AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 119:87–91 (2002) Brief Communication: Arboreal Bipedalism in Bwindi Chimpanzees Craig B. Stanford* Jane Goodall Research Center, Department of Anthropology, University of Southern California, Los Angeles, California 90089-0032 KEY WORDS arboreal bipedalism; chimpanzees; positional behavior ABSTRACT 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. Seventyeight 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 grasp- Theories to account for the earliest stages of hominid bipedalism comprise a spectrum of postural adaptations ranging from obligate terrestrial bipedal walking (Lovejoy, 1978, 1988) to bipedalism with substantial retained arboreality (Stern and Susman, 1983; Susman et al., 1984). Some researchers have advocated anatomical/behavioral precursors for terrestrial bipedalism in the vertical climbing and brachiation patterns of great apes (Fleagle et al., 1981), while others have argued for a terrestrial bipedal phase following arboreal bipedal locomotion. The likeliest selection pressure on the transition from an arboreal ape with an unknown degree of bipedalism to a ground-dwelling biped is a subject of much debate (e.g., Isaac, 1978; Rodman and McHenry, 1980; Steudel, 1994; Wheeler, 1984). Jolly (1970), Wrangham (1980), and Rose (1984, 1991) argued that bipedalism arose from adaptations to terrestrial feeding on small objects such as seeds or small fruits. They pointed out that chimpanzees and baboons sometimes shuffle bipedally short distances between feeding sites rather than switching between bipedal feeding and quadrupedal locomotion. More recently, Hunt (1994, 1996) provided an arboreal perspective on small-object feeding and bipedalism. In the most detailed field study conducted of chimpanzee bipedalism, Hunt (1994, 1996) documented 97 instances of bipedalism in Mahale National Park chimpanzees in 701 hr of observation (0.14 bouts/hr), more than 80% of which occurred in © 2002 WILEY-LISS, INC. ing 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 smallfruit 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. Am J Phys Anthropol 119:87–91, 2002. © 2002 Wiley-Liss, Inc. a feeding context. Bipedalism in Hunt’s (1994, 1996) study was as commonly seen in trees as on the ground, and was used especially when foraging for small-diameter fruits such as figs. Nearly all of his bipedalism data were based on postural, as opposed to locomotor, bipedalism. In this paper, I report on the extensive use of arboreal bipedalism by a previously little-known chimpanzee population. During one 2-week period in May 2001, the Ruhija chimpanzees of Bwindi Impenetrable National Park were bipedal at a rate exceeding that published for any other population of free-ranging chimpanzees. Grant sponsor: National Geographic Society; Grant sponsor: C.I.E.S. (Fulbright) Foundation; Grant sponsor: L.S.B. Leakey Foundation; Grant sponsor: Wenner-Gren Foundation; Grant sponsor: University of Southern California. *Correspondence to: Craig B. Stanford, Jane Goodall Research Center, Department of Anthropology, University of Southern California, Los Angeles, CA 90089-0032. E-mail: firstname.lastname@example.org Received 2 August 2001; accepted 26 November 2001. DOI 10.1002/ajpa.10050 Published online in Wiley InterScience (www.interscience.wiley. com). 88 C.B. STANFORD MATERIALS AND METHODS The chimpanzees (Pan troglodytes schweinfurthii) of Bwindi Impenetrable National Park in southwestern Uganda (S 01° 05⬘, E 29° 38⬘) have been studied since 1996 as part of the Bwindi Impenetrable Great Ape Project, a field study of the sympatric ecology of chimpanzees and mountain gorillas (Gorilla gorilla beringei). Bwindi Impenetrable National Park (331 km2) is one of the largest remaining tracts of East African afro-montane forest still in existence, and has a high level of floral and faunal species endemism. The Ruhija chimpanzee community occupies a home range of unknown size in the northeastern sector of the park, within an elevational gradient from approximately 2,000 –2,350 m. Although the study subjects cannot be followed on the ground at close range, they tolerate observers within 30 m while in feeding trees. Twenty individually identified members of the study community were observed during May 2001 as they fed in an adjacent pair of large strangler figs (Ficus natalensis, Moraceae): 5 adult males, 1 subadult male, 5 adult females, 5 infants, and 4 juveniles. Data were collected on the 9 days on which the chimpanzees fed in the Ficus. Observations were made with binoculars, and data were collected in 15-min scan sampling whenever animals were visible between 0715–1430 hr, with critical events noted ad libitum. Bipedalism was defined, following Hunt (1994), as a posture in which more than 50% of the body’s weight was judged to be supported by the hind limbs. If the forelimbs lent support or stability, as by grasping an overhead branch, the posture was characterized as assisted bipedalism. In practice, the diversity and gradations of bipedal and semibipedal postures sometimes made it difficult to judge at what point most of the weight support had been shifted to the legs. Since all observed instances of bipedalism were arm-assisted (no unassisted bipedalism standing or walking was seen), all bipedal bouts involved some degree of support from the upper body. Other variants on bipedalism were noted descriptively and later categorized on the basis of Hunt (1994). RESULTS A total of 38.5 hr of observational data was collected on 20 individuals, during which 78 instances of bipedalism by 9 individuals were recorded, an average of 0.49 bouts per observation hour for the entire community. All bipedalism occurred arboreally on the larger limbs of the Ficus natalensis, and all instances occurred in a fig-fruit feeding context. Individuals varied widely in their tendency to be bipedal (Fig. 1), as well as in the average duration of their bipedal bouts. One male (KD) was bipedal at least 24 times in 20.25 contact hours. The sample included 4 adult males and 4 adult females; males were bipedal significantly more often than females (Table 1). The overall mean duration of bipedal bouts was 13.7 sec (⫾1.6 sec). Females exhibited a longer mean duration of bipedal bouts, though not significantly so (Fig. 2, P ⬎ 0.05). This longer duration was due mainly to one adult female (MA) who engaged in several lengthy bipedal feeding bouts of up to 65 sec. The females stood bipedally while carrying dependent infants, either on their backs or clinging to their chests. On three occasions, pairs of chimpanzees stood bipedally side-by-side while foraging from the same cluster of figs. Perhaps the most noteworthy aspect of these observations of bipedalism was not its frequency, but its continuity with other forms of arboreal posture and locomotion. Although some bipedal bouts consisted simply of the animals standing upright on a limb while reaching up for overhead fruits, in at least 45 of 78 instances (58%), bipedalism was used either in conjunction with, or graded into, armhanging and foot-hanging postures that allowed a greater reach during fruit-foraging. For instance, a chimpanzee would, after a short period standing bipedally with both feet planted on the limb and one hand lending support overhead, reach further out into space for more fruit. As it did so, its body would slowly lean from vertical toward horizontal, and at some point the arm on the branch above would shift from a supporting role to a brachiator role. This allowed the animal to swing across to an adjacent limb, whereupon it might resume a bipedal posture. Alternatively, the two-legged bipedal posture might give way to one leg on the substrate and one leg lifted in the air, allowing the chimpanzee greater reaching distance with its arms. As in Hunt (1994), foraging for small-diameter fruits (in this case, figs) seemed to promote bipedal posture. No data were collected on substrate diameter or angle, but this was clearly also a major determinant of bipedal foraging. Bipedalism was observed only on the largest terminal branches of the Ficus, perhaps because only these limbs provided both access to preferred ripe figs and a large-diameter substrate for standing upright. DISCUSSION AND CONCLUSIONS Whether the extensive use of bipedalism noted at Bwindi is characteristic of the chimpanzees there or was a rare aberration is unknown. Certainly many primates engage in brief bouts of arboreal bipedalism while foraging. If Bwindi chimpanzees are more bipedal than other chimpanzee populations, it is unknown whether this is due to aspects of the forest structure at Bwindi that promote arboreal bipedal foraging, or is a culturally inherited locomotor tradition. Some evidence suggests that a special foraging substrate may have accounted for the level of bipedalism observed. The large Ficus natalensis that was the main feeding site for these data was growing on a steep hillside, leaning at an approximately 45° angle from the vertical. Because of this, the large ARBOREAL BIPEDALISM IN BWINDI CHIMPANZEES 89 Fig. 1. Bipedalism bouts observed in individual chimpanzees. FD, KM, MA, and AF are adult females; FR, KD, KU, and MB are adult males; JU and YW are immatures. TABLE 1. Frequency of bipedalism by age-sex class during May 2001 Age-sex category Total bipedal bouts % 15-min scans, bipedal Adult male Adult female Immature 48 21 6 19.5 10.0 8.8 outer branches of the fig were nearly horizontal, providing arboreal substrates that were both strong enough to be stood upon and also with fruits reachable on the terminal branches. Had the tree been standing vertically, these branches would have been angled closer to the vertical and would not have been substrates on which bipedalism could have been easily used. The unusual angle of growth created a web of branches that were nearly horizontal and in some cases parallel to each other, allowing chimpanzees to stand on one limb and reach upward to the next for support and for fruit. Since limited observations of the same animals in other tree crowns produced no evidence of bipedalism, the level of bipedalism reported in this paper may have been promoted by the unusual angle of growth of the Ficus. One explanation for bipedalism in wild chimpanzees has been injuries to the arms or hands. Following a polio epidemic in the 1960s in Gombe National Park, Tanzania, some chimpanzees who suffered paralysis to the upper body began to walk bipedally (Goodall, 1986). Snare injuries to the hands are a common problem for chimpanzees in Ugandan forests, and this might explain a high incidence of bipedalism. However, among the Ruhija chimpanzees only one animal, the adult male (KU) who accounted for 4 of the 78 bouts of arboreal bipedalism, possessed a severe snare injury. It seems unlikely, therefore, that injury accounts for the frequency of bipedalism among Bwindi chimpanzees. Despite widespread anecdotal mention of the degree of bipedalism in bonobos, P. paniscus (e.g., Kano, 1992; de Waal and Lanting, 1997), there are no published data indicating that wild bonobos are more bipedal than wild chimpanzees. Doran and 90 C.B. STANFORD Fig. 2. Mean duration of bipedalism bouts, males vs. females. Immatures were omitted due to small sample size. Hunt (1994) compared locomotor data on the two species and found that bonobos were more arboreal than wild chimpanzees, but their analysis did not include bipedalism data. Videan and McGrew (2001) showed that among captive populations of both species, there was no statistically significant difference in the degree of bipedalism. Assertions that bonobos are more bipedal than chimpanzees should therefore be regarded with caution. It has long been thought that savanna-dwelling chimpanzee populations may be highly bipedal. Data from Bwindi chimpanzees, like those of Hunt (1994), suggest that forest-living chimpanzees may be as bipedal, although on different substrates, as those living in more open landscapes. Chimpanzees have long been a model for the evolution of human behavior, and chimpanzee locomotion has long been used as evidence in debates about the locomotor patterns of the earliest hominids. Washburn (1963, 1968), for example, saw terrestrial knuckle-walking as the way our immediate prehominid ancestors must have traveled, and advocated early terrestriality on emerging savannas as the behavioral ecological shift that preadapted prehominids to bipedalism. Bipedalism and its variants may, however, have emerged from an arboreal hab- itus that placed an evolutionary premium on foraging benefits that accrued to apes during small-object feeding (Tuttle, 1981; Rose, 1984; Hunt, 1994). Further studies of bipedal posture and locomotion in free-ranging great apes can address this question as a key complement to the fossil record. ACKNOWLEDGMENTS Research in the Bwindi Impenetrable National Park was carried out with the permission of the Uganda Wildlife Authority, the Ugandan National Council for Science and Technology, and the Institute for Tropical Forest Conservation. I gratefully acknowledge Dr. Alastair McNeilage, Caleb Mgambaneza, John Bosco Nkurunungi, and Gervase Tumwebaze for their assistance. LITERATURE CITED de Waal FBM, Lanting F. 1997. Bonobo: the forgotten ape. Berkeley: University of California Press. Doran DM, Hunt KD. 1994. Comparative locomotor behavior of chimpanzees and bonobos. In: Wrangham RW, McGrew WC, de Waal FBM, Heltne PG, editors. Chimpanzee cultures. Cambridge, MA: Harvard University Press. p 93–108. Fleagle JG, Stern JT, Jungers WL, Susman RL, Vangor AK, Wells JP. 1981. Climbing: a biomechanical link with brachiation and with bipedalism. Symp Zool Soc Lond 48:359 –375. ARBOREAL BIPEDALISM IN BWINDI CHIMPANZEES Gebo DL. 1996. Climbing, brachiation, and terrestrial quadrupedalism: historical precursors of hominid bipedalism. Am J Phys Anthropol 101:55–92. Goodall J. 1986. The chimpanzees of Gombe: patterns of behavior. Cambridge, MA: Harvard University Press. Hunt KD. 1994. The evolution of human bipedality: ecology and functional morphology. J Hum Evol 26:183–202. Hunt KD. 1996. The postural feeding hypothesis: an ecological model for the evolution of bipedalism. S Afr J Sci 92:77–90. Isaac GL. 1978. The food-sharing behavior of proto-human hominids. Sci Am 238:90 –108. Jolly CJ. 1970. The seed-eaters: a new model of hominid differentiation based on a baboon analogy. Man 5:1–26. Kano T. 1992. The last ape. Stanford, CA: Stanford University Press. Lovejoy CO. 1978. A biomechanical review of the locomotor diversity of early hominids. In: Jolly C, editor. Early hominids of Africa. New York: St. Martin’s Press. p 403– 429. Lovejoy CO. 1988. The evolution of human walking. Sci Am 259:118 –125. Rodman PS, McHenry HM. 1980. Bioenergetics and the origin of hominid bipedalism. Am J Phys Anthropol 52:103–106. Rose MD. 1984. Food acquisition and the evolution of positional behavior: the case of bipedalism. In: Chivers DJ, Wood BA, Bilsborough A, editors. Food acquisition and processing in primates. New York: Plenum Press. p 509 –524. 91 Rose MD. 1991. The process of bipedalization in hominids. In: Coppens Y, Senut B, editors. Origine(s) de la bipédie chez les hominidés. Paris: Centre National de la Recherche Scientifique. p 37– 48. Stern JT, Susman RL. 1983. The locomotor anatomy of Australopithecus afarensis. Am J Phys Anthropol 60:279 –317. Steudel KL. 1994. Locomotor energetics and hominid evolution. Evol Anthropol 3:42– 48. Susman RL, Stern JT, Jungers WL. 1984. Arboreality and bipedality in the Hadar hominids. Folia Primatol (Basel) 43:113– 156. Tuttle RH. 1981. Evolution of hominid bipedalism and prehensile capabilities. Philos Trans R Soc Lond [Biol] 292:89 –94. Videan E, McGrew WC. 2001. Are bonobos (Pan paniscus) really more bipedal than chimpanzees (Pan troglodytes)? Am J Primatol 54:233–239. Washburn SL. 1963. Behavior and human evolution. In: Washburn SL, editor. Classification and human evolution. Chicago: Aldine. p 190 –203. Washburn SL. 1968. Speculation on the problem of man’s coming to the ground. In: Rothblatt B, editor. Changing perspectives on man. Chicago: University of Chicago Press. p 191–206. Wheeler PE. 1984. The evolution of bipedality and loss of functional body hair in hominids. J Hum Evol 13:91–98. Wrangham RW. 1980. Bipedal locomotion as a feeding adaptation in gelada baboons, and its implications for hominid evolution. J Hum Evol 9:329 –331.