AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 86521-536 (1991)

Mechanical Implications of Chimpanzee Positional Behavior

KEVIN D. HUNT Department of Anthropology, Indiana University, Bloomington, Indiana 47405 KEY WORDS -hanging, Vertical climbing, Brachiation, Hu- meral abduction, Suspensory behavior

ABSTRACT Mechanical hypotheses concerning the function of chimpan- zee anatomical specializations are examined in light of recent positional behavior data. Arm-hanging was the only common chimpanzee positional behavior that required full abduction of the , and vertical climbing was the only distinctive chimpanzee positional behavior that required forceful retraction of the humerus and flexion of the . Some elements of the chimpanzee anatomy, including an abductible humerus, a broad thorax, a cone-shaped , and a long, narrow , are hypothesized to be a coadapted functional complex that reduces muscle action and structural fatigue during arm-hanging. Large muscles that retract the humerus (latissi- mus dorsi and probably sternocostal pectoralis major and posterior deltoid) and flex the elbow (biceps brachii, probably brachialis and brachioradialis) are argued to be adaptations to vertical climbing alone. A large ulnar excursion of the manus and long, curved metacarpals and phalanges are interpreted as adaptations to gripping vertical weight-bearing structures during vertical climbing and arm-hanging.A short torso, an iliac origin of the latissimus dorsi, and large muscles for arm-raising (caudal serratus, teres minor, cranial trapezius, and probably anterior deltoid and clavicular pectoralis major) are interpreted as adaptations to both climbing and unimanual suspension.

Apes share a distinctive anatomy, most motion (Keith, 1891,1899,1923;Avis, 1962). notably long forelimbs (fingers included), Muscles particularly large or distinctively mobile , distinctively wide, shal- shaped in apes were reasoned to be espe- low, short , and no tail (Keith, 1891, cially important as brachiating propulsors 1899,1903,1923; Schultz, 1930,1936,1953; (Keith, 1891; Miller, 1932; Campbell, 1937; Washburn, 1950; Erikson, 1963). Myologi- Inman et al., 1944; Ashton and Oxnard, cally they are distinguished by large muscles l963,1964a, b; Erikson, 1963; Oxnard, 1963; that flex the elbow, retract the humerus, and Corruccini and Ciochon, 1976). The wide raise the arm (Ashton and Oxnard, 1963, thorax and the accompanying relocation of 1964a; Napier, 1963; Oxnard, 1963, 1967; the scapula to a more dorsal position on the Ashton et al., 1965; Tuttle, 1969b). Keith thorax hypothetically oriented the scapulo- (1891, 1899, 1903) proposed that such ana- humeral joint laterally, increasing the ex- tomical specializations in gibbons were ad- cursion of the humerus by removing the aptations to brachiation; others extended chest wall as a barrier (Miller, 1932; Avis, the hypothesis to all apes (Gregory, 1916, 1962).A long, narrow scapula’ was hypothe- 1928,1934; Morton, 1922,1926; Frey, 1923; Miller, 1932; Midlo, 1934; reviewed in Tut- tle, 1974; Andrews and Groves, 1976). ‘Mediolaterally reduced and axially elongated The distance The short lumbar region (Schultz, 1936) between the glenoid fossa and the angle of the superior vertebral and high intermembral index of apes were border is small compared to the distance from either the glenoid interpreted as aspects of an overall reduction fossa or the angle of the vertebral border to the inferior angle of the scapula. of body parts not active (or disadvantageous: - Hildebrand, 1974) during suspensory loco- Received October 8,1990; accepted June 4,1991.

@ 1991 WILEY-LISS,INC. 522 K.D. HUNT sized as serving to increase the mechanical Quadrumanous climbing was offered as a advantage of trapezius and serratus anterior more universal hominoid behavior than bra- during the scapular rotation necessary for chiation (Washburn, 1968,1973;Conroy and arm-raising (Ashton and Oxnard, 1963, Fleagle, 1972; Fleagle, 1976; Cartmill and 1964a; Oxnard, 1963,1967).Reduced articu- Milton, 1977; Fleagle et al., 1981). Such a lation between the ulna and the carpus and a reassessment was more a nomenclatural neomorphic ball and socket-like joint be- clarification than an advance in understand- tween the radius and the ulna (Midlo, 1934; ing since brachiation (sensu lato) had come Lewis, 1965 et seq.) compared to Old World to encompass essentially the same behaviors monkeys (Benton, 1967; Jones, 1967; Jen- proposed for quadrumanous climbing; i.e., kins, 1973; O’Connor, 1975, 1976) were in- suspensory locomotion, suspensory posture, terpreted as adaptations to wrist rotation vertical climbing, and walking on inclined or during brachiation. small-diameter weight-bearing structure(s) Although widely accepted, many of these (WBS) (Washburn, 1968,1973; Cant, 1986). hypotheses were simplistic or incorrect. Bra- Two developments refined the climbing chiation (sensu stricto)2 was rarely observed hypothesis, changing its focus and giving it a in naturalistic studies of great apes; instead, powerful theoretical orientation. The first terrestrial knuckle-walking dominated Afri- was the functional linking of high intermem- can ape behavior (reviewed in Tuttle, 1986; bra1 indices and vertical climbing. Long Yerkes and Yerkes, 1929). The carpus and were hypothesized as functioning to metacarpus of chimpanzees and gorillas re- increase friction between the tree bole and flect this adaptation in being less flexible the pes, allowing apes to ascend larger WBS and more reinforced compared to orangu- than monkeys (Kortlandt, 1968, 1974; Cart- tans and gibbons (Tuttle,l965,1969a,c; Jen- mill, 1974; Jungers, 1976; Mendel, 1976; kins and Fleagle, 1975). Knuckle-walking, Stern et al., 1977; Fleagle et al., 1981; however, cannot explain most ape synapo- Jungers and Stern, 1980, 1981, 1984; morphies since it differs from the terrestrial Jungers and Susman, 1984; Sarmiento, quadrupedalism of other princi- 1987). The second was electromyography pally in the orientation of the wrist and (EMG) research, demonstrating that many manus, suggesting that specializations muscles particularly large in apes were more should be limited to those structures, since active during vertical climbing than during quadrupedalism is no more common among knuckle-walking or brachiation (Miller, apes than most other primates (Feldesman, 1932; Inman et al., 1944; Ashton and Ox- 1982; Tuttle, 1986; Hunt, 1991a). nard, 1963, 1964a,b; Oxnard, 1963; Fleagle, Whereas Lewis (1965 et seq.) maintained 1974, 1977; Corruccini and Ciochon, 1976; that distal displacement of the pisiform and Tuttle et al., 1972; Tuttle and Basmajian, a reduced ulnar-triquetral articulation were 1974a,b,c, 1977, 1978a,b; Stern et al., 1977; evolved to allow extensive wrist rotation Susman and Stern, 1979; Jungers and Stern, during brachiation (sensu stricto), the gib- 1980; Swindler and Wood, 1982; Larson and bon, the preeminent brachiator, was shown Stern, 1986,1987). It appeared that the more to have the least mobile wrist of all apes restricted mode, vertical climbing, as op- (Conroy and Fleagle, 1972). Furthermore, posed to the more general quadrumanous “brachiating” characters were observed in climbing, could be the behavior for which ape lorises (Cartmill and Milton, 1977), indicat- synapomorphies were evolved, since it (hy- ing that a flexible wrist may be an adapta- pothetically) necessitated mobility tion to slow (= quadrumanous) climbing (in reaching up for a new handhold), elon- rather than brachiation. Jenkins (1981) gated forelimbs (for climbing large trunks), showed that in fact the articulation between and ape muscular specializations, all “bra- the styloid process of the ulna and the trique- chiating” hallmarks (Stern et al., 1977, tral and pisiform had little to do with wrist 1980a,b; Fleagle et al., 1981). rotation, which occurs mostly in the midcar- Although it was not clearly reconcilable pal joint. with this interpretation, it remained obvious to these researchers and others that sus- pensory posture also was an important as- ‘The term brachiation (sensu stricto) means hand-over-hand pect of the ape positional behavior and must suspensory locomotion, with or without a period of free flight, as have accompanying anatomical adaptations opposed to a more liberal usage (sensu lato). Iticochetal brachia- tion is reserved for gibbon-like brachiation with a period of free (Ellefson, 1968,1974; Chivers, 1972; Andrews flight. and Groves, 1976; Fleagle, 1976, 1988; Git- CHIMPANZEE BIOMECHANICS 523 tins, 1983; Srikosamatara, 1984; Sabater Pi, tween the torso and the arm bear the body 1979; Susman et al., 1980; Sugardjito, 1982; weight they create bending forces on the ribs Hollihn, 1984; Kano and Mulavwa, 1984; and tensile stress on vertebrocostal liga- Susman, 1984; Fleagle and Kay, 1985; Sug- ments, ultimately resulting in fatigue (Bas- ardjito and van Hooff, 1986; Cant, 1987a,b; majian, 1965; MacConnaill and Basmajian, Fleagle, 1988; Hunt 1989a,b,l990,1991a,b). 1969). EMG research demonstrated that the digital Here, mechanical hypotheses explaining flexors were virtually the only active mus- chimpanzee anatomical specializations (many cles during a~-m-hanging.~This implies sig- of which are shared by all apes) are exam- nificant skeletal and ligamentous (but not ined in the context of chimpanzee positional muscular) adaptations (ibid.) to arm-hang- behavior data (Hunt, 1991b). An attempt is ing to assure that body weight is borne by made to follow the tenet that anatomy skeleton, ligaments, intramuscular septa, evolves to reduce muscular demand and and/or passive muscular tension (Tuttle and strain in and ligaments during common Basmajian, 197413, 1977, 1978a,b; Tuttle positional behaviors, thereby reducing fa- et al., 1977, 1983; Preuschoft and Demes, tigue and conserving energy (Basmajian, 1984; Hollihn, 1984). 1965; MacConnaill and Basmajian, 1969; Recent data on chimpanzees suggests that Cartmill et al., 1987). Some chimpanzee spe- arm-hanging and vertical climbing are the cializations are discussed as possible adap- most distinctive chimpanzee positional tations to unimanual arm-hanging, includ- modes; arm-hanging was reasoned to influ- ing the following: broad manubrium of the ence upper body anatomy more because it is sternum, ventrally placed vertebral column, kinematically different in chimpanzees and shallow, wide, cone-shaped torso (Schultz, Old World monkeys, whereas vertical climb- 1930, 1936, 19611, narrow ~capula,~crani- ing is not (Hunt, 1991b). ally oriented glenoid fossa, ulnocarpal disso- Arm-hanging has several unusual me- ciation, and long, curved fingers. chanical requirements. Whereas most pos- tures typically exert compressive forces on MATERIALS AND METHODS skeletal elements, unimanual arm-hanging Observations were made on chimpanzees places the supporting limb in net tension at the Mahale Mountains (571 hours of ob- (Stern and Oxnard, 1973), a situation for servations) and Gombe Stream (130 hours) which the mammalian body plan (and indeed National Parks, Tanzania, resulting in bone itself) is poorly adapted. Unlike, for 16,303 instantaneous, two-minute focal ob- example, standing, during suspension the servations (Altmann, 1974)on 26 well habit- body weight must be supported by a grip, uated prime adults spanning all social which requires powerful and long-lasting ranks. Observations were made throughout muscle action. The majority of the body the ranges of the respective community unit weight is suspended beneath an eccentri- groups at all hours chimpanzees were active cally placed forelimb and borne by the gleno- (see Hunt, 1989b, 1991b, for more detail). At humeral joint capsule. The humerus, ad- the two-minute mark the animal was instan- ducted and attached to the body via a rather taneously sighted and positional mode, an- ventrolaterally facing glenoid fossa in most gle that supporting WBS made with the mammals, must be completely abducted. horizontal, WBS diameter, and grip type (as During arm-hanging a ventrolateral orien- applicable) were recorded for each cheirid- tation of the glenoid fossa potentially causes ium and/or the ischia (Hunt, 1989b). Other the caudal aspect of the joint capsule to be quantitative results are reported elsewhere much tauter than other parts, differentially (Hunt, 1989b, 1991b). straining it. Because the shoulder is lateral to both the spinal column and the point RESULTS AND DISCUSSION normally directly over the center of gravity, Manus and carpus the vertebral column must bend as the body settles under the shoulder. Body weight cre- Chimpanzee rays 11-V are elongated and ates shear stress between the shoulder and have a marked ventral curvature (Jones, the spine in the sagittal plane. When the bony, ligamentous, and muscular links be- 4The contention that such dimensions increase leverage for a muscular couple to rotate the scapula during arm-raising (Inman et al., 1944; Oxnard, 1963, 1967; Erikson, 1963; Ashton and 'Unless otherwise indicated arm-hanging refers to unimanual Oxnard, 1963, 1964a) has been disproved (Larson and Stern, suspension. 1986; Larson et al., 1991). 524 K.D. HUNT

TABLE 1. WBS diameters during posture by grip type Power' Hook2 Diagonal3 Palm4 Knuckle5 Rest6 Elbow7 Median (cm) 2.5 2.5 2.5 5.1 10.2 10.2 5.1 Mean (cm) 4.5 4.7 2.6 7.8 10.3 11.7 9.0 Range 0.6-45.7 0.6-40.6 0.6-15.2 1.3-63.5 2.5-50.1 1.3-25.4 2.5-35.6 S.D. 4.8 5.4 3.1 7.4 8.4 8.8 8.7 N 183 767 114 334 64 98 47 'Thumb or thenar eminence involved in grip, WBS relatively perpendicular to long axis of cheiridium. 2Fingers only or fingers and distal palm only involved in grip of WBS relatively perpendicular to long axis of cheiridium 3Similar to hook except WBS crosses palm/fingers diagonally. 'Palm only contacts WBS. 5Sensu Tuttle (1974). "Some part of cheiridium or distal limb touching WBS but bearing little weight. 'Weight borne on the process.

1942; Straus, 1940, 1949; Schultz, 1927, the adductible wrist in chimpanzees, that it 1930,1956; Susman, 1979). Long fingers are allows the hand to clear the WBS in knuckle- generally presumed to be an adaptation for walking (Conroy and Fleagle, 19721, is dis- gripping larger diameter WBS during either proved (Jenkins and Fleagle, 1975). Since suspension (Preuschoft and Demes, 1984) or the limit of ulnar deviation occurs with con- climbing. If the former, one would expect the tact between the styloid process of the ulna diameter of a typical WBS from which a and the carpus (Tuttle, l965,1969b, c),ulno- chimpanzee suspends itself to be larger than carpal dissociation may be an adaptation to that which a typical hand might retain a large range of ulnar deviation in a circumduct. Yet, most ecological hypotheses wrist generally adapted for stabilization. U1- (e.g.,Avis, 1962; Grand, 1972) purport sus- nar deviation may be necessary during arm- pensory behavior to be an adaptation to hanging and vertical climbing. small, terminal branch milieus, a perspec- Of those positional modes that require tive strongly supported in naturalistic stud- strong digital flexion to support the body ies of orangutans (Cant, 1987a,b) and chim- weight (arm-hanging, arm-hanging with panzees (of all postures in chimpanzees, support, clinging, vertical climbing, and sus- arm-hanging occurs on the smallest WBS; pensory locomotion) only arm-hanging (all Hunt, 1991b). The hook grip, a common sus- modes = 4.4%) and vertical climbing (0.9%) pensory grip, was used on WBS with a me- constitute >0.3% of chimpanzee positional dian diameter of only 2.5 cm (Table l),and behavior (Table 2; Hunt, 1991b). Both arm- over 96% of all WBS were smaller than 6.5 hanging (>19% of WBS were within 30" of cm. Long fingers might be argued to be true vertical, Table 3) and vertical climbing merely a pleiotropic or linkage effect of selec- (88%of WBS were within 30" of true vertical, tion for elongated arms; if so, fingers should Table 3) commonly involve supporting a sig- be equal to or shorter than the remainder of nificant portion of the body weight by grip- the forelimb in relation to some other body ping subvertical WBS. Because the part. In relation to trunk height chimpanzee is near vertical during these behaviors, it fingers are relatively even longer than their approaches being parallel to the WBS. If the arms, whereas among other hominoids the wrist cannot be adducted, the fingers will be same is true only for orangutans (Schultz, parallel to the WBS and therefore unable to 1936: Figs. 15,16).Such elongation suggests grip it. The more nearly parallel the fingers that some positive selective force maintains are to the WBS, the larger is its effective digit length. diameter, and the longer fingers must be to The chimpanzee wrist exhibits extensive circumduct it. For example, when the long volar flexion, whereas the range of ulnar axis of the hand makes an angle of 45" with a deviation is great but not remarkably so vertical WBS the effective diameter of the (Tuttle, l965,1969b, c; Jenkins and Fleagle, branch is 40% greater than when the hand is 1975; Sarmiento, 1988). Radial and dorsal perpendicular to the WBS. The ability to mobility are rather severely restricted (radi- ulnar-deviate the wrist therefore is particu- al more so), presumably to stabilize the wrist larly valuable for animals that grip vertical during forceful retraction of the arm during branches. quadrupedal knuckle-walking (ibid.). Per- Two aspects of climbing work to reduce haps the only specific explanation offered for weight depending on the carpus and pes TABLE 2. ChimDanzee oositional behavior’ Arm- AH Bip. Knuckle- Vertical Susp. Palm- Bip. Sit (in)2 Sit Lie4 hang5 (supp)6 Stand7 Squats Cling9 Standlo walk” climb12 Run13 Leap’4 10~0.~~walk16 walkI7 28.4 34.0 12.1 0.8 3.6 2.5 0.7 0.3 0.3 15.7 0.9 0.3 0.0 0.2 0.6 0.1

1 Derived from 16,303instantaneous observations of focalindividuals,standardized for hour of day; Gombe and Mabale figures averaged. Positional mode descriptions given in detail in Hunt, 1991b. Values expressed as percentages of each behavior. *Sitting with knees and flexed. 3Sitting knees and hips extended. ‘On side, back, or stomach. sUnimanual suspension with no other support. 6Arm-hanging (with support): more than half the body weight suspended from a manus; some support from lower limbs or ischia. ’Quadrupedal or tripedal posture, trunk pronograde. *Weight solely on fully flexed hindlimbs. 4Support from adducted, retracted, flexed forelimbs and fully flexed hindlimb. IOBipedal stand: support from hindlimbs with knees extended, hips partly or wholly extended. “Sensu Tuttle (1974). I2Hand over hand ascension or descension on WBS angled at >45O; propulsion provided by hind limbs and forelimbs. I3With a period of free flight. “Saltatory locomotion with propulsion provided by extension of the spine and hind limbs. L5Suspensorylocomotion: brachiation, transferring, riding, tree swaying, “amoebic” movement, arm-swinging that involved suspensory locomotion with a fully abducted humerus. ‘6Walking with the manus contacting the WBS by the palm, with the manus supinated, and dorsiflexed. I7Bipedal walk locomotion involving propulsion solely by the hind limbs. 526 K.D. HUNT

TABLE 3. Angle' of WBS contacting manus by positional behavior mode (arboreal observations only)

Positional Weight bearing stratum angle behavior2 xo-900 >30-60° 530' Bent to vertical Crook Sit (in) (413) 11.6 3.6 77.7 3.4 3.6 Sit (out) (719) 8.4 6.5 78.6 2.8 3.8 Sit3 (68) 0.0 8.8 44.1 0.0 47.1 Lie (585) 0.0 2.3 88.0 1.2 8.5 Arm-hang (83) 19.3 3.6 60.2 16.9 0.0 AH (supp.) (307) 21.5 7.1 60.9 10.4 0.0 AH (stand)4(45) 35.6 17.8 28.8 15.6 0.0 Stand (60) 6.7 10.0 63.4 18.3 1.7 Sauat (2% 20.7 0.0 62.0 17.2 0.0 Cling (31 j 77.4 9.7 9.7 0.0 3.2 Knuckle-walk (13) 0.0 15.4 69.2 0.0 0.0 Vertical climb (93) 88.2 9.7 0.0 2.2 0.0 Brachiate5 (14) 0.0 14.2 78.5 7.1 0.0 Palm-walk (43) 2.3 16.3 76.8 4.7 0.0

'Degrees from true horizontal, i.e., 90' = vertical. Angles are for the manus only; angles for the pes are often different. If both hands contacted the same WBS and angles were similar one value was recorded. 'Number of observations in parentheses. "Posture similar to sitting in a chair. Pooled with sit (out) in Table 2. 'Lower limbs provided support in a fashion similar to that in bipedal posture. Pooled with AH (supp.) in Table 2. 5Hand-over-handsuspensory locomotion. Pooled with suspensory locomotion in Table 2.

when the forearm is parallel to the WBS. First, not all weight depends on a forelimb during vertical climbing, since the contralat- era1 pes is recruited to support and propulse the body weight. Second, the forearm is near parallel to the WBS only at the beginning of the propulsive stroke. During unimanual arm-hanging the entire body weight depends on the manus, and the forearm is always Human Chimpanzee parallel to a vertical WBS. Among chimpan- zees suspensory behavior occurred among Fig. 1. Gripping in humans and chimpanzees. Note terminal branches on WBS with median di- that with curved phalanges a more uniform distance is ameters of 2.5 cm (n = 376; Hunt, 1991b). maintained between bone (black bars) and a gripped vertical WBS (stippled area) than with straight phalan- This diameter branch is small enough that it ges. In a straight-fingered individual pressure on the is often bent to near vertical from the weight WBS is higher near the middle of the phalanx where the of the animal (Grand, 1972; Hunt, 1991b), bone is closer to the WBS, whereas in a curved-finger which in turn increases its effective diame- individual pressure is more uniformly applied along the length ofthe digit. Note that with curved phalanges even ter so that it may require longer fingers and though the distance between bone and WBS remains the an adductible wrist. same (arrows)a larger WBS may be gripped. Ray curvature in the apes parallels degree of arboreality and frequency of suspen- sory activity (Susman, 1979; Hunt, 1991a). Sarmiento (1988) showed that ray curvature volar skin upward, thus creating radial tor- serves a muscle-sparing function during sus- sion in the volar tissue, which may fatigue pensory behavior. Ventral curvature may or damage tissue during sustained arm- also be an adaptation to distributing grip- hanging. Straight phalanges put much of the ping force more evenly around the circumfer- pressure of a strong grip on a relatively small ence of vertical WBS and thereby reducing surface area of volar tissue near the middle tissue strain. The weight of the body, when of the phalanx, whereas other tissue is rela- supported by a single manus in arm-hang- tively unstressed (Fig. 1).Curved phalanges ing, tends to pull digital and palmar tissue maintain a constant distance between the contacting the WBS in an upward direction, phalanx and the WBS along the entire volar or radially. The body weight pulls the pha- aspect of the finger, thereby assuring similar langes downward while the WBS pulls the pressures along the length of the digit. Be- CHIMPANZEE BIOMECHANICS 527

Chimpanzee

Monkey

Fig. 2. Schematic transverse section of and (Fc). Even when body weights are equal [i.e., chimpanzee torsos. The vertebral column is represented F ,m) = F I making the tension in the arms equal at the top, the sternum at the bottom. Because the I#,,,,, = ~~h~,,l,the forces compressing the torso are is lateral to the center of gravity (C,) the greater in the monkey than in the chimpanzee force of gravity (F,) and the counteracting force of the LF,,,, > F,,,,]. anchored arm (Fah)tend to create forces compressing the

cause a greater surface area bears weight, out its length, it is constricted most superi- the maximum strain on midphalangeal tis- orly, both in coronal and sagittal section sue is reduced and torsional strain is reduced (Erikson, 1963; Schultz, 1961). This gives as well. the rib cage a rather cone-shaped appear- Ventrally curved phalanges also allow fin- ance compared to the more barrel-shaped gers of a given length to circumduct larger appearance in monkeys. Perhaps the most WBS. With straight phalanges, bone near widely accepted explanation for a broad tho- the middle of the phalanx approximates the rax is that it separates the shoulders and WBS more closely than does that near the orients the glenoid fossae laterally, thereby joints (Fig. 1).This proximity limits the size increasing the span of the arms and allowing of the WBS a finger can circumduct. Curved circumduction of larger tree trunks when phalanges have this area of bone “moved” climbing (Cartmill and Milton, 1977); how- farther from the WBS. When human and ever, large-WBS-vertical-climbing is rare chimpanzee fingers circumduct a WBS so among Mahale and Gombe chimpanzees that the fingertip touches the palm, the cir- (Hunt, 1991b), suggesting that selection to cumference spanned by the curved digit is maximize mechanical efficiency for it may be greater (Fig. 1). Although gripping larger insignificant. WBS may be rare, a rather simple modifica- This feature may be an adaptation to arm- tion that allows it may be advantageous, and hanging. Stresses on the torso during arm- such an adaptation may be necessary for hanging may be viewed in the transverse gripping more commonly encountered, mod- and the sagittal planes in order to examine erately sized WBS that are subvertical. the influence of shape on tissue strain. Be- This line of reasoning suggests that long, cause the shoulder joint is lateral to the curved rays and an adductible wrist may be a center of gravity during arm-hanging (Fig. 2: functionally related adaptation to strongly transverse section) there is a lateral compo- gripping vertical or subvertical WBS during nent to the forces acting on the rib cage, and arm-hanging and vertical climbing, posi- as a consequence the torso is stressed as if tional behaviors hypothesized to exert the the shoulderjoint were being pulled laterally strongest selective pressure on the chimpan- against the force of the body weight, stress- zee positional apparatus (Hunt, 1991b). ing the torso dorsoventrally (i.e., causing the sternum and spinal column to be pressed Thorax together). The greater the anteroposterior Although the chimpanzee thorax is con- diameter of the torso, the greater is this stricted dorsoventrally(i.e., shallow)through- force. 528 K.D. HUNT t t 'ah(m)

convex ---)

Chimpanzee

Fig. 3. Schematic side view of monkey and chimpan- [i.e.,F,,,, = F ,,,J the forces compressing the torso are zee torsos (sagittalsection). Note that the force ofgravity greater in &e deeper (i.e., monkeydike) torso (F,) and the counteracting force of the anchored arm IF,,,, > F,,,J. Note also that the convex area of the (F& create forces compressing the rib cage (FJ that are monkey torso is subjected to compressive stress by ten- greater the greater the distance between the anchor sion in structures that attach to the humerus. points on the torso. Even when body weights are equal

A similar situation applies in the sagittal and large WBS vertical climbing are respon- plane. When the arm is raised above the sible for shoulder mobility or intermembral head, the muscles of the shoulder, the scap- proportions in orangutans (Cant, 1987a,b) ula, and the are oriented in a tent- and chimpanzees (Hunt, 1989a,b, 1991a,b). like configuration (Fig. 3). The anchors of the Among chimpanzees vertical climbing in- tent are the thoracohumeral muscles, the volved little humeral abduction (Hunt, sternoclavicular joint, the scapulohumeral 1989a, 1991b), and arm-hanging (all modes = muscles, and the scapula (attached to the 4.4%) was the only behavior with a frequency torso in part by trapezius and serratus ante- of >0.2% in which full humeral abduction rior). At the peak of the tent are the direct was observed. Shoulder mobility is poorly and indirect attachments of these structures quantified in primates, but qualitative ob- to the humerus. As in the transverse plane, servation indicates that humeral abduction the tension in these structures caused by the (i.e., elevation in coronal plane) is consider- body weight compresses the torso, and a ably more restricted in nonhominoids than is deep torso is under greater dorsoventral protraction (= flexion, i.e., elevation in the stress than is a shallow torso. By reducing sagittal plane). Humeral abductibility has the dorsoventral diameter of the thorax, the been linked to vertical climbing (Fleagle ribs, ligaments, and muscles of the torso are et al., 19811, but evidence from both labora- less strained. A monkey-like profile, with a tory (Larson and Stern, 1986) and natural deep upper torso, results in a concentration settings (Hunt, 1989a,b, 1990, 1991b) sug- of strain on the upper region of the rib cage. gests forelimb elevation during vertical Tension in structures that attach to the hu- climbing is anterior, with a kinematic simi- merus will tend to straighten them, thereby lar to that of walking, not lateral (i.e., the compressing the convex-profiled upper torso humerus is protracted rather than ab- of monkeys differentially. A shallower upper ducted). This kinematic is similar in baboons torso presents a straighter profile and is (Hunt, 1989b, 1991b) and other monkeys more evenly stressed. A similar dynamic (personal observations), and is therefore un- applies in coronal section. By narrowing the likely to be responsible for chimpanzee hum- upper torso, making for narrower shoulders, era1 abductibility and accompanying shoul- stresses compressing the torso mediolater- der specializations. ally are reduced. Arm-hanging (including arm-hanging with support) is the only common chimpan- Scapula zee positional behavior requiring complete Recent primate field studies have not sup- abduction of the arm (Hunt, 1989a,b, 1990, ported the hypothesis that vertical climbing 1991b1, and is therefore the most likely ex- CHIMPANZEE BIOMECHANICS 529

GJC

Human Chimpanzee

Fig. 4. Schematic human and chimpanzee torsos in posterior view. The “narrow” scapula and the cone-shaped torso of the chimpanzee allows the scapula to rotate farther when the arm is abducted, lessening distance A, the distance between the glenoid fossa and the midline. In chimpanzees the shoulder joint may more closely approach a point more directly above the center of gravity when the arm is abducted (A, > AJ Note that the glenohumeral joint capsule (GJC) in humans is unevenly stretched. planation for chimpanzee shoulder mobility. of shear stress in the structures between the A cranially oriented glenoid fossa may be an glenoid fossa and the spine is reduced. The adaptation to distributing strain more greater the distance between the glenoid evenly over the glenohumeral joint capsule fossa and the spinal column the greater the during unimanual arm-hanging, since a lat- moment arm the lower body weight, via the erally or ventrally oriented glenoid fossa spinal column, has on the area between the concentrates strain on the caudal aspect of spinal column and the lateral link between the glenohumeral joint capsule (Fig. 4). the scapula and the rib cage, serratus ante- Anarrow scapula may maximize the range rior. Third, compressive stress is more of rotation so that during arm-hanging the evenly distributed on the rib cage. A cone- glenoid fossa may approach a point more shaped rib cage reduces strain in the upper directly over the center of gravity (Hunt, rib cage. The close approximation of the 1989a,b, 1990). Scapular rotation approxi- shoulder to the midline in chimpanzees can mates the vertebral border of the scapula be seen by observing that during arm-hang- and spinous processes of the vertebrae (and ing the shoulder seems to disappear behind attached tissues). In humans a close approx- the in ventral view, whereas in humans imation of the shoulder joint to the midline the shoulder remains well lateral. It is sug- would bring the large supraspinous area of gested, therefore, that a long, narrow scap- the scapula into contact with structures as- ula is an adaptation to arm-hanging. A rela- sociated with the vertebrae before it tively great superoinferior length may be achieved the degree of rotation possible for retained to allow the origin of serratus ante- the chimpanzee (Fig. 4). When the glenoid rior and caudal trapezius muscles to remain fossa approximates the spinal column dur- inferior, making a more direct link with the ing arm-hanging, and is thus close to a posi- lower body, while maintaining a constant tion directly over the center of gravity, there area for the origin of the scapular muscles. are three benefits. First, there is less bend- The scapula is anchored ventrally by the ing of the spinal column. Second, the amount clavicle, and therefore the acromioclavicular 530 K.D. HUNT attachment might be expected to be espe- during climbing. Although vertical climbing cially robust in an arm-hanger; it is strongly constituted only 0.9% of all positional behav- anchored by the conoid ligament (Swindler ior, it had the highest of all behaviors for and Wood, 1982). This robust attachment is which the short lumbar region of apes has an adaptation to transmit weight from the been hypothesized to be adapted. This func- glenohumeral capsule to the manubrium via tional complex also may function to provide a the clavicle. The manubrium is particularly more direct link between the suspended broad in chimpanzees and other arm-hang- lower body and the weight-bearing humerus ers (including Ateles: Schultz, 1930, 1936, during unimanual arm-hanging. 1961). Since weight borne by bone requires no muscular effort and does not fatigue liga- Intermembral index ments, the broad manubrium of arm-hang- The low incidence of large WBS vertical ers may be an adaptation to reducing thorac- climbing (0.06%; Hunt, 1991b) makes it un- ical fatigue. likely that the high intermembral index of Corruccini and Ciochon (1976) noted two chimpanzees evolved as an adaptation to features that distinguish hominoids from this positional mode. Given the high fre- other catarrhines: the presence of a cora- quency of arm-hanging, the hypothesis that coacromial ligament, and a more distal loca- long forelimbs are an adaptation to increase tion of the greater and lesser tubercles of the reach in the terminal branches during sus- humerus. The former was suggested to pre- pensory feeding is more likely (Kortlandt, vent vertical dislocation of the humerus and 1968, 1974; Cartmill and Milton, 1977; Hol- to increase muscular leverage during abduc- lihn, 1984; Cant, 1987a). Reach may scale tion, and the latter was hypothesized to func- with body weight (Jungers, 1985; Cant, tion to increase muscular leverage during 1987a)to increase the number of supporting arm raising and to allow greater abduction. structures and the number of food items Such features are useful adaptations to arm- within reach of an individual feeding among raising necessary during vertical climbing terminal branches (Grand, 1972). Attenu- and while foraging during arm-hanging. ated hind limbs have been (Jungers, 1984) suggested as functioning to bring the center Spinal column of gravity closer to arboreal WBS during Rapid, ricocheting brachiation was not quadrupedal walking, thereby decreasing seen in chimpanzees, and other brachiation the chance of falling (Jungers, 1984; Cant, (sensu stricto) was too rare (0.1% of all posi- 1987a). Short legs also may function to tional behavior; Hunt, 198913, 1991b) to ex- lighten the lower body, allowing suspensory plain the short lumbar region of the spinal feeding among smaller branches by reducing column of the African apes as a response to fatigue andor energy expenditure. reducing torsion during rapid suspensory locomotion (Hildebrand, 1974). Musculature A short trunk has been hypothesized as The hypothesis that muscles that are dis- functioning to maintain truncal rigidity tinctively large in apes (i.e., “brachiating” when the lower body is fixed to a support muscles) function as propulsors during bra- when reaching out to cross gaps; a top-heavy chiation (sensu stricto) has not been borne tendency in apes would tend to increase such out. EMG studies show that brachiation re- bending stresses (Cartmill and Milton, quires relatively little muscular activity 1977). However, bridging with truncal rigid- (Jungers and Stern, 1980, 1981, 1984), im- ity is rare among chimpanzees (Hunt, plying that it cannot select for distinctively 1989b). Most transferring occurs in small- large muscle masses (Preuschoft and Demes, branch milieus where reaching out while 1984: 101; Hollihn, 1984).Nor is it likely that holding the lower body rigid is impossible “brachiating” muscles are adapted to arm- (Hunt, 1991b). hanging; most muscles are either silent dur- A short lumbar region has been hypothe- ing arm-hanging (Tuttle and Basmajian, sized to better resist buckling strain pro- 1974, 1977, 1978a,b), or modestly active duced by propulsive forces from the hind (caudal serratus anterior, caudal trapezius, limbs during climbing (Jungers, 1984). Tut- and intermediate deltoid are active during tle and Basmajian (1977) hypothesized that some passive hanging, Jungers and Stern, a short torso and an iliac origin of latissimus 1984; Larson and Stern, 1986; Larson et al., dorsi together serve to form a direct link 1991). between the lower body and the humerus Vertical climbing is typically accompanied CHIMPANZEE BIOMECHANICS 53 1 by considerable muscle activity in species for quantitative data on relative size of cranial which it has been measured. Furthermore, and caudal pectoralis major are lacking, the muscles that are large in apes are generally greater size of the entire muscle suggests more active during vertical climbing motions both are relatively large in apes. Caudal than during other common positional behav- pectoralis major and pectoralis minor are iors, implying that it is for this behavior that most active during humeral retraction in the the large size of these muscles has been support phase of vertical climbing, and are maintained (Jungers and Stern, 1980,1981, therefore probably adaptations to vertical 1984). Such a conclusion assumes that the climbing. Likewise, if posterior deltoid is kinematics of vertical climbing are not found larger in chimpanzees, it is associated with in other important (= high frequency) posi- vertical climbing. Cranial pectoralis was ac- tional behaviors. Some movements typical of tive in rapid non-weight-bearing protraction vertical climbing are also common during of the arm during climbing; it may also aid in arm-hanging, and muscles associated with reaching out during feeding. Lowest caudal these movements may be adapted to both. serratus anterior is active during both arm- Kmematics, positional mode frequency, hanging and arm-retraction and may func- muscle size, and muscle activity may be tion to fix the lower scapula to the torso considered together to address this issue. against cranialward suspensory forces. Bra- Relative muscle size, when considered chialis and brachioradialis, elbow flexors, with information on limb motion and EMG are active during humeral retraction and are activity during common positional behaviors therefore probably adapted to climbing, but such as vertical climbing, quadrupedal walk- EMG data are missing. ing, arm-hanging, and arm-raising (either protraction or abduction), suggests the adap- CONCLUSIONS tive function of muscle specializations in Chimpanzee positional behavior, consid- chimpanzees (summarized in Table 4). It is ered in light of the mechanical arguments presumed that muscles that are active dur- above and previous research on EMG activ- ing a positional mode shown to be selectively ity and relative muscle mass, provides important in chimpanzees, that are particu- strong support for the contention that most larly large in chimpanzees, and that are not osteoligamentous specializations of the active in any other common behavior are chimpanzee upper body are adaptations to evolved for or maintained for that positional arm-hanging and most muscular specializa- behavior. If exactly the same muscles are tions are adaptations to vertical climbing (cf. active in two or more behaviors, each with Tuttle and Basmajian, 1977; Preuschoft and similar selective importance, large muscle Demes, 1984; Hollihn, 1984). mass is likely to be adapted to all of those Long, narrow scapulae, cone-shaped rib behaviors. cages, robust clavicular anchors, anteropos- Several hypotheses are supported. A teriorly flattened thoraxes (and accompany- flexor of the elbow (biceps brachii) and a ing strongly curved ribs), mobile, abductible major humeral retractor (latissimus dorsi) humeri, wide manubria of the sterna, and are unambiguously correlated with vertical cranially oriented glenoid fossae are hypoth- climbing alone (VC, Table 4). Teres minor, esized to be a functionally related adaptive middle caudal serratus anterior, and cranial complex related to arm-hanging. These fea- trapezius are unambiguously correlated tures are hypothesized to have evolved to with arm-raising, a motion observed both reduce muscular activity and ligamentous during the swing phase of vertical climbing and skeletal strain during unimanual sus- and in reaching out for food while arm-hang- pension. The lack of a tail reflects the rela- ing (VC, AH, Table 4). Intermediate deltoid tive unimportance of leaping in chimpan- is active in abduction, not protraction, and zees. Liberal ulnar deviation of the manus, therefore is suggested to be an adaptation to long, curved metacarpals and phalanges, reaching out during arm-hanging (AH, and a short lumbar region are likely to be Table 4). adaptations to both vertical climbing and In some cases precise comparisons be- arm-hanging. tween apes and monkeys muscle masses or Large elbow flexors and humeral retrac- EMG data during critical behaviors are un- tors are best explained as adaptations to available, but likely adaptations are sug- vertical climbing (Stern et al., 1977; Fleagle gested (positional mode keys followed by a et al., 1981). Humeral protractors are likely question mark, Table 4). Although separate to be adaptations to arm-raising both during TABLE 4. Muscle size and function in chimpanzees Larger Active during Active Active Active in Likely in humeral during during protraction Muscle adaptation? chimps? retraction? walking? arm-hanging? or abduction? Biceps brachii vc +++a --111).15 (-3.5) Brachialis VC? ++8,-10 -(11).15 Brachioradialis VC? +8,17,-10 --(11).15 Deltoid (whole) +++I34 -anterior VC, AH? +++6.'4 -intermediate AH +++Z ++&I4 -posterior VC? ++I4 Infraspinatus 0 0' -4 +6J4 Latissimus dorsii vc ++;1,16 --I4 Pectoralis major +++9 -clavicular VC,AH? +(5),6 -sternacostal VC? ++15),6,14 Pectoralis minor 0 0' ++6 Rhomboids X +2 +14 Serratus anterior -middle caudal VC,AH ++I3 --14 -lowest caudal VC,AH ++'.9 Subscapularis 0 -4 Supraspinatus 0 01, ++2,6 -- 4 Teres -major 0 01,4 ' -minor VC,AH +4 Trapezius cranial VC, AH ++1.4.9 caudal X ++4 Trirpns n --9 -(11j.15 +(lI),lS

Simplificationsand interpretations were made in compiling this review. Muscle comparisons with Old World monkeys were often made with ape data pooled. Details are given below. Most EMG data are for chimpanzees,but where chimpanzeedata are unavailable data from other apes are offered (in parentheses). Where results arediametrically opposed, twovalues are given; an attempt was made to give a single value if possible. Likely adaption (bold face): an adaption to a single positional behavior is suggested. Underline: adaption to two behaviors suggested. Positional mode followed by a questionmark: some data missing, but adaption likely. 0: muscle size smaller in apes, so no behavioral specialization identifiable; X too little data, or not distinctive. VC: vertical climbing, AH: reaching during arm-hanging. EMG activity: +++, marked in most or all studies; ++, variably high (by study or experiment) or consistently moderate; +, low 0rvariablymoderate;-, inactiveinmoststudiesorverylow activity; --,inactivein all studies. Musclesize: +++, muchlargerin apes bymostmeasures; ++, largerin apes by most measuresorlargerin mostapes; +,somewhatlargerin apes bymostmeasures; 0,nolargerinapes or variableaccordingtomeasure; -,smallerin apesorvariablysmalleraccording to measure; --, much smaller in apes in most studies. 'Ashton and Oxnard, 1963(apes);Worruccini andciochon, 1976;"Fleagleet al., 1981 (gibbons); 'Inman et al., 1944 (musclecomparisonfor chimps against other primates; EMG on humans only);5Jungers andstern, 1980,1984(gibbons);6Larsonand Stern, l986,1987(chimps);'Larsonet al., 1991 (chimps);RMiller,1932(chi1nps);~Oxnard, 1963(apes);'"Swindlerand Wood, 1982 (chimp compared to Pupio); I' Tuttle and Basmajian, 1974 (gorilla);12Tuttle and Basmajian, 1977 (great apes); '3Tuttle and Basmajian, 1978a (chimps unless in parentheses); "Tuttle and Basmajian, 197813 (chimps); 'jTuttle et al., 1977; I6Ziegler, 1964. CHIMPANZEE BIOMECHANICS 533 vertical climbing and arm-hanging. High Ashton EH, Oxnard CE, and Spence TG (1965) Scapular frequencies of arm-hanging and vertical shape and primate classification. Proc. Zool. SOC. climbing support the hypothesis that large Lond. 145.125-142. Avis V (1962) Brachiation: The crucial issue for man’s digital flexors and an iliac origin of latissi- ancestry. 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