Susannah K. S. Thorpe

Origin of Human Bipedalism As an Adaptation for Locomotion on Flexible Branches

Human bipedalism is commonly thought to have evolved from a quadrupedal terrestrial precursor, yet some recent paleontological evidence suggests that adaptations for bipedalism arose in an arboreal context. However, the adaptive benefit of arboreal bipedalism has been unknown. Here we show that it allows the most arboreal great ape, the orangutan, to access supports too flexible to be negotiated otherwise. Orangutans react to branch flexibility like humans running on springy tracks, by increasing knee and hip extension, whereas all other primatesdothe reverse. Human bipedalism is thus less an innovation than an exploitation of a locomotor behavior retained from the common great ape ancestor.

Locomotion and posture from the common hominoid ancestor to fully modern hominins, with special reference to the last common panin/hominin ancestor

Based on our knowledge of locomotor biomechanics and ecology we predict the locomotion and posture of the last common ancestors of (a) great and lesser apes and their close fossil relatives (hominoids); (b) chimpanzees, bonobos and modern humans (hominines); and (c) modern humans and their fossil relatives (hominins). We evaluate our propositions against the fossil record in the context of a broader review of evolution of the locomotor system from the earliest hominoids of modern aspect (crown hominoids) to early modern Homo sapiens. While some early East African stem hominoids were pronograde, it appears that the adaptations which best characterize the crown hominoids are orthogrady and an ability to abduct the arm above the shoulder – rather than, as is often thought, manual suspension sensu stricto. At 7–9 Ma (not much earlier than the likely 4–8 Ma divergence date for panins and hominins, see Bradley, 2008 ) there were crown hominoids in southern Europe which were adapted to moving in an orthograde posture, supported primarily on the hindlimb, in an arboreal, and possibly for Oreopithecus, a terrestrial context. By 7 Ma, Sahelanthropus provides evidence of a Central African hominin, panin or possibly gorilline adapted to orthogrady, and both orthogrady and habitually highly extended postures of the hip are evident in the arboreal East African protohominin Orrorin at 6 Ma. If the traditional idea that hominins passed through a terrestrial ‘knuckle‐walking’ phase is correct, not only does it have to be explained how a quadrupedal gait typified by flexed postures of the hindlimb could have preadapted the body for the hominin acquisition of straight‐legged erect bipedality, but we would have to accept a transition from stem‐hominoid pronogrady to crown hominoid orthogrady, back again to pronogrady in the African apes and then back to orthogrady in hominins. Hand‐assisted arboreal bipedality, which is part of a continuum of orthograde behaviours, is used by modern orangutans to forage among the small branches at the periphery of trees where the core hominoid dietary resource, ripe fruit, is most often to be found. Derivation of habitual terrestrial bipedality from arboreal hand‐assisted bipedality requires fewer transitions, and is also kinematically and kinetically more parsimonious.

Orangutans use compliant branches to lower the energetic cost of locomotion

Within the forest canopy, the shortest gaps between tree crowns lie between slender terminal branches. While the compliance of these supports has previously been shown to increase the energetic cost of gap crossing in arboreal animals (e.g. Alexander 1991 Z. Morphol. Anthropol. 78, 315–320; Demes et al. 1995 Am. J. Phys. Anthropol. 96, 419–429), field observations suggest that some primates may be able to use support compliance to increase the energetic efficiency of locomotion. Here, we calculate the energetic cost of alternative methods of gap crossing in orangutans (Pongo abelii). Tree sway (in which orangutans oscillate a compliant tree trunk with increasing magnitude to bridge a gap) was found to be less than half as costly as jumping, and an order of magnitude less costly than descending the tree, walking to the vine and climbing it. Observations of wild orangutans suggest that they actually use support compliance in many aspects of their locomotor behaviour. This study seems to be the first to show that elastic compliance in arboreal supports can be used to reduce the energetic cost of gap crossing.

Arboreality, terrestriality and bipedalism

The full publication of Ardipithecus ramidus has particular importance for the origins of hominin bipedality, and strengthens the growing case for an arboreal origin. Palaeontological techniques however inevitably concentrate on details of fragmentary postcranial bones and can benefit from a whole-animal perspective. This can be provided by field studies of locomotor behaviour, which provide a real-world perspective of adaptive context, against which conclusions drawn from palaeontology and comparative osteology may be assessed and honed. Increasingly sophisticated dynamic modelling techniques, validated against experimental data for living animals, offer a different perspective where evolutionary and virtual ablation experiments, impossible for living mammals, may be run in silico, and these can analyse not only the interactions and behaviour of rigid segments but increasingly the effects of compliance, which are of crucial importance in guiding the evolution of an arboreally derived lineage.

Morphological analysis of the hindlimb in apes and humans. II. Moment arms

Flexion/extension moment arms were obtained for the major muscles crossing the hip, knee and ankle joints in the orang‐utan, gibbon, gorilla (Eastern and Western lowland) and bonobo. Moment arms varied with joint motion and were generally longer in proximal limb muscles than distal limb muscles. The shape of the moment arm curves (i.e. the plots of moment arm against joint angle) differed in different hindlimb muscles and in the same muscle in different subjects (both in the same and in different ape species). Most moment arms increased with increasing joint flexion, a finding which may be understood in the context of the employment of flexed postures by most non‐human apes (except orang‐utans) during both terrestrial and arboreal locomotion. When compared with humans, non‐human great apes tended to have muscles better designed for moving the joints through large ranges. This was particularly true of the pedal digital flexors in orang‐utans. In gibbons, the only lesser ape studied here, many of the moment arms measured were relatively short compared with those of great apes. This study was performed on a small sample of apes and thus differences noted here warrant further investigation in larger populations.

Orangutans employ unique strategies to control branch flexibility

Orangutans are the largest habitually arboreal mammal. For them, as for all arboreal mammals, access to the abundant fruits and narrowest gaps found among the thin peripheral branches of tree crowns poses considerable safety risks and energetic demands. Most arboreal primates use flexed-limb postures to minimize problems caused by branch compliance and instability. Here, we show that Sumatran orangutans employ unique locomotor strategies to control compliance and allow access to the terminal branch niche for feeding and gap crossing. We calculated a “stiffness score,” which is a measure of the flexibility of the supports on which orangutans moved. We found that certain locomotor behaviors clearly are associated with the most compliant supports; these behaviors appear to lack regular limb sequences, which serves to avoid the risk of resonance in branch sway caused by high-frequency, patterned gait. Balance and increased stability are achieved through long contact times between multiple limbs and supports and a combination of pronograde (horizontal) and orthograde (vertical) body postures, used both above branches and in suspension underneath them. Overall, adult females seem to be the most conservative in their travel, selecting more solid and secure supports than males and adolescents. These results have implications for understanding locomotor diversity in fossil and extant apes and for orangutan conservation and reintroduction programs.

Gait parameters in vertical climbing of captive, rehabilitant and wild Sumatran orang-utans (Pongo pygmaeus abelii).

SUMMARY Vertical climbing is central to the locomotor and foraging strategies of the great apes and, indeed, to theories about the evolution of locomotor specialisations of hominoid primates. Nevertheless, its kinematics have yet to be fully evaluated. Here, we present spatio-temporal parameters of 80 climbing sequences containing 560 limb cycles obtained from video recordings of captive, rehabilitant and wild Sumatran orang-utans (Pongo pygmaeus abelii). Gait parameters such as cycle duration, duty factor, laterality of footfalls, relative stride length and normalised speed were analysed to identify the influence of body size (through an intraspecific comparison of age/sex classes), the influence of the environment (through an intraspecific comparison of animals living in different habitats) and the influence of morphology (through an interspecific comparison with the climbing characteristics of other primates) on climbing ability in orang-utans. Results show that there are only few differences between the climbing of wild, rehabilitant and captive individuals. Cycle duration is longer and speed is lower for the wild individuals than for other groups due to the complexity of their environment and lack of familiarity with each substrate, which results in a more cautious gait. Sex/age-related differences in climbing were found to be small, although juveniles generally exhibited a shorter cycle duration and lower duty factor than other groups. The spatio-temporal gait parameters of adult females carrying infants were not found to differ significantly from those for females without an infant, which suggests that climbing kinematics are not affected by the presence of a clinging infant. Extended-elbow vertical climbing is primarily characterised by a higher duty factor than flexed-elbow climbing, indicating that the former is an energetically more demanding form of locomotion. In comparison with other primates, orangutans exhibit a longer cycle duration, longer strides but lower climbing speed, reflecting a compromise between the demands of a large body mass and extreme joint mobility.

Inertial properties of hominoid limb segments

Quantitative, accurate data regarding the inertial properties of body segments are of paramount importance when developing musculo‐skeletal locomotor models of living animals and, by inference, their ancestors. The limited number of available primate cadavers, and the destructive nature of the post‐mortem, result in such data being very rare for primates. This study builds on the work of Crompton et al. (Am. J. Phys. Anthropol. 1996, 99, 547–570) and reports inertial properties of the body segments of gorillas, chimpanzees, orang‐utans and gibbons. Segment mass, centre of mass and the radius of gyration of five ape cadavers were measured using a complex‐pendulum technique and compared with the results derived from external measurements of segment lengths and diameters on the same animals. With additional data from external measurements of eight more hominoid cadavers, and published data, intergeneric differences between the inertial properties and the distribution of mass between limb segments are analysed and related to the locomotor habits of the species. We found that segment inertial properties show extensive overlap between ape genera as a result of large interindividual variation. Segment mass distribution also overlaps between apes and humans, with the exception of the shank segment. However, owing to a different distribution of mass between the limb segments, the centre of mass of both the arms and the legs is located more distally in apes than in humans, and the natural pendular period of ape forelimbs is larger than that of the hindlimbs. This suggests that, in contrast to the limbs of cursorial mammals and cercopithecoid primates, hominoid limbs are not optimized for efficiency in quadrupedal walking, but rather reflect a compromise between various locomotor modes. Common chimpanzees may have secondarily evolved a more efficient quadrupedal gait.

Nest-building orangutans demonstrate engineering know-how to produce safe, comfortable beds

Nest-building orangutans must daily build safe and comfortable nest structures in the forest canopy and do this quickly and effectively using the branches that surround them. This study aimed to investigate the mechanical design and architecture of orangutan nests and determine the degree of technical sophistication used in their construction. We measured the whole nest compliance and the thickness of the branches used and recorded the ways in which the branches were fractured. Branch samples were also collected from the nests and subjected to three-point bending tests to determine their mechanical properties. We demonstrated that the center of the nest is more compliant than the edges; this may add extra comfort and safety to the structure. During construction orangutans use the fact that branches only break half-way across in “greenstick” fracture to weave the main nest structure. They choose thicker branches with greater rigidity and strength to build the main structure in this way. They then detach thinner branches by following greenstick fracture with a twisting action to make the lining. These results suggest that orangutans exhibit a degree of technical knowledge and choice in the construction of nests.

Functional adaptations in the forelimb muscles of non-human great apes

The maximum capability of a muscle can be estimated from simple measurements of muscle architecture such as muscle belly mass, fascicle length and physiological cross‐sectional area. While the hindlimb anatomy of the non‐human apes has been studied in some detail, a comparative study of the forelimb architecture across a number of species has never been undertaken. Here we present data from chimpanzees, bonobos, gorillas and an orangutan to ascertain if, and where, there are functional differences relating to their different locomotor repertoires and habitat usage. We employed a combination of analyses including allometric scaling and ancovas to explore the data, as the sample size was relatively small and heterogeneous (specimens of different sizes, ages and sex). Overall, subject to possible unidentified, confounding factors such as age effects, it appears that the non‐human great apes in this sample (the largest assembled to date) do not vary greatly across different muscle architecture parameters, even though they perform different locomotor behaviours at different frequencies. Therefore, it currently appears that the time spent performing a particular behaviour does not necessarily impose a dominating selective influence on the soft‐tissue portion of the musculoskeletal system; rather, the overall consistency of muscle architectural properties both between and within the Asian and African apes strengthens the case for the hypothesis of a possible ancient shared evolutionary origin for orthogrady under compressive and/or suspensory loading in the great apes.