that can only be acquired through artificial training for an inherently quadrupedal primate.This revised version was published online in April 2005 with corrections to the cover date of the issue.     

Evolution of the hominoid vertebral column: The long and the short of it

The postcranial axial skeleton exhibits considerable morphological and functional diversity among living primates. Particularly striking are the derived features in hominoids that distinguish them from most other primates and mammals. In contrast to the primitive catarrhine morphotype, which presumably possessed an external (protruding) tail and emphasized more pronograde trunk posture, all living hominoids are characterized by the absence of an external tail and adaptations to orthograde trunk posture. Moreover, modern humans evolved unique vertebral features that satisfy the demands of balancing an upright torso over the hind limbs during habitual terrestrial bipedalism. Our ability to identify the evolutionary timing and understand the functional and phylogenetic significance of these fundamental changes in postcranial axial skeletal anatomy in the hominoid fossil record is key to reconstructing ancestral hominoid patterns and retracing the evolutionary pathways that led to living apes and modern humans. Here, we provide an overview of what is known about evolution of the hominoid vertebral column, focusing on the currently available anatomical evidence of three major transitions: tail loss and adaptations to orthograde posture and bipedal locomotion.     

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.     

Theories of bipedal walking: an odyssey

In this paper six theories of bipedal walking, and the evidence in support of the theories, are reviewed. They include: evolution, minimising energy consumption, maturation in children, central pattern generators, linking control and effect, and robots on two legs. Specifically, the six theories posit that: (1) bipedalism is the fundamental evolutionary adaptation that sets hominids--and therefore humans--apart from other primates; (2) locomotion is the translation of the centre of gravity along a pathway requiring the least expenditure of energy; (3) when a young child takes its first few halting steps, his or her biomechanical strategy is to minimise the risk of falling; (4) a dedicated network of interneurons in the spinal cord generates the rhythm and cyclic pattern of electromyographic signals that give rise to bipedal gait; (5) bipedal locomotion is generated through global entrainment of the neural system on the one hand, and the musculoskeletal system plus environment on the other; and (6) powered dynamic gait in a bipedal robot can be realised only through a strategy which is based on stability and real-time feedback control. The published record suggests that each of the theories has some measure of support. However, it is important to note that there are other important theories of locomotion which have not been covered in this review. Despite such omissions, this odyssey has explored the wide spectrum of bipedal walking, from its origins through to the integration of the nervous, muscular and skeletal systems.     

Ground reaction forces and center of mass mechanics of bipedal capuchin monkeys: Implications for the evolution of human bipedalism

Tufted capuchin monkeys are known to use both quadrupedalism and bipedalism in their natural environments. Although previous studies have investigated limb kinematics and metabolic costs, their ground reaction forces (GRFs) and center of mass (CoM) mechanics during two and four‐legged locomotion are unknown. Here, we determine the hind limb GRFs and CoM energy, work, and power during bipedalism and quadrupedalism over a range of speeds and gaits to investigate the effect of differential limb number on locomotor performance. Our results indicate that capuchin monkeys use a “grounded run” during bipedalism (0.83–1.43 ms^?1) and primarily ambling and galloping gaits during quadrupedalism (0.91–6.0 ms^?1). CoM energy recoveries are quite low during bipedalism (2–17%), and in general higher during quadrupedalism (4–72%). Consistent with this, hind limb vertical GRFs as well as CoM work, power, and collisional losses are higher in bipedalism than quadrupedalism. The positive CoM work is 2.04 ± 0.40 Jkg^?1 m^?1 (bipedalism) and 0.70 ± 0.29 Jkg^?1 m^?1 (quadrupedalism), which is within the range of published values for two and four‐legged terrestrial animals. The results of this study confirm that facultative bipedalism in capuchins and other nonhuman primates need not be restricted to a pendulum‐like walking gait, but rather can include running, albeit without an aerial phase. Based on these results and similar studies of other facultative bipeds, we suggest that important transitions in the evolution of hominin locomotor performance were the emergences of an obligate, pendulum‐like walking gait and a bouncy running gait that included a whole‐body aerial phase. Am J Phys Anthropol, 2013. © 2012 Wiley Periodicals, Inc.     

Effects of housing differences upon activity budgets in captive sifakas (Propithecus verreauxi)

Activity budgets of captive sifakas (Propithecus verreauxi coquereli and Propithecus verreauxi verreauxi) were assessed from 500 hours of observational data obtained at the Duke University Primate Center (Durham, NC). Data were examined for behavioral differences according to gender, availability of intergroup contact, subspecies, indoor/outdoor housing, and enclosure size. Results showed few differences between the activity budgets of males and females. Several differences found in conjunction with availability of intergroup contact appeared to relate more to subspecific, than to contact, differences. Sifakas housed outdoors were more active, spending less time resting and more time in locomotion, feeding, and playing than sifakas housed indoors. The findings of this study implicate outdoor housing as a primary factor in stimulating activity in these rare prosimian primates.