Mechanisms for the acquisition of habitual bipedality: are there biomechanical reasons for the acquisition of upright bipedal posture?

Abstract

Morphology and biomechanics are linked by causal morphogenesis ('Wolff's law') and the interplay of mutations and selection (Darwin's 'survival of the fittest'). Thus shape-based selective pressures can be determined. In both cases we need to know which biomechanical factors lead to skeletal adaptation, and which ones exert selective pressures on body shape. Each bone must be able to sustain the greatest regularly occurring loads. Smaller loads are unlikely to lead to adaptation of morphology. The highest loads occur primarily in posture and locomotion, simply because of the effect of body weight (or its multiple). In the skull, however, it is biting and chewing that result in the greatest loads. Body shape adapted for an arboreal lifestyle also smooths the way towards bipedality. Hindlimb dominance, length of the limbs in relation to the axial skeleton, grasping hands and feet, mass distribution (especially of the limb segments), thoracic shape, rib curvatures, and the position of the centre of gravity are the adaptations to arboreality that also pre-adapt for bipedality. Five divergent locomotor/morphological types have evolved from this base: arm-swinging in gibbons, forelimb-dominated slow climbing in orangutans, quadrupedalism/climbing in the African apes, an unknown mix of climbing and bipedal walking in australopithecines, and the remarkably endurant bipedal walking of humans. All other apes are also facultative bipeds, but it is the biomechanical characteristics of bipedalism in orangutans, the most arboreal great ape, which is closest to that in humans. If not evolutionary accident, what selective factor can explain why two forms adopted bipedality? Most authors tend to connect bipedal locomotion with some aspect of progressively increasing distance between trees because of climatic changes. More precise factors, in accordance with biomechanical requirements, include stone-throwing, thermoregulation or wading in shallow water. Once bipedality has been acquired, development of typical human morphology can readily be explained as adaptations for energy saving over long distances. A paper in this volume shows that load-carrying ability was enhanced from australopithecines to Homo ergaster (early African H. erectus), supporting an earlier proposition that load-carrying was an essential factor in human evolution.

Fig. 1

Hand of a chimpanzee, loaded in knuckle-walking (a). The external load Fe is about 20% of body weight. (b) Loaded in suspended posture. The external load Fe is proportional to total body weight. In arm-swinging, it may readily increase to twice body weight, because of centrifugal force. The forces acting on the metacarpal are indicated in both cases and drawn to the same scale.

Fig. 2

Proportions of several hominoids redrawn after Schultz (1956). From left to right: Hylobates, Pongo, Pan, Gorilla, Oreopithecus, Australopithecus afarensis AL 288-1 ‘Lucy’, Homo ergaster (early African H. erectus), H. sapiens.

Fig. 3

Distribution of body weight on fore- and hindlimbs on inclined substrates. Note that the pair of limbs closer to the ground receives a greater share of the substrate reaction force.

Fig. 4

Grasping with digits, pressing a grasped object against an abutment. In the feet of primates, this is commonly the hallux; in the hands, the pollex (a) may be replaced by (b) the soft tissue over the heads of the metacarpals, or the thenar plus hypothenar eminences. Increased length of the autopodia (hands and feet), which increases the span of the grip, nevertheless reduces the contact pressure (c). Reduced width of the hand (d) leads to higher pressure over the contact area. Because friction depends on the contact pressure, this allows the transmission of greater rotating moments.

Fig. 5

Schematic drawings of fore- and hindlimbs to show the effect of elevation of carpus or heel, respectively, from the ground for elongation of the functionally important limb length (= inverted limb pendulum). The examples are plantigrade humans, semiplantigrade vervets, digitigrade vervets, chimpanzee, dog hind- and forelimbs. The vertical bars indicate the elongation of the inverted limb pendulum.

Fig. 6

Trunk flexion in springing gaits of quadrupedal primates. Drawn after film recordings. The vertebral columns and pelvic outlines are tentative. (a): Cheirogaleus, (b): baboon, (c): chimpanzee.

Fig. 7

Chimpanzee in the usual semi-upright posture. The tensile forces along the dorsal contour are provided by the erector spinae and the gluteus medius. A rough estimate of the hip resultant (Ri) shows that it passes close to the sacro-iliac joint, which therefore is not exposed to high torques. The same holds true for the chimpanzee in quadrupedal posture.

Fig. 8

Plot of the torques (bending moments) evoked by the weight of head, neck, forelimbs and trunk at the lumbo-sacral joint. All these parts are represented by a cylinder. Horizontal axis: increased erection of trunk axis, inclination angle from pronograde to orthograde. Vertical axis: ratio between length/diameter increasing from 10 : 3 (thick-bellied gorilla) to 10 : 1.5 (slender human).

Fig. 9

Schematic cross-section through the shoulder region of a cursorial mammal in (left) two-limb support and (right) one-limb support. Skeleton: black, muscles: double lines. The narrower the trunk, the smaller the moments. The joint forces in the shoulder joint lie in a parasagittal plane. A clavicle is superfluous.

Fig. 10

Shoulder region of a climber, in side view (a), and in cranial view (b,c). The joint resultant in the shoulder joint has a large component in the medial direction. To counterbalance this component, the scapula must offer a glenoid surface that faces laterally. The muscles pectoralis, latissimus and serratus exert high bending moments on the ribs. A pronounced curvature of the ribs gives them the necessary strength to sustain these bending moments. In addition, a clavicle is of advantage to prevent giving way of the scapula.

Fig. 11

Deep trunk (left) compared with a shallow trunk (right) in upright posture.

Fig. 12

Six ‘Baumuster’ (specializations), realized among hominoids: (a) the quadrupedal arborealist Proconsul; (b) chimpanzee, as representative of the African apes, generalist, adapted climber and quadrupedal walker with bipedal potential; (c) gibbon, highly specialized brachiator; (d) orang-utan and the similar Oreopithecus, slow climbers in trees, on the ground or on rigid, horizontal branches, bipedalists who use their arms for support; (e) Australopithecus, bipedal ground-dweller with high potential for climbing in trees; (f) Homo, highly specialized terrestrial bipedalist, not afraid of the third dimension, but not really gifted in using it.

Fig. 13

(a) Energy-saving effect of long forelimbs. The longer the arms in vertical clinging or climbing, the lower the forces acting on the forelimbs. (b) Length increase of the arms is limited by the disproportional increase of arm mass in comparison with muscle strength. (c) Increase of mass is a third power function of linear dimensions; increase of load moments of rotation a fourth power function; and increase of mass moments of inertia, which must be overcome in rapid movements, a fifth power function of linear dimensions. Muscle strength on the opposite side is a second power function.

Fig. 14

The specific elongation of the trunk (a) seen in humans, in contrast to its shortness in the other Hominoidea (b), offers the mass moment of inertia necessary to stabilize the trunk and head against the movements of heavy and long hindlimbs. A tendency for the trunk to rotate about its vertical axis during walking is resisted by the pattern of distribution of body mass about its cross-section (c,d). This distribution explains the greater pelvic and shoulder breadth in Homo compared with other apes. Elastic stretching and recoil of the oblique muscles of the abdomen (e) recover energy during steady-state walking, while forming a waist between the pelvis and thorax.

Fig. 14

The specific elongation of the trunk (a) seen in humans, in contrast to its shortness in the other Hominoidea (b), offers the mass moment of inertia necessary to stabilize the trunk and head against the movements of heavy and long hindlimbs. A tendency for the trunk to rotate about its vertical axis during walking is resisted by the pattern of distribution of body mass about its cross-section (c,d). This distribution explains the greater pelvic and shoulder breadth in Homo compared with other apes. Elastic stretching and recoil of the oblique muscles of the abdomen (e) recover energy during steady-state walking, while forming a waist between the pelvis and thorax.

Fig. 15

Pelvic shapes in side view (top and middle) and cranial view (bottom). (a) Chimpanzee in a position different from those shown in Fig. 7; the resultant of all forces acting on the hip joint, Ri, also passes through the iliosacral joint, relieving the ilium from bending. In contrast, the iliac neck in humans (b,c) is usually exposed to bending moments. The iliac neck (hatched) therefore can be long in the chimpanzee (d) and must be short in Homo (f). The iliac crest (black, g–i) indicates low resistance to bending in the chimpanzee (g) and high resistance to bending in Homo (i). Australopithecus (e,h) assumes an intermediate position.

Fig. 16

Stresses in the pelvis according to Lenz (1993). The pelvic entrance (a) is taken as a ring, loaded by body weight applied to the sacrum and supported by the hindlimbs at the hip joints. The stresses are shown as negative values for several postures (b,c); the distribution of bone material allows the stresses to be kept at the same level along the entire pelvic ring. The calculation leads to a distribution of material that roughly corresponds to the arrangement of bone in a human (b) or a chimpanzee (c).

Fig. 17

Schematic variation of trunk shapes to minimize the bending moments along the trunk axis. The dorsal muscles have to exert tensile forces to keep the mobile spine in its position. Left, in semi-upright posture, muscle activity is necessary along the entire trunk; second left, if a lordotic flexion is assumed, the muscle activity can be confined to the part caudal to the flexion; second right, if the flexion is shifted caudally, muscle force can be saved, but this is only possible if the pelvis is short (as in australopithecines); or right, if the pelvis itself is involved in the lordotic curvature (as in Homo). The inclined position of the long axis of the pelvis, from iliac crest to the ischial tuberosity, allows the musculature to remain without great functional change.

Fig. 18

Because of the eccentric position of the vertebral column, even when the upper lumbar and thoracic segments are fully upright, a moderate torque remains at the intervertebral joints. In the human trunk, the vertebral column is displaced ventrally (compare a and b) to give the body weight components short (and the muscles long) lever arms. (c,d) Comparison of the position of the load and lever arms in relation to the vertebral column in cross-sections at the level of a thoracic vertebra in (c) a human and (d) a chimpanzee.