Positional Behavior of Pan Troglodytes in the Mahale Mountains and Gombe Stream National Parks, Tanzania KEVIN D

Home , Gibbon, Orthograde posture, Pan (genus)

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 87233-105 (1992)

Positional Behavior of Pan troglodytes in the Mahale Mountains and Gombe Stream National Parks, Tanzania KEVIN D. HUNT Department of Anthropology, Indiana University, Bloommgton, Indiana 4 7405 KEY WORDS Arm-hanging, Quadrumanous climbing, Brachia- tion, Humeral abduction ABSTRACT The positional behavior of habituated adult chimpanzees and baboons was observed for 784 hr in a year-long study. Comparisons between species were made to establish the distinctiveness of chimpanzee positional behavior and habitat use. Brachiation (sensu stricto, i.e., hand-over-hand suspensory locomotion) was observed in low frequencies among chimpanzees, and its significance for chimpanzee anatomy is judged slight. Although no significant differences were found between sympatric baboons and chimpanzees in the proportion of time spent in the terminal branches, or in the mean diameter of weight-bearing strata, chimpanzees exhibited evidence of a terminal branch adaptation in that they, unlike baboons, used postures among smaller supporting strata different from those used among larger supports. Among chimpanzees, unimanual arm-hanging was most common among the smallest strata and was associated with smaller mean and median support diameter than other postures. Unimanual arm-hanging was the only common behavior among chimpanzees that usually involved complete abduction of the humerus. A number of behaviors often subsumed under the label “quadrumanous climbing” were distinguished in this study. Compared to baboons and other cercopithecoids, chimpanzees did not show increased frequencies of large-stratum vertical climbing, and their vertical climbing did not involve significant humeral abduction. Arm-hanging (i.e., unimanual suspension) and vertical climbing distinguish chimpanzee positional behavior from that of monkeys.

Apes share high intermembral indices, which these traits are evolved. Keith (1891, curved metarcarpals and phalanges, long 1899,1903) speculated that the morphologi- fingers, mobile shoulders, mediolaterally re- cal specializations of the gibbon were related duced scapulae, cranially oriented glenoid to brachiation (sensu stricto),’ and assumed fossae, cone-shaped ribcages, anteroposteri- that the then-unstudied African apes shared orly flattened torsos with concomitantly long this adaptation (cf. Chivers, 1972; Andrews clavicles, strongly curved ribs resulting in and Groves, 1976). The ascendancy of this more ventrally placed vertebral bodies, wide paradigm inspired anatomists to interpret manubria of the sterna, reduced numbers of virtually every ape specialization as adapted lumbar vertebrae, the lack of a tail (Keith, to brachiation (e.g., Napier, 1963a,b, 1967; 1899; Schultz, 1930; Erikson, 1963; Susman, Erikson, 1952,1954,1957,1963;Ashton and 19791, a distinctive pelvic floor (Keith, 1923) Oxnard, l963,1964a,b; Oxnard, 1963,1967; and a predominance of muscles that flex the elbow and raise (i.e., abduct or protract) the upper arm (Ashton and Oxnard, 1963; Received December 15,1989; accepted June 3,1991. Napier, 1963a; Oxnard, 1963, 1967; Ashton ‘The term brachiation (sensu stricto) means hand-over-hand et al., 1965; Tuttle, 1969). The anatomical suspensory locomotion, with or without a period offree flight. The qualifier distinguishes it from a liberal usage (sensu lato). Rico- similarity of the apes implies that they share chetal brachiation is used even more restrictively to mean only a limited number of positional modes for gibbon-like brachiation with a period of free flight.

@ 1992 WILEY-LISS,INC. 84 K.D. HUNT

Benton, 1967, 1976; O’Connor, 1975, 1976; that were purported to be kinematically sim- Napier, 1963a). ilar to brachiation (sensu stricto), such as Avis (1962) demonstrated that when con- vertical climbing, hoisting, arm-swinging, fronted with a variety of weight-bearing and, at least tacitly, any other humerus- structures (WBS) apes more often brachi- abducted, forelimb-dominated behaviors, in- ated beneath thin, unstable WBS, whereas cluding postures (Washburn, 1973; Mor- monkeys preferentially locomoted on top of beck, 1972). Some researchers continued to more stable WBS. Brachiation was thought refer to these behaviors as brachiation (see to allow apes to gain access to food resources Andrews and Groves, 1976), but the term found among the small branches at the pe- quadrumanous climbing has come to be pre- riphery of trees (Avis, 1962) andlor to travel ferred. more efficiently than Old World monkeys Although field research on wild primates among the terminal branches by moving di- was interpreted as supporting a quadruman- rectly between adjacent feeding sites (Rip- ous climbing adaptation in apes (Fleagle, ley, 1970; EIlefson, 1974; Rose, 1978).In one 1976a,b; Mittermeier and Fleagle, 1976; form or another the amalgamation of Keith’s Fleagle and Mittermeier, 19801, the term anatomical and Avis’ ecological hypotheses suffers from the same liability as brachiation has dominated ape positional behavior re- (sensu lato) since it conflates a number of search to the present. kinematically diverse behaviors-including Not all anatomical evidence accorded with suspensory locomotion (Fleagle, 1976b, Fig. the brachiation paradigm. Many aspects of 2), quadrupedal walking on slightly inclined the African ape wrist and hand that had WBS (Fleagle, 1976b, Fig. 31, arm-swinging, been supposed to be adaptations to brachia- transferring, scrambling, clambering, and tion were shown to be knuckle-walking ad- vertical climbing-under a single nomen aptations (Tuttle, 1965, et seq.; Jenkins and (Cant, 1986). Fleagle, 1975; Rodman, 1984; Grand, 1984). Of the various positional modes subsumed The contention that the mobile wrist of apes under quadrumanous climbing, vertical was an adaptation to brachiation (sensu climbing has received the most intensive stricto) (Gregory, 1916; Lewis, 1965 et seq.) theoretical attention. Long arms were hy- was cast into doubt by evidence that gibbons, pothesized to confer an advantage to vertical the preeminent brachiators, have the great- climbers by allowing them to ascend larger est ulnar-carpal articulation of all apes (Con- WBS than monkeys (Kortlandt, 1968,1974; roy and Fleagle, 1972). Cartmill and Milton Cartmill, 1974; Tuttle, 1975; Jungers, 1976; (1977) demonstrated that lorises have a re- Mendel, 1976; Stern et al., 1977; Fleagle et duced ulnar-carpal articulation as an adap- al., 1981; Jungers and Stern, 1980; Tuttle et tation to slow (cautious) climbing, leading al., 1979; Jungers and Susman, 1984). Stern them to hypothesize that the large body size et al. (1977) and Fleagle et al. (1981) showed of apes necessitated a similar cautious that muscles that are larger in apes were as climbing locomotion. Jenkins (1981) showed or more active in vertical climbing than in that Lewis’ supposition (1965, et seq.) that a brachiation, indicating that they may have lesser articulation between the styloid pro- been maintained as an adaptation to the cess of the ulna and the triquetral and pisi- former. Fleagle et al. (1981) maintained that form allowed wrist rotation was wrong, since shoulder mobility was an adaptation to wrist rotation occurs mostly in the midcarpal reaching up during climbing and concluded joint. that vertical climbing is responsible for Field studies of positional behavior did not many of the synapomorphies (including support a brachiation (sensu stricto) special- shoulder mobility) in the hominoid clade. ization in apes (Bingham, 1932; Donisthorpe, Most students of ape positional behavior 1958; Schaller, 1963; Schaller and Emlen, recognize that adaptation to suspensory pos- 1963; Nissen, 1931; Goodall, 1963; Kort- ture is significant in all apes (e.g., Fleagle, landt, 1962, 1968, 1974; Reynolds, 1965; 19881, yet its conflation with vertical climb- Carpenter, 1938; Schaller, 1961; Harrison, ing has obscured the extent of the adaptation 1962), although evidence from some chim- and perhaps overemphasized the importance panzee researchers was equivocal (e.g., Rey- of vertical climbing. Brachiation (sensu nolds and Reynolds, 1965; Goodall, 1968). To stricto), vertical climbing, unimanual arm- accommodate these data it was reasoned hanging, hoisting, clambering, amoebic that ape anatomy was adapted to behaviors suspensory locomotion, arm-swinging, and PAN TROGLODYTES POSITIONAL BEHAVIOR 85 transferring are distinct behaviors, one or 1954, 1957, 1963; Avis, 1962; Miller, 1932). several of which may be the behavior or Multivariate analysis of shoulder morphol- behaviors for which ape specializations were ogy places them in a cluster with other mon- evolved. Here quantitative data on the posi- keys, separated from apes (Corruccini and tional behavior of chimpanzees and baboons Ciochon, 1976). are compared in order to determine which mode(s) distinguish chimpanzees from Old Study group and sampling method World monkeys. Chimpanzees were observed for 571 hr at Mahale and 130 hr at Gombe. Here 14,866 METHODS instantaneous, 2-min focal observations Study sites (Altmann, 1974) on 26 well-habituated The Mahale Mountains and Gombe prime adults spanning all social ranks are Stream National Parks are located on the analyzed (see Hunt, 1989 for more detail). At shores of Lake Tanganyika, Tanzania the 2 min mark the target was instanta- (Nishida, 1968, Goodall, 1968). The principal neously sighted and values were recorded for differences between the two sites relate to 25 positional behavior variables (Hunt, the greater rainfall at Mahale (Hunt, 1989). 1989). Approximately equal numbers of ob- The Mahale M group range is characterized servations were made in wet and dry seasons by closed forest and vine tangles, whereas at (7,984 vs 6,882) and on males and females Gombe there is less vine tangle and forest (7,754 vs 7,112). Baboons at Gombe were and more open woodland (Collins and Mc- observed for 83 hr resulting in 2,087 obser- Grew, 1988). The greater forest floor cover at vations. Identical methods of data collection Mahale is the most remarkable difference were employed for both species. The baboon between the two sites (personal observa- home range was considerably smaller than tion). that of the chimpanzees and located near the center of the Kasekela community range. Choice of baboons as a comparative species An attempt was made not to observe the Even in closely related species with very same individual 2 days in a row in order to similar morphologies, greater body weight avoid potential positional bias associated limits saltatory locomotion [e.g., hylobatids with the collection of temporarily abundant (Carpenter, 1940; Chivers, 1972; Fleagle, fruit; of 147 chimpanzee follows, the same 1976b), galagos (Crompton, 1984), 7 Suri- individual was followed 2 days in a row 7 nam monkeys (Fleagle and Mittermeier, times. None was followed 3 days in a row. 1980), and 8 African forest monkeys (Rollin- Targets were discovered as early in the day son, 1975)l. Body weight is of particular as possible and followed for as long as possi- interest in ape studies since hominoid mor- ble or until they entered their night nest. phology and positional behavior have often Any purposeful decision to cease taking data been hypothesized to be adaptations to their was made at least an hour in advance, after greater weight (e.g., Keith, 1891, 1923; which no other data were taken in the same Miller, 1932; Napier, 1963a,b, 1967; Lewis, day. No data were recorded in feeding camp, 1965 et seq.; Ripley, 1970, 1976, 1979; Rose, in staff camp (Goodall, 19861, or while the 1973,1974;Cartmill, 1974).Among all living animals were mobile-provisioned (Nishida, nonhominoid primates only Mandrillus 1979). sphinx is closer in body size to the chimpanzee than the baboon is (Jungers, 1985). Nev- Data collected ertheless, baboons have typical cercopithe- cine anatomy, including restricted wrist The following variables are analyzed here: mobility, restricted shoulder mobility, a ventrally oriented glenoid fossa, a low inter- 1.Location in tree: the target was recorded membral index, fewer thoracic and more as being on the ground, in the terminal lumbar vertebrae, a narrow, barrel-shaped branches (i.e., any part of the target’s trunk (as opposed to cone-shaped) torso, and short within 1 m of the tree edge), or in the central manual digits with a large thumb (Jones, part of the tree (i.e., not within 1 m of the 1967; Benton, 1967, 1976; Corruccini and edge). Note that a separate measure was Ciochon, 1976; Lewis, 1972a; Swindler and kept for the size of the supporting structure Wood, 1973; Schultz, 1936,1937,1944,1953, (WBS); not all supports in the terminal 1956,1961,1963,1967,1969;Erikson, 1952, branches are small. 86 K.D. HUNT

2. Contact with WBS (weight-bearing reasoned were the best choice despite the structure) (typically recorded for posture fact that behavioral inertia may violate the only): it was noted which of the ischia, side, assumption that observations are indepen- belly, back, or four limbs were supporting a dent. The procedure used here is similar. To significant portion of the body weight. minimize the dependence between data 3. Locomotor or postural mode: in the points, somewhat artificial “bouts”were cre- course of study 65 different positional modes ated from instantaneous observations. The were observed; these were collapsed into 20 data were reduced by pooling sequential ob- positional modes presented in Appendix A. servations in which positional mode did not Note that climbing means vertical climbing change. Analytical variables were averaged and that brachiation means hand-over-hand over the series of sequential bouts, and the suspensory locomotion. resulting group of observations was consid- 4. Weight bearing structure (WBS) diame- ered a single observation or bout. For exam- ter: the diameter of the supporting structure ple, if there were 20 consecutive 2-min obser- that the hand(s) andlor footlfeet were touch- vations in which the same positional ing was estimated. If the sizes of WBS con- category (e.g., “sitting”)was observed, the 20 tacting the left and right cheiridia were sim- samples would be collapsed into one observa- ilar in size but distinguishable, the left and tion and analytical variables such as canopy right were averaged. If one was more than height, WBS size, and WBS angle would be approximately double the size of the other, averaged over the 20 observations, regard- the size of the WBS judged to be bearing the less of whether other variables changed. The most weight was recorded. Often the ischia artificial bouts were made up of a varying contacted a large diameter WBS and the feet number of observations from one to scores rested on smaller WBS; in such cases the (the mean number was 2.96). This collapsing diameter of the WBS of the body part(s) (feet or reduction produced a number of “bouts” versus ischia) bearing the most weight was that totalled approximately one third the recorded. When the WBS consisted of a num- number of observations in the raw data. ber of intertwined branches of small diame- Reduced data sets were used for all statis- ter it was recorded simply as “tangle;” such tical procedures (Fisher’s exact tests, x2 tests support was as stable as the largest WBS and Mann-Whitney U tests). There was no and was pooled with large WBS when appro- need to reduce climbing data, since these priate (Hunt, 1989). were continuous. Fisher’s exact tests were 5. Canopy level: height above the ground used when ossible since they are more accu- was estimated in meters. rate than xF tests on small samples (Gibbons, 6. Context or activity: 116 different behav- 1983); on larger samples Fisher’s exact val- iors associated with positional behavior were ues asymptotically approach x2 values (Gib- recorded. bons, 1983:120). Since Fisher’s exact tests give only P values, x2 values are presented. Continuous data were collected whenever More observations were made in the mid- a target animal was observed climbing, as dle hours of the day than early or late, a bias follows: that introduced significant distortion since chimpanzees exhibited a marked daily cycle 1. WBS diameter: recorded for each dis- (Hunt, 1989). Chimpanzees spent more time tinct climbing bout. feeding just after waking and in the last few 2. Angle of WBS: angle above horizontal. hours before entering their night beds than 3. Climbing mode: flexed-arm climb, ex- at other times of the day (comparison on data tended-arm climb, ladder climb, and pulse reduced on context: hours 07-08 compared to climb were recognized; see Appendix A for 09-14, Fisher’s exact test, P < .01; x2(1) = definitions. 4.9; hours 15-18 compared to hours 09-14, Fisher’s exact test, P< .0001; x2(1) = 68.8). Statistical method As a consequence raw measures underrepre- Observations only 2 min apart are present feeding positional behaviors. To com- sumably highly dependent due to what pensate for time-of-daybias, data were stan- might be called behavioral inertia, compli- dardized by hour of day for Table 1.Activities cating statistical analysis. Many positional were calculated by the hour and proportions studies have chosen to omit statistical test- from each hour were averaged over the typi- ing altogether. Cant (1987a,b) tested posi- cal 12- or 13-hr daily schedule. Such stan- tional differences with x2 tests, which he dardization precludes statistical analysis, PAN TROGLODYTES POSITIONAL BEHAVIOR 87 and is therefore used only for Table 1. Strat- ified data on Gombe chimpanzees were sus- pect in some cases due to small sample sizes. In these cases observations are presented for Mahale chimpanzees only. In cases where values are nearly identical between sites, data are pooled for comparisons with baboons. RESULTS Table 1 presents the composite positional schedules (i.e., standardized for hour of day) for the Mahale and Gombe chimpanzee pop- ulations based on 11,393 and 2,700 2-min instantaneous focal observations respec- tively. Gombe baboon figures are mid-sex averages (there were 1,113 and 937 observations on males and females) standardized by hour. Chimpanzees showed more variety in positional behavior than baboons. Standing, sitting, and walking made up nearly 95% of all baboon positional behaviors versus 79.2% in chimpanzees. Compared to baboons, chimpanzees sat more, lay more, arm- hung more (with and without support from the ischia and feet), palm-walked more, and vertical-climbed more, but stood (tripedal and quadrupedal standing pooled) less and walked less (all Fisher’s exact tests on pooled Gombe and Mahale data, P< .05, df = 1).

Positional variation by WBS diameter and -9u canopy location S .-..Au There were no significant differences in IR WBS size usage between baboons and chim- G panzees whether in feeding (Mann-Whitney -.I U test, U = 61,065, P = .16, n = 1117; see Table 2) or nonfeeding contexts (Mann- J Whitney U test, U = 15,636, P = 32, 2 n = 607. Nor did chimpanzees spend more time in the terminal branches (Fisher’s exact test, P = .70, x2 = .15 for Gombe; P = .61, x2 = .22 for Mahale; see Table 3) even though baboons spent significantly less time $2 in trees compared to sympatric chimpanzees mm (Fisher’s exact test, P< .0001; x2 = 38.6) and Mahale chimpanzees (Fisher’s exact test, P< .0001; x2 = 15.5). Whether measured by proximity to the edge of the tree (Table 4) or by WBS diameter (a more accurate measure of stability; see Table 5), positional behavior differed in chimpanzees according to the canopy structure. Sitting was the most common posture, regardless of WBS diameter. Unimanual arm-hanging both with and without support 88 K.D. HUNT

TABLE 2. Mean WBS diameter compared in chimpanzees and baboons Mean (cm) n SD Feeding Mahale chimpanzee 5.8 1,904 5.3 Gombe chimpanzee 6.3 692 5.5 Baboon 6.5 304 3.4 Nonfeeding Mahale chimpanzee 13.4 1,475 9.9 Gombe chimpanzee 10.8 275 6.5 Baboon 11.6 162 12.9

TABLE 3. Percentage of time in each stratum level compared in baboons and chimpanzees Study Terminal Cental Context mouu n branches tree Ground Feeding Baboon 851 11.3 27.6 61.1 Gombe chimp 1,140 14.8 54.2 31.0 Mahale chimp 3,972 16.8 40.0 43.2 Nonfeeding Baboon 997 0.7 17.3 82.0 Gombe chimp 1,554 0.6 41.8 57.6 Mahale chimp 6,192 1.9 27.0 71.1 All Baboon 2,082 5.2 22.6 72.2 Gombe chimp 3,056 6.0 46.8 47.2 Mahale chimp 11,896 7.1 32.2 60.7

TABLE 4. Percentage of each posture in Mahale adults by stratum level Posture Armhang Sit/ Armhang Location Sit (in) Sit (out) Stand Armhang w/support Lie Squat recline stand Terminal 30.7 28.4 2.2 7.1 15.5 9.5 1.9 0.4 3.2 branches (n = 749) Central tree 35.9 40.1 1.0 0.9 4.7 13.9 0.8 1.6 0.5 (n = 3,458) Ground 39.8 34.0 2.4 0.5 0.0 21.5 0.1 1.5 0.1 (n= 5,426)

from other parts of the body was more com- proximity to edge of tree and by WBS diam- mon among the smaller WBS [Fisher’s exact eter. Though sample sizes were small (only test, P< .0001; ~‘(1)= 93.6, n = 1,436; see 34 surveys in the terminal branches) vertical Table 51. Unimanual arm-hanging had the climbing, palm-walking (both observed sig- smallest mean and median WBS diameter of nificantly more than brachiation, Fisher’s all postures (Table 6; all contexts represent- exact test, P < .05 in both cases) and trans- ed), followed by arm-hang with support and ferring (but not significantly, P = .17, Fish- arm-hanglstand. These results are strong er’s exact test on reduced data) were the evidence that it was unimanual arm-hang- most common locomotor behaviors in the ing (all modes) that gave chimpanzees access terminal branches. Brachiation made up to the smallest, terminal branches. 8.8% of all locomotor behavior in the termi- Tables 7 and 8 present locomotor modes by nal branches and was observed in approximately the same frequency in the central parts of the tree (7.7%).Quadrupedal knuckle- ‘Suspensory modes in which half or more of the body weight depended on a fully abducted forelimb were pooled under the walking had the highest median WBS diam- label “arm-hanging(all modes).”“Arm-hanging“ means the entire eter, followed by climbing, palm-walking, body weight is suspended from one arm, whereas “arm-hanging with support”meansthat 50%+ is suspended from a forelimb, but and running. Transferring was observed on that some ofthe bodyweight is supported withotherbody contact. the smallest WBS (Table 8). PAN TROGLODYTES POSITIONAL BEHAVIOR 89

TABLE 5. Postural mode freauencies bv WBS size in Mahale adults Posture Substrate Armhang Sit/ Arm-hang diameter Sit (in) Sit (out) Stand Armhang w/support Lie Squat recline stand <3cm 35.0 36.9 2.2 2.3 16.9 2.0 1.5 0.3 1.9 (n = 976) 3-10 cm 36.9 48.0 0.8 0.2 5.4 5.0 1.0 1.4 0.7 (n = 1,328) > 10 cm 38.4 33.9 2.3 0.0 0.4 22.6 0.3 1.7 0.3 (n- 7.175)

TABLE 6. Mean and median substrate diameter by posture (Mahale only, all contexts)’ Posture Arm-hang Sit/ Arm-hang Sit (in) Sit (out) Stand Arm-hang w/support Lie Squat recline stand Mean (in cm) 9.7 7.1 11.2 2.6 3.5 47.6 4.4 11.2 3.9 n. 336_.. 581 42 76 257 530 16 49 43 SD 17.0 9.7 17.3 1.5 5.4 33.3 3.4 4.2 5.6 Median (in cm) 5.1 5.1 5.1 2.5 2.5 35.6 2.5 10.2 2.5 ‘Means and medians aregiven for the suhstratediameter contacting the feet, except for arm-hanging,for which only the hand(s) contacted the stratum.

TABLE 7. Locomotor mode frequencies by stratum location in Mahale adults Locomotion Quadrupedal Palmar Bipedal Location knuckle-walk Climb walk walk Brachiate Transfer Run Terminal 0.0 32.4 29.4 2.9 8.8 20.6 0.0 branches (n = 34) Central tree 6.3 54.5 24.5 1.4 7.7 1.4 0.7 (n - 143) Ground 98.6 0.1 0.1 0.1 0.0 0.0 0.8 (n = 1,557)

Locomotion in travel versus feeding tional behavior was postural (Gombe and Mahale data pooled, n = 5,038). Chimpan- Quadrupedal knuckle-walking was the zees fed 87.8% of the time when among the most common positional mode when moving terminal branches (Table 10; data from Ma- between feeding patches and when traveling hale chimpanzees only). Of unimanual arm- with no recognizable purpose (Table 9). In hanging 95.7% occurred during feeding contexts where individuals moved within a bouts. In other humerus-abducted arm- patch while feeding (“Feed in Table 91, hanging modes chimpanzees fed 89.4% and knuckle-walking was still the most common 84.6% of the time (Table 11). For arm-hang- locomotor mode, but palm-walking and ing (all modes), 90% of all observations were climbing were observed in high frequencies feeding. as well. Transferring was also more common Postural modes during food comsumption in feeding contexts. or harvesting are tabulated in Table 12 (rows sum to approximately 100%). “Small” fruit Positional behavior during feeding species are those in which the height of adult Of all feeding contexts (including moving trees was 4 15 m. No one postural mode within a feeding patch), 96.8% of all posi- appears to be specifically adapted to a nar- 90 K.D. HUNT

TABLE 8. Locomotor mode frequencies by WBS size in Mahale adults

Locomotion Quadrupedal Palmar Bipedal Location knuckle-walk Climb walk walk Brachiate Transfer Run <3cm 0.0 47.4 15.8 1.8 14.0 14.0 0.0 (n= 57) 3-10 cm 2.6 43.6 35.9 0.0 10.3 0.0 2.6 (n= 39) > 10 cm 95.1 2.5 1.2 0.0 0.1 0.0 0.9 (n= 1,615) Median 15.2(4) 7.6(84) 7.6(42) 5.1(2) 2.5(14) 1.3(8) 7.6(1) substrate size’ ‘Number of surveys in parentheses; tree observations only

TABLE 9. Locomotion in chimpanzees while feeding and while traveling Knuckle- Palm- Bip. Site Activitv n walk Climb walk walk Brachiate Transfer Mahale Feed 123 57.7 13.0 21.1 1.6 4.1 2.4 Travel 1,055 98.6 0.9 0.1 0.0 0.2 0.1 Gombe Feed 34 58.8 11.8 20.6 5.9 0.0 2.9 Travel 333 98.5 0.6 0.6 0.0 0.0 0.0

TABLE 10. Percentage of contexts for chimpanzees by stratum level (Mahale only)‘ Context Move Groom between Move in Location n Feed Rest male Groom2 Looks uatches uatch Travel Terminal 763 87.8 5.1 0.8 1.2 0.8 0.5 1.2 0.0 branches Central 3,197 49.9 23.6 4.8 11.5 2.3 0.7 0.7 0.0 tree Tree 3,960 57.2 20.1 4.0 9.6 2.0 0.6 0.8 0.0 Ground 6,161 28.3 17.8 10.4 13.1 2.5 10.3 0.9 7.6 All 10,203 40.6 18.6 7.8 11.8 2.3 6.5 0.9 4.6 1PVPld ‘Not all contexts included does not sum to 100%. %eludes females, estrus females, juveniles, unidentified individuals, and autogrooming 31ncludes cases where there are no data on type of location within the tree.

row range of food items, but several trends more readily available and sit (in) and sit are apparent. “Sit (in)” was the preferred (out) postures constituted approximately posture while harvesting and eating stems of equal percentages (21.4 vs 21.9%). Suspen- Pennisetum purpureum, perhaps because it sory postures were used most often when is difficult to extend the legs among the feeding on fruit. Unimanual arm-hanging closely set grasses. The “sit (out)” posture (without support) was most often used when was used most often when eating fruit in feeding on fruit in large trees, whereas uni- small trees. This posture appeared to be manual arm-hanging with support was used particularly stable among small WBS be- most often when feeding on fruit in small cause it increased diameter of the base of trees. It seemed that large trees were less support by distributing weight over several likely to have tangles of interwoven vines or branches. In larger trees large WBS were twigs that could be grasped with the feet PAN TROGLODYTES POSITIONAL BEHAVIOR 91

TABLE 11. Percentage of activities for chimpanzees by posture (sites pooledil Context Groom Posture n Feed Rest Male Groom2 Looks Infant Care Sit (in) 3,682 55.6 11.3 7.6 12.2 4.2 3.7 Sit (out) 3,918 50.9 12.8 9.0 18.2 2.4 3.4 Stand3 186 34.4 3.2 4.8 5.9 16.1 1.1 Arm-hang 93 95.7 0.0 0.0 0.0 1.1 0.0 Arm-hang 358 89.4 2.2 0.8 1.4 1.1 1.1 w/support Lie 2,108 5.1 75.9 6.5 7.5 0.8 1.7 Arm-hang 52 84.6 0.0 0.0 0.0 0.0 1.9 /Stand

~~ 'Not all contexts included; does not sum to 100%. 21ncludesfemales, estrus females, juveniles, unidentified individuals, and autogrooming. %sten, make nest, and rest in travel make up most of the rest of the contexts in this posture.

when hanging, and were more likely to have angled WBS. If such means were not avail- isolated branches so that arm-hanging able chimpanzees vertical-climbed small (without support) was the only possible pos- (2-10 cm) vertical WBS, e.g., vines or adja- ture among the smallest strata. cent small trees. Only if no large gently Although lying was not a common feeding angled or small vertical WBS were available posture, when chimpanzees fed while lying did chimpanzees climb large trunks. Over the food item was most often fruit or insects. 85% of chimpanzee climbing bouts were on Sometimes chimpanzees carried a branch WBS 10 cm or smaller (Table 13; see also laden with fruit to a day nest or large trunk Fig. 1). where they could lie, or fed lethargically on Two aspects of chimpanzee vertical climb- nearby fruit while lying in a day bed. While ing are worth emphasizing. First, chimpan- ant fishing individuals often lay to get closer zees did not fully abduct their humerus when to the anting aperture or to provide a stable climbing small, subvertical WBS, although position while leaving both hands free. when climbing graded into arm-hanging, the Squatting was observed often on vertical final reach before suspension often involved and subvertical (i.e., near-vertical) WBS. abduction. Second, the kinematics of baboon The WBS was grasped with the feet and the and chimpanzee vertical climbing differed upper body was stabilized with an arm. Fruit little. When climbing small WSthe torso found in small trees was harvested most was held subvertical, angled forward so that often by squatting, perhaps because the the shoulders were closer than the hips to trunk itself was the largest and most stable the WBS. Such a position appeared to bal- perch from which to feed. ance the upper body so that propulsive force from the legs did not cause backward rota- Vertical climbing tion. The arms assisted in elevating the body Chimpanzees climbed significantly more through flexure of the forearm and retrac- often than baboons [Fisher's exact test; tion (extension) of the humerus. The elbow P < .03; x2(1) = 3.7; Table 11, though the was completely extended only very rarely difference was small (0.9 versus 0.5%). The when climbing small diameter WBS, re- different frequencies of climbing may have maining partly flexed even as the arm was been due to different strategies for ascending raised above the head to its maximum ex- tree's. Baboons often ascended by alternately tent. The elbow was elevated to perhaps 10 leaping and walking on slightly angled WBS, cm above the shoulder at most; the humerus whereas chimpanzees used less saltatory lo- was protracted (flexed) rather than ab- comotor modes. ducted. That is, when elevated the humerus Ad lib observations suggested that chim- was held approximately parallel to the sagit- panzees preferentially entered trees by tal plane. A similar kinematic has been de- knuckle-walking on gently angled (< 45") scribed in a laboratory setting (Larson and large WBS (i.e., 15 + cm), or by palm-walk- Stern, 1986). Despite the fact that baboons ing on somewhat smaller (5-15 cm) gently were not observed to fully abduct their hu- 92 K.D. HUNT meri, and indeed seemed incapable of it, flexed-arm climbing made up a substantial part of their climbing repertoire (Table 14). The mechanics of chimpanzee climbing were different on larger WBS. The chimpanzee foot can grasp a WBS of up to 10 cm in diameter with a power grip, but WBS substantially larger cannot be easily grasped (personal observation). On large diameter WBS an extended elbow climbing was evinced wherein a “leaning back gestalt increased the friction between the tree trunk and the pes (Cartmill, 1974; Jungers, 1976; Jungers et al., 1982; Jungers and Susman, 1984). In such instances flexure of the forearm provided little or no propulsive force; extension of the spinal column and the hindlimbs and retraction of the humerus instead appeared to provide the climbing power. Stride length was extremely short; hands and feet were raised perhaps 10-50 cm at a time. This mode of climbing will be referred to as extended-arm climbing. The extended-arm or large-trunk-climbing 9 “2 9 0“2 hypothesis predicts that chimpanzees climb 0 0 0 larger WBS than baboons, a difference that should be pronounced given the larger body size of chimpanzees. Here there was no significant difference between chimpanzee (pooled Gombe and Mahale data) and baboon WBS diameters while climbing (Mann- Whitney U test, U = 5163.5, P = .08). Ex- tended-arm climbing (see Table 14; Fig. 2) was observed in chimpanzees almost exclusively on WBS greater than 10 cm in diameter. Baboons showed a similar trend. Among 9 baboons the extended elbow orientation was evinced during “pulse climbing,” which was observed more often on large diameter WBS, whereas flexed-arm (hand-over-hand) climbing was associated with smaller WBS. Although baboons ascended by walking and leaping more often than chimpanzees, on extremely large vertical WBS both species used a type of climbing in which the elbow was completely extended.

DISCUSSION Assessing the impact of positional behavior Positional mode frequencies are an important consideration in assessing the evolutionary origin of positional anatomy. The more frequent a positional behavior, the greater the need for reinforcing the locomotor apparatus against positional-mode-specific injury and wear; the greater the need for shaping skeleton and muscle to prevent fa- PAN TROGLODYTES POSITIONAL BEHAVIOR 93

TABLE 13. Percentage of climbing bouts by WBS diameter WBS diameter in cm L Site n and less >2-4 >4-6 >6-8 >8-10 >lo-20 >20 Mahale 101 9.9 40.6 27.7 6.9 3.0 9.9 2.0 Gombe 88 18.2 35.2 11.4 11.4 9.1 6.8 8.0

E 40 0 .-+ U L 30 0" L 0 8 20 :a 2

Fig. 1. Size of WBS in climbing compared in chim- is quite similar in the two species. Neither species panzees and baboons. Note that the size of WBS climbed climbed strata larger than 20 cm frequently.

tigue; and the greater the opportunity for determined (Kay and Cartmill, 1977; Kay, energy conservation if it is made more effi- 1984). In other words, the distinctiveness of cient. If the frequencies of various positional the mode must be considered. Furthermore, modes were the sole consideration in assess- the muscular effort required for a positional ing positional adaptations, one would con- mode and the associated stress in the muscu- clude that sitting is the most important posi- loskeletal system determine the anatomical tional behavior among chimpanzees (Table adaptations required to allow it. Frequency, 11, and other positional behaviors, in order of distinctiveness and physical stress must be decreasing importance could be said to be (2) considered together. That is, links can confi- quadrupedal knuckle-walking, (3) lying, (4) dently be made between specific anatomical unimanual arm-hanging (all modes), (5) features and specific behaviors with a three- standing, (6) climbing, (7) squatting, and (8) part protocol. First, the frequency of the palm-walking (other modes made up less behavior must be known in a representative than 0.5% each). Such an approach is clearly sample of wild subjects; second, the distinc- inappropriate. Certainly the frequency of a tiveness of the behavior relative to other positional mode is an important selective species must be demonstrated; and third, the force, but frequencies must be considered in physical stress involved must be established. comparison with other species to assess a Although the frequency of various positional morphological adaptation. Only by isolating modes was estimated rather accurately for a particular feature among species that also chimpanzees (Table l), measuring stress show a common behavior can function be and distinctiveness is problematical. As a 94 K.D. HUNT

TABLE 14. Percentage of climbing twe bv WBS diameter WBS diameter in cm Climbing 2 Site type and less >2-4 >4-6 X-8 >8- 10 >lo-20 >20 Mahale Palmar-walk 0.0 2.7 3.7 28.6 0.0 10.0 0.0 chimp Knuckle-walk 0.0 0.0 0.0 0.0 0.0 10.0 0.0 Flexed 100.0 97.3 96.3 57.1 100.0 50.0 0.0 Extended 0.0 0.0 0.0 14.3 0.0 30.0 100.0 Gombe Palm-walk 6.3 7.1 0.0 20.0 0.0 20.0 14.3 chimp Knuckle-walk 0.0 0.0 12.5 0.0 0.0 40.0 0.0 Flexed 87.5 92.9 87.5 80.0 100.0 Extended 0.0 0.0 0.0 0.0 0.0 Baboon Walk 9.1 18.8 14.3 33.3 33.3 Leap 18.2 12.5 14.3 0.0 0.0 Flexed 63.6 37.5 28.6 16.7 33.3 0.0 0.0 Pulse 9.1 31.3 42.9 50.0 33.3 60.0 100.0

e .-0

0d ,M 0 J

Fig. 2. Flexedvs extendedarmclimbingcompared by in more detail in Table 14. Note that extended arm size of supporting stratum. Data for this figure are given climbing is rare on substrates 10 cm and smaller.

first approximation, these latter factors are Jungers and Stern, 1980; Stern and Susman, estimated as follows. 1981; Stern et al., 1980), such information cannot be used to estimate physical stress Physical stress when evolutionary issues are involved. Al- though high EMG activity in particularly Although information derived from EMG large muscles does indicate great muscle, study had been an important tool for explain- ligament, and bone stress, this simple asso- ing muscle function (Basamajian, 1965, ciation is complicated by the assumption 1972; MacConnaill and Basmajian, 1969; that natural selection shapes the anatomy to Basmajian and Bazant, 1959; Basmajian reduce both muscular activity and structural and Stecko, 1963; Basmajian and Tuttle, stress in proportion to the frequency of the 1973; Tuttle and Basmajian, 1974a,b,c; Tut- behavior (Basmajian, 1965; MacConnail and tle et al., 1972; Stern et al., 1977, 1980; Basmajian, 1969; Cartmill et al., 1987). Po- Susman and Stern, 1979;.Tuttle et al., 1979; sitional behaviors for which animals are well PAN TROGLODYTES POSITIONAL BEHAVIOR 95 adapted are expected to produce less muscle vided by the percentage ofthe same behavior activity and less stress in the skeleton and in baboons; data from Table 1).Lying, for ligaments than behaviors for which the ani- example, was 3.8 times more common in mal is poorly adapted. For example, during chimpanzees than baboons. Actual figures arm-swinging EMG potentials of some mus- are given for cases where the frequency of cles are higher in a poorer brachiator (woolly the behavior was < 0.1% for baboons. Modes monkey) than a better brachiator (spider that were equal or more frequent in baboons monkey; Stern et al., 1977). Furthermore, cannot be considered to be distinctive chim- joints evolve so that in posture ligamentous panzee behaviors. Proportions are ranked in and skeletal elements, not muscles, bear column 3. The difference between chimpan- body weight (Basmajian, 1965, 1972; Bas- zees and baboons in the percentages of each majian and Bazant, 1959; Basmajian and behavioral mode are presented in column 4. Greenlaw, 1968; Basmajian and Stecko, Column 5 (difference rank) ranks the behav- 1963; Cartmill et al., 1987). Theoretically, iors in order from most distinctive to least the more common the positional mode the distinctive. greater the selective pressure to evolve this Proportions and differences are each esti- muscle sparing function. The consequence of mates of the distinctiveness of positional this evolutionary response is that compari- modes in chimpanzees, but each has its bi- sons between species should follow the ases. Distinctiveness rank based on propor- rather counterintuitive rule that less muscle tion may overrepresent rare behaviors when activity accompanies behaviors for which an values are extremely low (e.g., 0.5 versus animal is particularly well adapted. In as- 0.1% gives a proportion of 5, but the values sessing which of two (or more) equally com- are so low that they may be insignificant mon positional modes should be accompa- nevertheless). Ranks based on differences nied by the greatest anatomical adaptations, may overemphasize the distinctiveness of the force applied to the WBS is the critical common behaviors (e.g., the difference be- datum, rather than muscle activity or even tween 55 and 40% is greater than the differ- stresses in the skeleton of any particular ence between 10 and 0%, but is it more species. The latter can vary dramatically significant?). To moderate these biases dis- even in similar sized animals; the former tinctiveness will be assessed using the aver- must remain relatively constant regardless age rank of both methods (column 6, Table of how well adapted the animal is for the 151, and only for values that are significantly behavior. different. Of the 5 behaviors that are statis- As a preliminary method, force applied to tically more common in chimpanzees, the the WBS for common chimpanzee positional most distinctive to least distinctive are (1) modes was crudely estimated as high, me- lie, (2) unimanual arm-hang (all modes), (3) dium, or low. Climbing was considered to sit (in), (4)vertical climb, and (5) palm-walk. entail high stress since it involves acceleration directly against gravity. Running and Interpreting frequency, stress, and leaping were considered to entail high stress distinctiveness by virtue of their rapid acceleration. Other To estimate the relative selective force modes of locomotion were considered to have exerted by each positional mode on the chim- median force rankings (brachiating, walk- panzee locomotor apparatus, the combina- ing, palm-walking, and bipedal walking). tion of frequency, stress, and distinctiveness Postures (sitting, lying, unimanual arm- must be considered together. The aim is to hanging, standing, squatting, clinging, and assess the likely importance of each posi- bipedal standing) were assumed to involve tional mode in the evolution of distinctive low stress. chimpanzee morphological features. Below, each mode is discussed in order of highest to Assessing distinctiveness lowest frequency. Discussion is summarized Distinctiveness was quantified by compar- in Table 16. ing chimpanzee positional frequencies to Sitting was the most common positional those of baboons. In Table 15 five positional behavior in chimpanzees, constituting over modes that were significantly more common 61% of their waking behavior (none of the in chimpanzees than in baboons are bold data presented includes lying in a night faced. The proportion of chimpanzee to ba- nest). It was significantly more common in boon percentages is presented in column 2 chimpanzees than baboons [Mahale and (percentage of the chimpanzee behavior di- Gombe observations pooled, Fisher’s exact 96 K.D. HUNT

TABLE 15. Distinctiveness of chimpanzee positional behaviors Positional Chimp/baboon Proportion Chimp-baboon Difference Average behavior orouortion rank' difference (in %) rank rank2 Arm-hang3 4.4/0 4.4 2 Lie3 3.8 8.9 1.5 Climb3 1.8 0.4 4 Squat 1.4 0.2 5.5 Sit (in)3 1.3 5.9 3.5 Palm-walk3 0.6/0 0.6 5 Bipedal stand 0.3/0 0.3 6.5 susp. loco. 0.210 0.2 7.5 Bipedal walk 0.1/0 0.1 9 Cling 1.0 0.0 - Sit (out) 0.98 -0.6 - Walk 0.68 -7.5 - Run 0.75 -0.1 - Leap 0/0.2 -0.2 - Stand 0.17 -12.5 - 'For cases where the baboon figure is 0.0, the proportion is taken to be the percent of expression in chimpanzees 2Proportion and difference ranks averaged. 3Positional modes in bold face are significantly more common in chimpanzees (P< .05; Fisher's exact test).

TABLE 16. Distinctiveness, frequency, and stress for Although posture made up over 80% of all chimpanzee positional modes chimpanzee positional behavior, knuckle- Positional Average Stress walking was the second most common posi- behavior distinctiveness Frequency category tional mode (15.7%).Although the knuckle- Sit (out) - 0.340 Low walking mode of the African apes is unique Sit (in) 3.5 0.284 Low among the primates, related morphological Walk - 0.160 Medium adaptations are expected to be limited to the Lie 1.5 0.121 Low Arm-hang 2 0.044 Low manus and carpus, since selective pressures Stand - 0.025 Low on other parts of the positional apparatus Climb 4 0.009 High are presumably substantially similar to Squat 5.5 0.007 Low those in other primates. Whereas the knuck- Palm-walk 5 0.006 Medium ling aspect of chimpanzee walking is distinc- Bipedal stand 6.5 0.003 LOW Run - 0.003 High tive, walking was significantly more com- Cling - 0.003 Low mon in baboons [Fisher's exact test, P< Suspensory 7.5 0.001 Medium .0001; ~'(1)= 22.11, indicating that walking Bipedal walk 9 0.001 Medium may have less profound morphological implications for chimpanzees than for baboons and other monkeys. Quadrupedal walking is the most common locomotor mode in a number of primates [e.g.,Presbytis obscura (Flea- test, P <.0001; x2(1) = 15.01, and was third gle, 1980), Saguinus midas, Saimiri sci- in average distinctiveness rank. As a pos- ureus, Chiropotes satanas, Cebus apella, and ture, however, it falls in the lowest of the 3 Alouatta seniculus (Fleagle and Mitter- tiered stress estimations presented above, meier, 1980)l and is very common in some and therefore probably presents little selec- other primates [Galago crassicaudatus tive pressure in the form of injury. Further- (Crompton, 19841, Saguinus oedipus (Gar- more, it is similarly common in other Old ber, 1984),Alouatta seniculus (SchonYbarra World primates for which there are quanti- and Schon, 1987), and Colobus guereza tative positional information (Rose, 1974, (Rose, 197811. Evidence that knuckling is 1977, 1978; Morbeck, 1977; Fleagle, 1978). responsible for many characteristics of the Despite its high frequency and relatively wrist and hand shared by the African apes high distinctiveness in chimpanzees, the low (Tuttle, 1965, et seq.) is supported, but walk- stress involved in sitting makes it unlikely to ing per se cannot be the behavior €or which have been an important behavior in the evo- characteristic ape features are evolved since lution of distinctive chimpanzee anatomical quadrupedal walking is less common in hy- traits. lobatids (Chivers, 1972; Fleagle, 197613, PAN TROGLODYTES POSITIONAL BEHAVIOR 97 1980; Srikosamatara, 1984) and orangutans behavior; it was significantly more common (MacKinnon, 1974; Galdikas, 1978, 1979; in chimpanzees than in baboons [Fisher’s Sugardjito, 1982; Sugardjito and van Hooff, exact test, P < .03; ~‘(1)= 3.71. It is the sec- 1986; Rodman, 1984; Cant, 1987a,b) than ond most common chimpanzee locomotor are other behaviors previously proposed to mode and the sixth most common positional be responsible for ape (“brachiating”)charac- behavior. It had an average distinctiveness teristics (Hunt, 1991). rank of 4. It was placed in the highest stress Lying was the third most common chim- category. Its high stress and distinctiveness panzee positional mode; its frequency was support previous work postulating that this significantly higher in chimpanzees than in behavior is responsible for some chimpanzee baboons [Fisher’s exact test, P < .0001; specializations (Fleagle et al., 1981). There ~‘(1)= 40.11 and its average distinctiveness is, however, little support for the large-WBS- rank was highest of any positional mode. climbing hypothesis or for the contention However, in lying the weight of the body is that vertical climbing selected for ape hum- distributed over large areas, reducing stress era1 abduction abilities. Climbing WBS di- on any one body part. Adaptations for main- ameters and kinematics were not signifi- taining anatomical integrity during locomo- cantly different between chimpanzees and tion are likely to have preadapted the body baboons. Vertical climbing constituted less for such a relatively nonstressful behavior. than 1%of the total positional repertoire, Lying requires little muscular activity to and extended-arm climbing made up only stabilize or balance the body and thus selec- 6.6% of that. It is possible, however, that tion to improve efficiency is probably unim- extended-arm climbing might be a more portant. Despite its high frequency and high common positional mode in other habitats, distinctiveness, the low stress involved in since Gombe and Mahale habitats had few lying (presumably the lowest of all positional emergents (Collins and McGrew, 1988), and behaviors observed) argues against its hav- therefore few resources that could not be ing been an important selective force for harvested by climbing smaller trees or vines creating or maintaining the distinctive as- instead of large central trunks. Data pre- pects of chimpanzee morphology. sented here, however, indicate that extended Arm-hanging with support [Fisher’s exact arm climbing is not a distinctive aspect of the test, P< .0001; ~‘(1)= 34.71, unimanud arm- chimpanzee positional repertoire. hanging [Fisher’s exact test, P<.0001; ~‘(1)= The frequency of squatting was 0.7% com- 15.71, and arm-handstanding [Fisher exact pared to 0.2% in baboons (Table 1). Its aver- test, P < .005; ~‘(1)=5.31 were each signifi- age distinctiveness rank was 5.5, or sixth of cantly more common in chimpanzees (sites all positional behaviors. Its stress category pooled) than baboons. Pooled arm-hanging was low. Considering its low stress, low fre- modes, each of which was characterized by a quency, and relatively low distinctiveness, fully abducted humerus, constituted 4.4% of its evolutionary significance for chimpanzee all positional behavior, the fourth most com- anatomy is probably low as well. mon positional mode. The average distinc- Palm-walking (0.6%) was significantly tiveness rank of arm-hanging (all modes) more common in chimpanzees than in ba- was very high (second only to lying). Unlike boons [Fisher’s exact test, P < .002; ~‘(1)= sitting and lying, arm-hanging was both a 10.01. It had an average distinctiveness rank distinctive chimpanzee posture and a behav- of 5 (fifth) and a stress estimation of me- ior with physical demands unlike those of dium. This behavior was different from other postional behaviors. It is likely to have knuckle-walking in the orientation of the associated physical adaptations that distin- manus (the long axis of which appeared to be guish chimpanzees from baboons, and, in- rather perpendicular to the direction of deed, from all Old World monkeys for which movement, requiring that the wrist be supi- there are quantitative data (Rose, 1974, nated), in the extent of dorsiflexion of the 1977,1978; Morbeck, 1977; Fleagle, 1978). manus and in the volar contact with the Standing constituted 2.5%of all positional WBS. The medium stress rank and high behavior. Chimpanzees spent much less distinctiveness rank are evidence that adap- time standing than baboons [sites pooled; tations to this mode may be greater than Fisher’s exact test, P < .0001; ~‘(1)= 344.71; those for squatting, but less than those for standing therefore cannot be responsible for knuckling, arm-hanging (all modes), and chimpanzee specializations. climbing. More intensive study of the orien- Climbing constituted 0.9% of all positional tation of the manus during this locomotion 98 K.D. HUNT and of the stresses in the carpus and manus modes) rose the most of any posture as WBS is warranted. size decreased (Table 5). Arm-hanging (all Bipedal standing, clinging, and running modes) was seen in the context of feeding each was observed in chimpanzees 0.3% of more than any other posture. This evidence the time. Although bipedal standing re- strongly supports the hypothesis that sus- quired supporting the substantial weight of pensory behavior is an adaptation to har- the upper body against gqavity, its low fre- vesting fruits in the terminal branches and quency and relatively low distinctiveness that suspension helps to retain positional argue against it being an important chim- competence on small-diameter WBS despite panzee adaptation. Clinging and running the larger body size of chimpanzees com- were not distinctive in chimpanzees (see Ta- pared to monkeys. ble 15). Of all locomotor modes, vertical climbing, Brachiation constituted 0.1% of all posi- brachiation, and transferring were the most tional behavior. It is pooled with other hu- common among the smallest WBS. Small merus-abducted suspensory locomotion sample sizes make conclusionstentative, but (transferring, dropping, clambering, and it appears that climbing and transferring are arm-swinging), together termed “suspenso- preferred over brachiation among small ry locomotion.”This pooled mode constituted WBS. These results conflict with the conten- 0.2%of all positional behavior. Its average tion that brachiation (sensu stricto) provides distinctiveness rank was 7.5 (eighth) and its increased competence or efficiency among stress was medium. Suspensory behaviors small diameter WBS. necessitate suspending the body by one or Consideration of the frequency, stress, both arms with the scapula rotated and the and distinctiveness of each positional mode humerus abducted. Although the frequency in chimpanzees permits a ranking of behav- of suspensory behaviors was low, the suspen- iors with respect to selective force on mor- sion of the body weight from a single forelimb phology. Of the common chimpanzee posi- may exert great stress on the shoulder and tional behaviors, the high frequency and this mode may, therefore, have some evolu- distinctiveness of knuckling argue for a tionary consequences. strong adaptive response in the wrist and Bipedal walking is the least common of the hand, but knuckling cannot explain the most categories here presented. Its distinctive- distinctive morphology of chimpanzees and ness is low and stress is medium. Its rarity other hominoids. Lying and sitting produce argues against any significant anatomical too little stress to have important adapta- adaptations. tions. Other positional behaviors are re- garded as less important either because they CONCLUSIONS are not distinctive or not common. After The first functional discussion of the posi- lying and sitting (sit in), arm-hanging (all tional adaptation of apes emphasized the modes) was the most distinctive positional impact that large body size had on mobility behavior of chimpanzees. Although its stress within the canopy (e.g., Avis, 1962; Rose, was categorized as low, its high frequency 1974,1978; Ripley, 1967; 1970,1979; Grand, and high distinctiveness argue for substan- 1972,1984). The small size of available WBS tial morphological adaptations. Although in the most productive areas of fruiting trees vertical climbing was observed at low fre- was seen as the most significant evolution- quency in chimpanzees and was consider- ary pressure selecting for suspensory loco- ably less distinctive than arm-hanging, it motion. Data reported here support the sus- was in the highest stress category. Vertical pensory (as opposed to locomotor) aspect of climbing, however, was kinematically simi- this paradigm. There were, however, no sig- lar in baboons and chimpanzees, whereas nificant differences in mean WBS diameter arm-hanging was unlike any behavior ob- between baboons and chimpanzees, indicat- served in baboons, since it often involved ing that chimpanzees may not have a greater complete humeral abduction. competence on small WBS. Nevertheless, Data presented here suggest that arm- chimpanzees used suspensory postures in hanging (all modes) and climbing are the two much greater frequency among the smallest behaviors that most distinguish chimpanzees WBS, and arm-hanging had the smallest from baboons, and presumably from other average and median WBS of all feeding pos- monkeys as well. Functional anatomists tures. The proportion of arm-hanging (all should pay particularly close attention to PAN TROGLODYTES POSITIONAL BEHAVIOR 99 chimpanzee morphological complexes that In Tuttle RH (ed.): The Functional and Evolutionary are expressly involved in these two behav- Biology of Primates. Chicago: Aldine, pp. 292-304. Basmajian JV,and Bazant JV (1959)Factors preventing iors. downward dislocation of the adducted shoulder joint: An electromyographic and morphological study. J. ACKNOWLEDGMENTS Bone Joint Surg. 41-A:1182-1186. Comments by anonymous reviewers, M.G. Basmajian JV,and Greenlaw RK (1968) Electromyogra- phy of iliacus and psoas with inserted fine wire elec- Hunt, A. Kramer, F.B. Livingstone, G.L. Sul- trodes. Anat. Rec. 160:310-311. livan, V.J. Vitzthum, D.P. Watts, and L.A. Basmajian JV,and Stecko G (1963) Role of muscles in Yaroch, benefitted this manuscript greatly. arch support ofthe foot. J. Bone Joint Surg. 45A31184- J. Warner provided critical statistical ad- 1190. vice. J. Goodall and T. Nishida generously Basmajian JV,and Tuttle RH (1973)EMG of locomotion in gorilla and man. In Stein RB, Pearson KB, Smith welcomed me at their field sites. C. Boehm, RS, and Redford JB (eds.): Control of Posture and D.A. Collins, N. James, K. Kawanaka, S. Locomotion. London: Plenum, pp. 599-609. Kobayashi, K. and M. Masui, T. Pandit, and Benton RS (1967) Morphological evidence for adapta- H. and K. Takasaki aided me in the field. I tions within the epaxial region of the primates. In thank Acting Director E. Massawe of the Vagtborg H (ed.): The Baboon inMedical Research, Vol 2. Austin: Univ. Texas Press: pp. 201-216. Mahale Mountains Wildlife Research Cen- Benton RS (1976) Structural patterns in the Pongidae ter, the staffs of the MMWRC and the Gombe and Cercopithecidae. Yearbook Phys. Anthropol. Stream Research Center, M. Bunengwe, A. 18:65-88. Madaraka, H. Bunengwe, R. Nyundo, R. Bingham HC (1932) Gorillas in a Native Habitat. Carn- Olomi, D. Gilageza, and H. Katinkila for egie Institute Publication. Cant JGH (1986) Locomotion and feeding postures of crucial logistical help. I am grateful to the spider and howling monkeys: Field study and evolu- Tanzania Scientific Research Council, the tionary interpretation. Folia Primatol. 46:l-14. Serengeti Wildlife Research Institute, K. Cant JGH (1987a)Positional behavior of female Bornean Hirji, the village of Mugambo, and to the orangutans (Pongopygmaeus).Am J. Primatol. 12:71- generous people of the Socialist Republic of 90. Cant JGH (1987b) Effects of sexual dimorphism in body Tanzania for their hospitality during my size of feeding postural behavior of Sumatran orangu- field work. R.W. Wrangham and C.L. Brace tans (Pongo pygmaeus). Am J. Phys. Anthropol. provided important criticism of research at 74:143-148. every stage. Research was aided by grants Carpenter CR (1938) A survey of wild life conditions in from the Margaret Wray French Fund, Atjeh, North Sumatra, with special reference to the orangutan. Netherlands Committee for International Sigma Xi, the Leakey Foundation, the Uni- Nature Protection. 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Yearbook Phys. Anthropol. i. Sit (in): sitting with the weight sup- 20:498-507. ported by the ischia and one or two legs, of Stern JT Jr, Wells JP, Jungers WL, Vangor AK, and which the hip and knee were tightly flexed so Fleagle JG (1980) An electromyographic study of the that the heel(s) were near or touching the Pectoralis Major in Atelines and Hylobates, with spe- ischia and dorsal aspect of the thigh. The feet cial reference to the evolution of a Pars Clavicularis. Am. J. Phys. Anthropol. 52:13-25. were judged to have borne an amount of the Sugardjito J (1982)Locomotor behavior of the Sumatran weight roughly proportional to that borne by orangutan Pongo pygmaeus abelii at Ketambe, the ischia. The trunk was orthograde. Gunung Leuser National Park. Malay Nat. J. 35.57- ii. Sit (out): sitting with the legs extended, 64. that is, the feet “out” so that the ischia bore Sugardjito J, and van Hooff JARAM (1986)Age-sex class most of the body weight. The feet were used differences in the positional behavior of the Sumartan orang-utan Pongo pygmaeus abelii in the Gunung mainly for balance, and did not appear to Leuser National Park, Indonesia. 47(1):14-25. bear much more than their own weight. Sit! Susman RL (1979)Comparative and functional morphol- recline was included in this category; it was a PAN TROGLODYTES POSITIONAL BEHAVIOR 103 type of sitting in which the ischia bore most arm-hanging. Arm-hanglstand was a rare of the weight, but the elbow, back, stomach, posture and was subsumed under this mode. side, or some part of the forelimbs may have It is a combination of suspension by the been in contact with the supporting stratum. arm(s), with the humerus completely ab- This mode is made up mostly of a torso- ducted, and bipedal standing, with the knee orthograde posture similar to that of a per- and hip extended and weight borne equally son sitting in a chair. by the forelimb(s) and the feet. The trunk iii. Cling: this posture was observed on was almost always orthograde. The hand- vertical or subvertical strata. One or two foot hang typical in orangutans (trunk hori- hands grasped the WBS, the elbow(s) was zontal; Cant, 1987a,b) was rare in chimpan- (were) flexed, the humerus was adducted zees and was subsumed under this mode. and the torso was held at or near an or- viii. Lie: reclining on a relatively horizon- thograde orientation. The feet may or may tal WBS with the body weigh borne by the not have grasped the substratum, but sup- back, side, or stomach. Occasionally the ani- ported a proportional part of the body mal grasped a supporting WBS, but it was weight. The ischia bore none of the body judged that the limb involved bore little weight. Rarely, two separate horizontal more than its own weight. Often, however, branches were used in clinging, or the hands when lying on a side individuals supported grasped a horizontal branch while the feet the upper body by an elbow resting on the contacted a vertical support. lower stratum, usually the ground. iv. Stand: posture on 3 or 4 limbs on a ix. Squat: the body weight was borne by relatively horizontal supporting stratum. the feet, with both the hip and the knee The elbow and knee were typically extended strongly flexed. The arms bore less than a and the trunk was close to horizontal (pro- proportional amount or none of the body nograde). Crouch was rare (< 1%of all behav- weight. The trunk was vertical. ior) and was subsumed under standing; in x. Quadrupedal knuckle-walk: locomotion this behavior the individual stood quadrupe- characterized by the common primate diago- dally on a relatively flat stratum with the nal couplet (Hildebrand, 1967; Larson and elbows flexed. Rarely the knees also were Stern, 1987). Forelimbs contacted the WBS slightly flexed. via the knuckles and the feet either rested on v. Bipedal stand: posture on the two hind- the volar skin or grasped a WBS. Crutching limbs with no significant support from any (a rare behavior constituting < 0.1% of all other body part. The torso was typically held locomotion) was also included in this mode. at a 45" angle, and was rarely completely This was a terrestrial knuckling locomotion orthograde. where the adducted forelimbs moved for- vi. Arm-hang:unimanual suspension with ward in concert, the elbow completely or no other part of the body contacting a WBS. almost completely extended. After planting The humerus was abducted and the elbow the forelimbs the body and the hindlimbs are was complete extended. The trunk was or- swung though the arms. Crutching was seen thograde. almost exclusively in the descent of ex- vii. Arm-hang with support (AHsupp): tremely steep hills. hanging with what was judged to be approx- xi. Climb: ascending and descending loco- imately half of the body weight suspended motion on WBS at greater than a 45" angle. from one forelimb and the other half sup- This mode refers to vertical climbing only. ported by some combination of the ischia, The kinematics of the mode described here feet (with hindlimbs flexed), side, back or are depictedinFleagle et al. (1981, Fig. 5). Of (rarely) the elbow of the contralateral arm. the modes Fleagle (197613) included in qua- Rarely one arm was observed to be com- drumanous climbing, only that depicted in pletely abducted whereas the other forelimb Figure 4 falls into this category. Other be- was used in a manner similar to that seen in haviors that might be labeled quadruman- clinging, that is, with the humerus adducted ous climbing were categorized as walking and the forearm flexed. In these rare cases (Fleagle, 197613, Fig. 3), suspensory locomo- whether the animal was scored as arm-hang- tion (other than brachiation, e.g., amoebic ing or clinging depended upon which arm locomotion; Fleagle, 1976b, Fig. 2), arm- appeared to be bearing the most weight. The swinging, transferring, clambering (sensu humerus was less often completely abducted Cant, 1987a), and scrambling. In the most in this tpe of posture than in unimanual common type of vertical climbing a hindlimb 104 K.D. HUNT and its contralateral forelimb provided pro- ducting it with the arms and legs, after pulsion. The arms helped to elevate the body which the animal allowed its body to descend by the retraction of the humerus and flexion by sliding. Sometimes the arms regulated of forearm. This flexion is noted in calling the velocity of the descent with a hand-over- this mode of locomotion flexed-arm climbing. hand movement. In flexed-arm climbing the elbow rarely rose xii. Quadrupedal palm-walk: locomotion more than approximately 10 cm above the similar to knuckle-walking, except that the shoulder, and the humerus was typically forelimbs contacted the WBS by the volar protracted, (i.e., overhead anterior reach, surface. This behavior was similar to Fleagle Larson and Stern, 1986) in the process of (1976b, Fig. 3). Chimpanzees supinated and reaching upward, not abducted. The torso partly dorsiflexed the wrist so that a larger was held nearly parallel to the WBS being portion of the volar area contacted the WBS. climbed. When descending there was more Occasionally the thumb was recruited to pro- abduction of the arm than was common in duce a power grip. The term scrambling was ascension. A variation on flexed-arm climb- used to describe nonsuspensory quadrupe- ing was observed on horizontal WBS, or dal progression without a regular gait and tangles of small twigs. This type of climbing with grasping cheirideal contact. This type of was very similar to the movement of a person locomotion was seen on small andlor ex- climbing a ladder. It was similar to flexed- tremely irregular WBS, especially in the ter- arm climbing and the two modes were pooled minal branches of trees. Progression was for this analysis. On large WBS (> 20 cm) a primarily horizontal. The torso was typically different type of climbing was observed. The held fairly pronograde, unlike the largely elbow was extended and the WBS was suspensory clambering mode common in or- gripped by the entire volar surface of the angutans, in which the torso was held verti- hand, including palm and fingers, and the cal and progression was assisted by the hind- retraction of the arm appeared to provide limbs (Cant, 1987a,b). Scrambling was rare very little of the force needed to elevate the in chimpanzees and the mode was subsumed body. Instead, retraction of the humerus and under palm-walking. extension of the hindlimbs provided most of xiii. Bipedal walk: only the hindlimbs the propulsive power. This mode of climbing were used in locomotion. In most cases bipe- is considered in more detail above, where it is dalism was characterized by hip and knee analyzed separately from other types of flexion but still involving a stride of perhaps climbing. For most analyses, however, it was 0.25 m. Although bipedal running was seen pooled with other climbing behaviors. Two rather often during adult male social dis- other extremely rare behaviors kinemati- play, it was never sampled. cally similar to hand-over-hand climbing xiv. Run: the hand and wrist bore weight were included in this mode; namely, “pull- in a knuckled orientation, while the volar up’’ (hauling or hoisting) and “pulse climb- surface of the foot contacted the WBS. A ing” or bear climbing (MacKinnon, 1974; this period of free flight was observed. mode was observed only in baboons in this xv. Brachiate : hand-over-hand orthograde study). In a pull-up a branch, usually hori- suspensory locomotion was virtually no con- zontal, was grasped by both hands in an tribution by the hindlimbs in support or arm-hanging posture and the body was lifted locomotion. In chimpanzees this behavior by retraction of the humerus and flexion of was typically slow and without a period of the forearm. In pulse climbing the forelimbs free flight. The swing phase ended with both grasped the WBS and the hindlimbs were arms contacting the superstratum approxi- gathered underneath the body by flexure of mately a meter apart briefly after which the the knee, hip, and spine, the legs and back trailing grip was released and a pendulum- were extended pushing the body upward, like swing began. In almost all cases the while the forelimbs simultaneously and in humerus was completely abducted and the unison reached upward to grasp a higher elbow was completely extended. When the handhold. This motion has a pulsing appear- term brachiation is used, only this hand- ance as the animal ascends the vertical or over-hand suspensory locomotion is meant. subvertical WBS. Pooled also with climbing xvi. Leap: the flexed hindlimbs and spine is a rare mode (< 0.1% of all behavior) la- were forcefully extended to propel the ani- beled firepole slide, wherein a vertical WBS, mal into a period of free flight. Hop described usually very large, was grasped by circum- a bipedal progression where both feet PAN TROGLODYTES POSITIONAL BEHAVIOR 105 pushed off roughly simultaneously followed zontal WBS. From this pose the torso de- by a period of free flight; it was rare and was scended, remaining orthograde, so that the subsumed under leaping. Included in this individual swung under the branch that had mode is a rare (i.e., < 0.1% of all behavior) been near the waist. Transferring most often “dropping” locomotion where the animal began with arm-hanging, followed by a lunge leapt with little force, or dropped, and caught to grasp an adjacent small branch. The itself on a lower stratum with the forelimbs, branch was pulled toward the animal with a after which a period of suspensory locomo- hand-over-foot motion, and weight was grad- tion or posture was commonly seen. The ually transferred to the new WBS. Unlike suspensory aspect of the behavior was re- brachiation this locomotion was irregular; it corded as such and included in the next often involved support or partial suspension category. from the hindlimbs. “Riding,” a behavior xvii. “Other suspensory locomotion” was similar to tree swaying, was subsumed un- used as a catch-all suspensory category that der this category as well. In this mode of included a number of kinematically similar locomotion a vertical, small-diameter tree locomotor modes in which there was full was grasped in a clinging posture and a humeral abduction, but which could not be violent movement was used to overbalance called brachiation (sensu stricto). This mode it. The weight of the animal’s body pulled the is pooled with brachiation in Table 1 under tree from a vertical orientation toward hori- the label “miscellaneous suspensory be- zontal. As the tree approached horizontal a havior.” Among these behaviors were arm- suspensory posture resulted, after or during swinging, transferring, “riding,”and “amoe- which the grip with the hindlimb was re- bic” locomotion (sensu Kortlandt, 1974). leased and the feet contacted some lower Arm-swinging is used to denote a mode in WBS, usually the ground. “Amoebic”locomo- which both hands release a WBS at the same tion, also included in the “misc. susp.” cate- time after briefly swinging under it. Often gory, was a suspensory movement among both grasp another WBS nearly simulta- very small WBS whereby changing contact neously as well, In chimpanzees a typical points and shifting weight effected a slow bout began with the elbows extended, the movement without a distinct locomotor bout. arms adducted, and the hands near the hips This behavior is perhaps analogous to Cart- bearing most of the weight on a single hori- mill and Milton’s (1977) cautious climbing.