Bipedal Behavior and the Emergence of Erect Posture in Man B. A. SIGMON Department of Anthropology, University of Toronto, Toronto, Canada ABSTRACT Bipedal behavior is present to some degree in most of the higher primates. Field studies of living pongids have shown that an upright stance and various types and degrees of bipedal progression are not uncommon and are thus presumably advantageous. Bipedal behavior similar to that in living pongids could also have been, and probably was, present in pre-hominids. As the environment of the pre-hominids changed, the increased use of bipedalism was of survival value. That is, it was a behavioral response to environmental circumstances and not just a random event. Once bipedal behavior became habitual, it formed part of a pattern of natural selection which shaped a physical type adapted for erect, bipedal posture. BIPEDALISM IN NON-HUMAN PRIMATES Almost all of the higher primates can assume an upright bipedal stance, although in some this locomotor behavior is more common than in others. This is well seen in pongids i n the wild. About one tenth of the locomotion of the gibbon is bipedal walking along the upper surfaces of branches of trees (Carpenter, ’64). Gorillas occasionally take a few bipedal steps-r stand upright on their lower limbs as a display or threat (Schaller, ’63). Bipedal progression in orangutans in the wild has not been observed, although it has been noted in captive animals (Napier, ’64). Most of the observations of bipedality in pongids in the wild (and also in experimental conditions) are of chimpanzees because they have been more frequently studied than almost any other non-human primate except perhaps the macaques. Because the field data are more abundant for chimpanzees, and because this animal is one of the closest relatives of man, the following discussion of bipedality in pongids will be centered around this particular African pongid. Chimpanzees make use of bipedal locomotion more frequently in some environments than in others (Nissen, ’31; KortIandt, ’62; Goodall, ’65; Reynolds and Reynolds, ’65). Differences in their beAM. J. PHYS.ANTHXOP., 34: 55-60. havior can be illustrated by the following field studies. Goodall’s study of chimpanzees in the wild involved a group that inhabit a deciduous woodland environment (Goodall, ’65). Goodall observed bipedalism in these chimpanzees in the following circumstances: (1) looking over tall grass, (2) searching for a comrade, (3) watching a n unusual part of the surroundings (for example, a human observer), (4) when carrying objects in the hands, (5) in threat displays, and (6) in greeting and courtship (standing upright and swaying from foot to foot). I n a later monograph (van Lawick-Goodall, ’68) she described a n additional circumstance during which bipedalism was used by the chimpanzees-when moving over ground which was wet after a hard rain. Under nonfield conditions, Kohler (‘59) also observed that chimpanzees will walk bipedally when the ground is damp o r cold. Two other ethologists, Reynolds and Reynolds (‘65) studied chimpanzees that live in a rain forest, which is a habitat that is quite different from that of the animals in Goodall’s study. The only bipedal behavior observed in these rain forest chimpanzees was bipedal walking which occurred “rarely” on the ground and “infrequently” along the branches of trees (with the forelimbs holding onto other branches for support). 55 56 B. A. SIGMON Differences in the amount of bipedal progression observed in these two groups of chimpanzees would appear to be due to differences in the type of environment inhabited. Two additional studies shed further light on this observation. Nissen (’31) studied chimpanzees occupying an area similar to that of the rain forest chimpanzees observed by Reynolds and Reynolds (‘65). The two studies agree with regard to the amount of bipedal locomotion observed. Nissen states: . . I never saw a chimpanzee in the bush walking upright, although on several occasions I saw them standing on their two hind limbs.” (’31:37). Normally, the chimpanzees studied by Nissen progressed quadrupedally at a leisurely pace; in addition, they were agile climbers and used various forms of running and leaping. A fourth field study is that of Kortlandt (’62) who observed chimpanzees living near a pawpaw-banana plantation in a habitat similar to that of the chimpanzees in Goodall’s study. Kortlandt noted that the chimpanzees that he observed were mostly terrestrial, preferring progression on the ground to swinging and climbing in trees. Arboreal movements are undertaken hesitantly and cautiously. In the plantation area he noted that bipedal walking and running were used for 10 to 15% of the distance covered by the animals, and he lists the following occasions during which an upright pose or gait was assumed: (1) to free the hands for eating or carrying food, (2) to view the surroundings at better advantage, (3) in jumping across brooks, and (4) in threats. Thus the nature of the habitat occupied by the four groups of chimpanzees reported in the above studies appears to have been a major factor in determining the amount of bipedal behavior that was observed. A semi-open environment, as in Goodall’s and Kortlandt’s studies, appears to be a stimulus for increased use of bipedal locomotion, while a dense rain forest environment, as in Nissen’s and Reynolds and Reynolds’ study, does little to encourage a two-legged gait. This is an interesting point worthy of emphasis and will be discussed later in relation to the origin of erect bipedalism in man. ‘I. BIPEDAL BEHAVIOR AS A PREADAPTATION Some authors have attempted to explain the origin of erect bipedality in terms of one or another behavioral characteristic of non-human primates. For example, Hewes (‘61, ’64) discussed the habit of food-carrying in non-human primates as a critical preadaptation for erect bipedal posture. His experimental work on stumptail macaques revealed that monkeys are capable of assuming an upright gait when carrying food in their hands. Hewes concluded that food-carrying in early hominids led to the f‘reeing of the upper limbs from locomotor activity and to the increased importance and use of only the lower limbs for progression. Wescott (’67) has suggested the importance of the role of threat display and “agonistic exhibitionism” as preadaptations for erect bipedal posture. Instead of selecting one or another behavioral trait, I suggest that the total range of bipedal behavior that has been observed in higher primates be taken into consideration. In extrapolating then from non-human higher primates to pre-hominids, it is probably reasonable to assume that the latter were making use of bipedalism in circumstances similar to those seen in living pongids: in courtship, greeting, threat display, jumping across barriers, while eating or carrying food, in viewing their surroundings at better advantage in order to look for predators, companions, or for other activities that we have neither observed nor thought of. It is almost certainly incorrect to single out one reason for upright locomotion over another as being the most important, or the one that was a major preadaptation for erect bipedalism in man. Bipedalism in non-human higher primates is used in a number of different circumstances, but the key factor is that it is used whenever it improves the chances of survival of the organism. The fact to stress then is that bipedal locomotion is used, disregarding for the moment what the circumstances may be, and that it is a behavioral response on the part of an animal attempting to adapt to its environmental circumstances. BIPEDAL BEHAVIOR AND ERECT POSTURE THE ROLE OF THE ENVIRONMENT AND OF BEHAVIOR Le Gros Clark (’55), Washburn and Howell (’60), Robinson (’63), and others have discussed the importance of changes in the environment of the pre-hominids as an impetus toward the adoption of erect bipedalism. It is generally agreed that the emergence of bipedal striding occurred in savannah areas sparsely dotted with forests where the pre-hominids would have been moving over the grassy plains between clumps of trees. Differences in environmental conditions have a n important effect on locomotion in non-human primates. This has been illustrated by differences in locomotor habits of chimpanzees living i n open deciduous woodland (Kortlandt, ’62; Goodall, ’65) as compared with chimpanzees living in rain forests (Nissen, ’31; Reynolds and Reynolds, ’65). The former use bipedal behavior much more frequently and in more varied circumstances than do the latter. Perhaps an analogy can be made between chimpanzees inhabiting a deciduous woodland region and pre-hominids also in a n environment with decreasing tree coverage. The latter environment could have provided the stimulus for the development of a new locomotor habit, or the increased use and refinement of one already being used, namely bipedal behavior. The emergence of erect bipedalism can be viewed in terms of three stages of development: a preadaptive, a behavioral, and a physical stage although the latter two are probably highly interrelated. During the preadaptive stage the prehominids would probably have been making use of bipedal locomotion in a number of circumstances (as has been illustrated to occur in chimpanzee groups). During this period of development, however, the use of upright locomotion would not have been critical to the survival of the species. Now let us assume that there is a change in the environment that is such as to make erect bipedalism of high adaptive value. This leads us into the second stage which is directly associated with the behavioral response of the organism. Before going into detail on the second 57 stage, let us consider the role of behavior as a sclcctive force in evolution (see also Ewer, ’60, Hardy, ’65). This capacity to respond to changes in the environment is a characteristic of the behavior of a n animal, and can be a very significant factor for the survival of the animal. Ewer (’60:163) says: “It would appear to be glaringly obvious that what a n animal does or tries to do, can determine what characters are of survival value, i.e., can decide the direction of natural selection. . . .” She further states that (‘60: 164): “The adaptability of behaviour to varying environmental conditions gives it a factor of safety allowing a n immediate behavioural response to be made at once to a changed situation, without the necessity of waiting for appropriate changes in the genetical structure of the population. Thus behavior will tend to be always one jump ahead of structure, and so to play a decisive role in the evolutionary process.” Thus after the animal responds behaviorally to environmental changes, this behavior can then become a part of the total pattern of natural selection, making it different from what it would have been otherwise. That is, following the new behavioral response, the morphological/ physiological structure of the organism can be modified by the modified selection pattern resulting from the changed behavior. Those physical changes that assist the behavioral adaptation will be selected for. It is in this sense that Ewer (’60) and Hardy (‘65) speak of behavior as a creative and a selective force in evolution. Perhaps the concept can be usefully applied to the process of the evolution of erect bipedal posture in the hominids. Let us return now to the second stage of development of erect bipedalism: the behavior a1 response . Bipedal behavior was probably present in the pre-hominids as a preadaptation. With the change in environment, the pre-hominids presumably responded behaviorally to increased selection pressure favoring bipedalism. The increased use of upright posture by pre-hominids was probably not merely a random event but improved their adaptation, hence their chances of survival. The capacity of the pre-hominids to make 58 B. A. SIGMON a behavioral response was probably a major factor contributing to their survival. Once the bipedal behavior became habitual, it influenced the natural selection pattern in a manner that favored the development andlor refinement of a physical type that further improved the behavioral character, bipedalism. The third stage involved the physical adaptations that were necessary in changing a pronograde animal to an habitual biped. The most significant changes can especially be seen in the foot, pelvis, vertebral column, skull, and the corresponding muscular systems of these areas. The literature on this subject is vast, and I will attempt to summarize only certain of the more salient points. It should perhaps be noted that the ape grade of organization is frequently regarded as representing the earlier pre-hominid condition. Consequently, the postulated pre-hominid morphology referred to in the following discussion is based on our knowledge of the ape grade of organization. As the pre-hominids began using an upright, bipedal gait more and more frequently, and as this means of locomotion began providing them with survival advantages, any morphological changes that would have increased the efficiency of bipedal posture would of course have had strong selective value. The sequence of changes probably began in the lower half of the body-in the foot, the lower limb, and the pelvis. The pre-hominid foot was adapted for tree climbing, being flexible and having powerful grasping muscles, an abducted great toe, and no arch. The lower limb was short and the pelvis long and narrow. As bipedalism began to be used more frequently, those pre-hominids deviating from the above pattern would have had a selective advantage. A more compact foot with an adducted great toe and an arch would absorb the shock produced in walking or running in an upright posture, while also providing a more efficient structure for a bipedal animal. Correspondingly, an increase in the length of the lower limb would have provided additional leverage needed by the muscles used in bipedal striding. Changes in the pelvis would also have been necessary in the acquisition of erect posture. The long, narrow pre-hominid pelvis became shorter and wider. The decrease in height is especially notable in the ilium and ischium. Most of the increase in width occurred in the ilium which simultaneously changed in shape from a blade-like structure to one with a sigmoid curvature. While the pelvic-thigh muscles of the hominid and ape grades of organization do not differ with regard to the type of action that can be produced, the effect of that action is significantly different. Of particular importance are the gluteus maximus and the hamstring muscles which in both upright bipeds and apes are important extensors of the thigh (Sigmon and Robinson, '67; Robinson, '68, Sigmon, '69). It was formerly thought that the gluteus maximus in the apes was primarily an abductor of the thigh and that the change from abduction in pongids to extension in hominids enabled the latter to become upright bipeds (Washburn, 'SO). This hypothesis has been shown to be incorrect; instead it is the effect of the action that differs, not the action itself (Robinson, '68, '70). In the great apes the ischium is relatively longer and the femur relatively shorter than it is in upright bipeds. These two skeletal elements are the major attachments for the hamstrings, and also for gluteus maximus in apes. Thus, with a long moment arm (ischium) and short lever arm (femur or lower limb), these muscles produce power of action, The upright bipeds have the reverse proportions-a relatively shorter ischium and longer femur, so that the hamstrings produce speed of action and a wider range of movement. Gluteus maximus in upright bipeds is more of a speed-of-action muscle compared to that of apes. Power would naturally be of more value to an animal that spends much time climbing, whereas speed and range of movement would be of greater advantage to a biped who has become more or less independent of trees both for food and for protection, and more dependent on his abilities to cover a lot of ground in the shortest possible time. In the upright BIPEDAL BEHAVIOR AND ERECT POSTURE biped, therefore, power of action has been sacrificed for speed of action. With the increased use of bipedalism the vertebral column became vertical and in the process acquired a n S-shaped curvature necessary for flexible movement and also important in balance. A s the orientation and curvature of the vertebral column changed, the occipital condyles on the skull shifted to a more anterior location, and as a result the skull occupied a more “balanced” position. I n the quadrupedal pre-hominid, the robust skull extended forward of the vertebral column and therefore had to be supported by strong neck muscles that originated high on the occiput. With the skull in a more balanced position, the neck muscles decreased in size and their bony attachment (nuchal crest) shifted to a lower position on the occiput and decreased in size as well. The adoption of upright posture also saw a shift in the center of gravity from the lumbar to the sacral region. Other changes were occurring in the face, jaws and teeth. The pre-hominid face was probably robust, and the jaws and teeth were large and strong due partly to their use in grasping and defense. As the forelimbs became freed with the use of upright locomotion, they took over the function formerly performed by the jaws and teeth, and as a result the latter were reduced in size. Subsequent changes in diet later continued this trend (Robinson, ’63, ’68). These and other changes could, of course, be discussed a t greater length. This abbreviated discussion serves only to highlight some of the major anatomical changes involved in the acquisition of erect bipedal posture. What should be stressed is that behavior itself played a n important role in the selection that shaped the physical structures that were adaptive for upright locomotion. CONCLUSION Three points are emphasized in this paper. First, the data from field studies on chimpanzees show that the animals behave differently in different environmental situations. Those groups of chimpanzees living in a deciduous woodland 59 environment make use of bipedal behavior more frequently and in more vaned circumstances than those groups inhabiting the rain forest. This fact indicates that the animals are capable of adjusting their behavioral responses to environmental differences. Second, stressing that a single specific behavioral trait is the major preadaptation for erect bipedalism in man overlooks the fact that bipedal behavior i n nonhuman higher primates is used in a number of different circumstances and, more importantly, is used whenever it improves the chances of survival of the animal. Third, as the environment of the prehominids changed, bipedal behavior must have become of greater importance than it had formerly been. The nature of behavior is such that it will often allow a n immediate behavioral response that can enable animals to adjust at once to changes in their environment. The genetical structure of a population does not change so rapidly. This capacity to make a n immediate behavioral response must have been a major factor enabling the pre-hominids initially to adapt to, and survive in, a changing environment. The subsequent physical changes would have evolved along the lines that were adaptive for the behavior, and thus bipedalism as a behavioral character was probably a very important force i n the evolution of erect bipedal posture in the hominids. ACKNOWLEDGMENTS It should be specially noted that many of the ideas in this paper have been developed through numerous conversations with Dr. J. T. Robinson of the University of Wisconsin. His participation i n discussicns and in his critical reading of the manuscript are gratefully acknowledged. LITERATURE CITED Carpenter, C. R. 1964 A field study in Siam of the behavior and social relations of the gibbon (1940). I n : Naturalistic Behavior of Nonh u m a n Primates. C. R. Carpenter, ed. Penn. State Univ. 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