Arboreal bipedalism in wild chimpanzees: implications for the evolution of hominid posture and locomotion

Field observations of bipedal posture and locomotion in wild chimpanzees (Pan troglodytes) can serve as key evidence for reconstructing the likely origins of bipedalism in the last prehominid human ancestor. This paper reports on a sample of bipedal bouts, recorded ad libitum, in wild chimpanzees in Bwindi Impenetrable National Park in southwestern Uganda. The Ruhija community of chimpanzees in Bwindi displays a high rate of bipedal posture. In 246.7 hr of observation from 2001-2003, 179 instances of bipedal posture lasting 5 sec or longer were recorded, for a rate of 0.73 bouts per observation hour. Bipedalism was observed only on arboreal substrates, and was almost all postural, and not locomotor. Bipedalism was part of a complex series of positional behaviors related to feeding, which included two-legged standing, one-legged standing with arm support, and other intermediate postures. Ninety-six percent of bipedal bouts occurred in a foraging context, always as a chimpanzee reached to pluck fruit from tree limbs. Bipedalism was seen in both male and female adults, less frequently among juveniles, and rarely in infants. Both the frequency and duration of bipedal bouts showed a significant positive correlation with estimated substrate diameter. Neither fruit size nor nearest-neighbor association patterns were significantly correlated with the occurrence of bipedalism. Bipedalism is seen frequently in the Bwindi chimpanzee community, in part because of the unusual observer conditions at Bwindi. Most observations of bipedalism were made when the animals were in treetops and the observer at eye-level across narrow ravines. This suggests that wild chimpanzees may engage in bipedal behavior more often than is generally appreciated. Models of the likely evolutionary origins of bipedalism are considered in the light of Bwindi bipedalism data. Bipedalism among Bwindi chimpanzees suggests the origin of bipedal posture in hominids to be related to foraging advantages in fruit trees. It suggests important arboreal advantages in upright posture. The origin of postural bipedalism may have preceded and been causally disconnected from locomotor bipedalism.     

Bipedal behavior of olive baboons (Papio anubis) and its relevance to an understanding of the evolution of human bipedalism

The bipedal behavior of a troop of olive baboons (Papio anubis) is described. Bipedalism is relatively rare but nevertheless occurs in a wide variety of situations, although bipedalism during feeding occurs much more frequently than in other situations. The incidence of bipedalism varies between different age-sex classes and between individuals within age-sex classes. This pattern of bipedalism occurred within an overall adaptive response, particularly in feeding behavior, which was similar to that of the gelada baboon (Theropithecus gelada). The data on bipedalism is used together with an existing model of early hominid differentiation based on T. gelada to indicate the types of bipedal behavior which might have occurred in early hominid small object feeders and to suggest how a bipedal pattern of this type might have served as a basis for the action of selection for a more committedly bipedal pattern at later stages of hominid evolution.     

Brief communication: arboreal bipedalism in Bwindi chimpanzees

Evidence of the form and function of bipedal behavior in nonhuman primates provides critical evidence to test theories about the origins of hominid bipedalism. Bipedalism has long been considered an evolutionarily interesting but rare behavior in wild chimpanzees. During May 2001, chimpanzees of the Ruhija community in the Bwindi Impenetrable National Park, Uganda, engaged in an exceptional frequency of arboreal bipedalism when feeding in large Ficus trees. Seventy-eight bipedal bouts of at least 5 sec duration were recorded for the entire community (0.49 bouts/hr), with a mean duration of 13.7 sec (+/-1.6 sec). The animals employed many variations on the bipedal postural theme, ranging from erect standing on the largest substrates while grasping overhead limbs for support, to standing on one leg while suspending the other leg in space, to extended-lean standing, in which bipedal standing transitioned into horizontal arm-leg suspension as the animal reached for more distant fruits. Bipedalism was used as part of a behavioral repertoire that integrated brachiation, four-limbed suspension, and forelimb-supported standing for effective small-fruit foraging. These observations suggest that under certain ecological conditions, arboreal bipedalism can be an important posture for wild chimpanzees, and may have been an important behavioral precursor to full terrestrial bipedalism.     

Neural control of quadrupedal and bipedal stance: implications for the evolution of erect posture

The transition among hominids from quadrupedalism to bipedalism resulted in modifications in their musculoskeletal morphology. It is unclear, however, whether changes in the circuitry of the CNS were also necessary in order to accommodate the unique balance requirements of two-limb support. This study addresses the issue of modifications in control strategies by investigating the rapid, automatic postural responses of feline and human subjects to sudden disturbances of balance in the anteroposterior (AP) direction while they stand quadrupedally and bipedally on movable platforms. Postural responses are characterized in terms of segmental adjustments, generated AP shear forces, and electromyographic activity. Feline and human subjects correct posture similarly when standing quadrupedally. Furthermore, both species correct stance primarily with their hindlimbs and use their forelimbs as supportive struts. In contrast, both species use completely different correctional strategies when standing bipedally. Morphological restrictions, however, prevent cats from adopting the pillar-like plantigrade posture of human beings. Thus, the correctional strategies of bipedal cats are distinct from those of bipedal human subjects. It is concluded that 1) automatic postural response patterns of quadrupedal Felis and bipedal Homo reflect the different biomechanical characteristics of the initial postures rather than species differences in CNS circuitry controlling stance; 2) hindlimb-dominated posture control is probably a common and relatively ancient pattern; and 3) reorganization of hominid CNS circuitry was probably unnecessary because hindlimb control was already a feature of the system.     

Biomechanical interpretation of the early hominid hip

A new pelvic fragment from Swartkrans provides the opportunity to analyze the hip joint mechanics of the robust form of early hominid. The function of the lateral support system provided by the abductor muscles of the hip appears to be similar to that of the gracile early hominid from Sterkfontein. The system is well adapted for providing the lateral support necessary for efficient bipedalism. The hip extensor mechanism and hip internal rotatory system also appear to be well adapted for efficient bipedalism in a way very similar to the other early hominids. The conclusion reached is that the robust and gracile forms of South African early hominids were basically similar in their locomotor adaptation and were most likely habitual bipeds.     

Divergent patterns of integration and reduced constraint in the human hip and the origins of bipedalism

When compared to other hominids--great apes including humans--the human pelvis reveals a fundamental reorganization of bony morphology comprised of multiple trait-level changes, many of which are associated with bipedal locomotion. Establishing how patterns of integration--correlations and covariances among traits--within the pelvis have evolved in concert with morphology is essential to explaining this evolutionary transition because integration may facilitate or constrain morphological evolution. Here, we show that the human hip bone has significantly lower levels of integration and constraint overall when compared to other hominids, that the focus of these changes is on traits hypothesized to play major functional roles in bipedalism, and we provide evidence that the human hip was reintegrated in a pattern distinct from other members of this group. Additionally, the evolutionary transition from a nonhuman great ape-like to human hip bone morphology was significantly easier to traverse using the human integration pattern in each comparison, which suggests hominin patterns may have evolved to facilitate this transition. Our results suggest natural selection for bipedalism broke down earlier hominid integration patterns, allowing relevant traits to respond to separate selection pressures to a greater extent than was previously possible, and reintegrated traits in a way that could have facilitated evolution along the vector specifying ancestral hominid and hominin morphological differences.     

THE EVOLUTION OF BIPEDAL RUNNING IN LIZARDS SUGGESTS A CONSEQUENTIAL ORIGIN MAY BE EXPLOITED IN LATER LINEAGES

The origin of bipedal locomotion in lizards is unclear. Modeling studies have suggested that bipedalism may be an exaptation, a byproduct of features originally designed to increase maneuverability, which were only later exploited. Measurement of the body center of mass (BCOM) in 124 species of lizards confirms a significant rearward shift among bipedal lineages. Further racetrack trials showed a significant acceleration threshold between bipedal and quadrupedal runs. These suggest good general support for a passive bipedal model, in which the combination of these features lead to passive lifting of the front of the body. However, variation in morphology could only account for 56% of the variation in acceleration thresholds, suggesting that dynamics have a significant influence on bipedalism. Deviation from the passive bipedal model was compared with node age, supporting an increase in the influence of dynamics over time. Together, these results show that bipedalism may have first arisen as a consequence of acceleration and a rearward shift in the BCOM, but subsequent linages have exploited this consequence to become bipedal more often, suggesting that bipedalism in lizards may convey some advantage. Exploitation of bipedalism was also associated with increased rates of phenotypic diversity, suggesting exploiting bipedalism may promote adaptive radiation.     

Bipedal tool use strengthens chimpanzee hand preferences

The degree to which non-human primate behavior is lateralized, at either individual or population levels, remains controversial. We investigated the relationship between hand preference and posture during tool use in chimpanzees (Pan troglodytes) during bipedal tool use. We experimentally induced tool use in a supported bipedal posture, an unsupported bipedal posture, and a seated posture. Neither bipedal tool use nor these supported conditions have been previously evaluated in apes. The hypotheses tested were 1) bipedal posture will increase the strength of hand preference, and 2) a bipedal stance, without the use of one hand for support, will elicit a right hand preference. Results supported the first, but not the second hypothesis: bipedalism induced the subjects to become more lateralized, but not in any particular direction. Instead, it appears that subtle pre-existing lateral biases, to either the right or left, were emphasized with increasing postural demands. This result has interesting implications for theories of the evolution of tool use and bipedalism, as the combination of bipedalism and tool use may have helped drive extreme lateralization in modern humans, but cannot alone account for the preponderance of right-handedness.     

Locomotor energetics and hominid evolution

The presence of a bipedal gait in fossil apes is now recognized as the earliest paleontological evidence of the beginnings of the human lineage. Thus, the search for the selective pressure that led to the adoption of bipedal posture and gait is the search for the origins of the human adaptation. One of the most popular candidates for the origin of erect posture is its purported energetic advantage.^1–4 This argument is reevaluated in light of data on the energetic cost of locomotion in mammals and, particularly, data on the effect of bipedalism on cost. I go on to discuss what morphological traces we might expect to see of changes in the locomotor economy of our ancestors once bipedalism became established.     

The rise of the hominids as an adaptive shift in fallback foods: plant underground storage organs (USOs) and australopith origins

We propose that a key change in the evolution of hominids from the last common ancestor shared with chimpanzees was the substitution of plant underground storage organs (USOs) for herbaceous vegetation as fallback foods. Four kinds of evidence support this hypothesis: (1) dental and masticatory adaptations of hominids in comparison with the African apes; (2) changes in australopith dentition in the fossil record; (3) paleoecological evidence for the expansion of USO-rich habitats in the late Miocene; and (4) the co-occurrence of hominid fossils with root-eating rodents. We suggest that some of the patterning in the early hominid fossil record, such as the existence of gracile and robust australopiths, may be understood in reference to this adaptive shift in the use of fallback foods. Our hypothesis implicates fallback foods as a critical limiting factor with far-reaching evolutionary effects. This complements the more common focus on adaptations to preferred foods, such as fruit and meat, in hominid evolution.     

Footprint Clues in Hominid Evolution and Forensics: Lessons and Limitations

In 1978 and 1979 at Laetoli, Northern, Tanzania, Mary D. Leakey and assistants excavated the most compelling evidence for the existence of bipedalism in Pliocene (3.5 Ma) hominids. They have stimulated controversy over the extent to which the three individuals had feet and gaits that are like those of humans versus having ape-like features and gaits. A short trail of bipedal tracks discovered in 1977 at Laetoli site A are probably not those of a hominid and more closely resemble the prints of bears. One of the original researchers on the Laetoli prints claimed that she could identify individual modern humans from their footprints, partial footprints and shoe prints because each individual has distinctive foot morphology on a par with the individuality of fingerprints. Courts of law should not have allowed her unproven (and now discredited) method to be used forensically prior to thorough review by scientific peers.     

The distal femoral anatomy of Australopithecus

The anatomy of the distal femoral fragments from Sterkfontein is reviewed, including its orthopaedic and biomechanical implications with respect to locomotion pattern. Comparisons are made with other hominids and a number of quadrupedal primates. Items which are considered are the obliquity and robustness of the shaft, the anterior intercondylar groove, the intercondylar notch, and the contour of the medial and lateral articular surfaces. The distinctive hominid status of these specimens is shown by their extensive adaptation to bipedal locomotion. No feature is found which is not fully commensurate with completely bipedal locomotion; rather, their distinctive hominid character points to a need for a reanalysis of the gait pattern in these early Pleistocene hominids.     

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.     

The relative cost of bent-hip bent-knee walking is reduced in water

The debate about how early hominids walked may be characterised as two competing hypotheses: They moved with a fully upright (FU) gait, like modern humans, or with a bent-hip, bent-knee (BK) gait, like apes. Both have assumed that this bipedalism was almost exclusively on land, in trees or a combination of the two. Recent findings favoured the FU hypothesis by showing that the BK gait is 50–60% more energetically costly than a FU human gait on land. We confirm these findings but show that in water this cost differential is markedly reduced, especially in deeper water, at slower speeds and with greater knee flexion. These data suggest that the controversy about australopithecine locomotion may be eased if it is assumed that wading was a component of their locomotor repertoire and supports the idea that shallow water might have been an environment favourable to the evolution of early forms of “non-optimal” hominid bipedalism.     

From apes to humans: locomotion as a key feature for phylogeny

If bipedalism has often been considered to be of a crucial interest for understanding hominid evolution, the acceptance of locomotor features to build phylogenies is still far from being a reality in the field. Especially for hominid evolution, it still seems to be difficult to accept that traits, other than craniodental ones, can be useful for defining the major dichotomies. The recent discovery of Australopithecus anamensis suggests a challenging view of the major dichotomy between apes and humans. Whilst it is widely accepted that Ardipithecus ramidus is ancestral to Australopithecus anamensis, which in its turn is ancestral to Australopithecus afarensis and then to later hominids, the postcranial adaptations, which should be taken into account, suggest another branching pattern. Based on the fact that by 4.0 million years two different locomotor patterns can be identified in hominids, two lineages would appear to be present: the "Australopithecine" lineage (with Australopithecus afarensis or Ardipithecus ramidus if the latter is really a hominid sensu stricto) and the "Hominine" lineage (with Australopithecus anamensis = Praeanthropus africanus).     

Bipedality in chimpanzee (Pan troglodytes) and bonobo (Pan paniscus): testing hypotheses on the evolution of bipedalism

A host of ecological, anatomical, and physiological selective pressures are hypothesized to have played a role in the evolution of hominid bipedalism. A referential model, based on the chimpanzee (Pan troglodytes) and bonobo (Pan paniscus), was used to test through experimental manipulation four hypotheses on the evolution of hominid bipedalism. The introduction of food piles (Carry hypothesis) increased locomotor bipedality in both species. Neither the introduction of branches (Display hypothesis) nor the construction of visual barriers (Vigilance hypothesis) altered bipedality in either species. Introduction of raised foraging structures (Forage hypothesis) increased postural bipedality in chimpanzees. These experimental manipulations provided support for carrying of portable objects and foraging on elevated food-items as plausible mechanisms that shaped bipedalism in hominids.     

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 metabolic costs of 'bent-hip, bent-knee' walking in humans

The costs of different modes of bipedalism are a key issue in reconstructing the likely gait of early human ancestors such as Australopithecus afarensis. Some workers, on the basis of morphological differences between the locomotor skeleton of A. afarensis and modern humans, have proposed that this hominid would have walked in a 'bent-hip, bent-knee' (BHBK) posture like that seen in the voluntary bipedalism of untrained chimpanzees. Computer modelling studies using inverse dynamics indicate that on the basis of segment proportions AL-288-1 should have been capable of mechanically effective upright walking, but in contrast predicted that BHBK walking would have been highly ineffective. The measure most pertinent to natural selection, however, is more likely to be the complete, physiological, or metabolic energy cost. We cannot measure this parameter in a fossil. This paper presents the most complete investigation yet of the metabolic and thermoregulatory costs of BHBK walking in humans. Data show that metabolic costs including the basal metabolic rate (BMR) increase by around 50% while the energy costs of locomotion and blood lactate production nearly double, heat load is increased, and core temperature does not return to normal within 20 minutes rest. Net effects imply that a resting period of 150% activity time would be necessary to prevent physiologically intolerable heat load. Preliminary data for children suggest that scaling effects would not significantly reduce relative costs for hominids of AL-288-1's size. Data from recent studies using forwards dynamic modelling confirm that similar total (including BMR) and locomotor metabolic costs would have applied to BHBK walking by AL-288-1. We explore some of the ecological consequences of our findings.     

Kinematics of bipedalism in Propithecus verreauxi

Bipedalism is rare in primates and has evolved in two distantly related groups: hominoids and indrids. Although copious data are available on the mechanics of bipedal locomotion in hominoids and vertical clinging and leaping (VCL) in indrids, no research has addressed the unique mode of bipedal locomotion exhibited by select indrid primates. Propithecus verreauxi is a highly specialized indrid vertical clinger and leaper that uses a peculiar form of bipedalism on the ground. The objectives of this study were to describe the bipedal gait of Propithecus , to assess the influence of VCL specializations on the kinematic patterns and propulsion mechanisms used by Propithecus during bipedalism, and to compare Propithecus bipedalism with the bipedal gaits of other primates capable of using bipedalism. Video was collected of five adult P. verreauxi moving bipedally in a seminatural setting at the Duke University Primate Center. Duty factor, footfall patterns, joint angles and center of mass movement were quantified in the sagittal plane for 73 steps. Propithecus uses a bipedal gallop, a gait unique to Propithecus . The kinematic similarities (e.g. large hip and knee angular excursions and preparatory countermovements) between bipedal galloping and VCL lead us to suggest that Propithecus takes advantage of specializations for VCL to conserve energy during bipedal galloping. Propithecus also walks bipedally at slower speeds. When Propithecus walks, it utilizes a relatively compliant gait similar to that of other primate facultative bipeds ( Pan , Hylobates ). During bipedal walking, energy conservation may be sacrificed for increased balance and reduced joint loads.     

Palaeoenvironments and the origin of hominid bipedalism

Abstract

It has long been accepted that hominids emerged during the Pliocene in a savannah environment in which a terrestrial quadruped gradually developed bipedal adaptations. However, data from the Late Miocene (i.e. 7–7.5 Ma), including detailed palaeontological and biogeochemical studies, suggest that our earliest Upper Miocene ancestors inhabited well-wooded to forested environments where they could have spent a certain amount of time in the trees. A plausible type of ecosystem in which upright posture and bipedal locomotion could have emerged is represented by Miombo Woodland, in which vertical arboreal supports predominate and trees are separated from each other by gaps. Subsequently hominids dispersed into the Savannah as accomplished bipeds, but retained the ability to climb trees. This scenario is compatible with the postcranial anatomy of Australopithecus, including its femoral elongation, body proportions, manual precision grip (also present in 6-million-year-old Orrorin) and a non-prehensile hallux.