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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 meral abduction, Suspensory behavior

Arm-hanging, Vertical climbing, Brachiation, Hu-

ABSTRACT Mechanical hypotheses concerning the function of chimpanzee 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 humerus, and vertical climbing was the only distinctive chimpanzee positional behavior that required forceful retraction of the humerus and flexion of the elbow. Some elements of the chimpanzee anatomy, including an abductible humerus, a broad thorax, a cone-shaped torso, and a long, narrow scapula, are hypothesized to be a coadapted functional complex that reduces muscle action and structural fatigue during arm-hanging. Large muscles that retract the humerus (latissimus 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 notably long forelimbs (fingers included), mobile shoulders, distinctively wide, shallow, short torsos, and no tail (Keith, 1891, 1899,1903,1923; Schultz, 1930,1936,1953; Washburn, 1950; Erikson, 1963). Myologi- cally they are distinguished by large muscles that flex the elbow, retract the humerus, and raise the arm (Ashton and Oxnard, 1963, 1964a; Napier, 1963; Oxnard, 1963, 1967; Ashton et al., 1965; Tuttle, 1969b). Keith (1891, 1899, 1903) proposed that such anatomical specializations in gibbons were adaptations to brachiation; others extended the hypothesis to all apes (Gregory, 1916, 1928,1934; Morton, 1922,1926; Frey, 1923; Miller, 1932; Midlo, 1934; reviewed in Tut- tle, 1974; Andrews and Groves, 1976).

The short lumbar region (Schultz, 1936) and high intermembral index of apes were interpreted as aspects of an overall reduction of body parts not active (or disadvantageous: Hildebrand, 1974) during suspensory loco-

motion (Keith, 1891,1899,1923; Avis, 1962). Muscles particularly large or distinctively shaped in apes were reasoned to be espe- cially important as brachiating propulsors (Keith, 1891; Miller, 1932; Campbell, 1937; Inman et al., 1944; Ashton and Oxnard, l963,1964a, b; Erikson, 1963; Oxnard, 1963; Corruccini and Ciochon, 1976). The wide thorax and the accompanying relocation of the scapula to a more dorsal position on the thorax hypothetically oriented the scapulohumeral joint laterally, increasing the excursion of the humerus by removing the chest wall as a barrier (Miller, 1932; Avis, 1962). A long, narrow scapula’ was hypothe-

‘Mediolaterally reduced and axially elongated The distance between the glenoid fossa and the angle of the superior vertebral border is small compared to the distance from either the glenoid fossa or the angle of the vertebral border to the inferior angle of the scapula.

- Received October 8,1990; accepted June 4,1991.

@ 1991 WILEY-LISS, INC.

522 K.D. HUNT

sized as serving to increase the mechanical advantage of trapezius and serratus anterior during the scapular rotation necessary for arm-raising (Ashton and Oxnard, 1963, 1964a; Oxnard, 1963,1967). Reduced articulation between the ulna and the carpus and a neomorphic ball and socket-like joint between the radius and the ulna (Midlo, 1934; Lewis, 1965 et seq.) compared to Old World monkeys (Benton, 1967; Jones, 1967; Jen- kins, 1973; O’Connor, 1975, 1976) were interpreted as adaptations to wrist rotation during brachiation.

Although widely accepted, many of these hypotheses were simplistic or incorrect. Bra- chiation (sensu stricto)2 was rarely observed in naturalistic studies of great apes; instead, terrestrial knuckle-walking dominated Afri- can ape behavior (reviewed in Tuttle, 1986; Yerkes and Yerkes, 1929). The carpus and metacarpus of chimpanzees and gorillas re- flect this adaptation in being less flexible and more reinforced compared to orangutans and gibbons (Tuttle, l965,1969a,c; Jen- kins and Fleagle, 1975). Knuckle-walking, however, cannot explain most ape synapomorphies since it differs from the terrestrial quadrupedalism of other primates principally in the orientation of the wrist and manus, suggesting that specializations should be limited to those structures, since quadrupedalism is no more common among apes than most other primates (Feldesman, 1982; Tuttle, 1986; Hunt, 1991a).

Whereas Lewis (1965 et seq.) maintained that distal displacement of the pisiform and a reduced ulnar-triquetral articulation were evolved to allow extensive wrist rotation during brachiation (sensu stricto), the gibbon, the preeminent brachiator, was shown to have the least mobile wrist of all apes (Conroy and Fleagle, 1972). Furthermore, “brachiating” characters were observed in lorises (Cartmill and Milton, 1977), indicat- ing that a flexible wrist may be an adaptation to slow (= quadrumanous) climbing rather than brachiation. Jenkins (1981) showed that in fact the articulation between the styloid process of the ulna and the triquetral and pisiform had little to do with wrist rotation, which occurs mostly in the midcar- pal joint.

‘The term brachiation (sensu stricto) means hand-over-hand suspensory locomotion, with or without a period of free flight, as opposed to a more liberal usage (sensu lato). Iticochetal brachiation is reserved for gibbon-like brachiation with a period of free flight.

Quadrumanous climbing was offered as a more universal hominoid behavior than brachiation (Washburn, 1968,1973; Conroy and Fleagle, 1972; Fleagle, 1976; Cartmill and Milton, 1977; Fleagle et al., 1981). Such a reassessment was more a nomenclatural clarification than an advance in understand- ing since brachiation (sensu lato) had come to encompass essentially the same behaviors proposed for quadrumanous climbing; i.e., suspensory locomotion, suspensory posture, vertical climbing, and walking on inclined or small-diameter weight-bearing structure(s) (WBS) (Washburn, 1968,1973; Cant, 1986).

Two developments refined the climbing hypothesis, changing its focus and giving it a powerful theoretical orientation. The first was the functional linking of high intermem- bra1 indices and vertical climbing. Long arms were hypothesized as functioning to increase friction between the tree bole and the pes, allowing apes to ascend larger WBS than monkeys (Kortlandt, 1968, 1974; Cart- mill, 1974; Jungers, 1976; Mendel, 1976; Stern et al., 1977; Fleagle et al., 1981; Jungers and Stern, 1980, 1981, 1984; Jungers and Susman, 1984; Sarmiento, 1987). The second was electromyography (EMG) research, demonstrating that many muscles particularly large in apes were more active during vertical climbing than during knuckle-walking or brachiation (Miller, 1932; Inman et al., 1944; Ashton and Ox- nard, 1963, 1964a,b; Oxnard, 1963; Fleagle, 1974, 1977; Corruccini and Ciochon, 1976; Tuttle et al., 1972; Tuttle and Basmajian, 1974a,b,c, 1977, 1978a,b; Stern et al., 1977; Susman and Stern, 1979; Jungers and Stern, 1980; Swindler and Wood, 1982; Larson and Stern, 1986,1987). It appeared that the more restricted mode, vertical climbing, as opposed to the more general quadrumanous climbing, could be the behavior for which ape synapomorphies were evolved, since it (hypothetically) necessitated shoulder mobility (in reaching up for a new handhold), elongated forelimbs (for climbing large trunks), and ape muscular specializations, all “brachiating” hallmarks (Stern et al., 1977, 1980a,b; Fleagle et al., 1981).

Although it was not clearly reconcilable with this interpretation, it remained obvious to these researchers and others that suspensory posture also was an important aspect of the ape positional behavior and must have accompanying anatomical adaptations (Ellefson, 1968,1974; Chivers, 1972; Andrews and Groves, 1976; Fleagle, 1976, 1988; Git-

CHIMPANZEE BIOMECHANICS 523

tins, 1983; Srikosamatara, 1984; Sabater Pi, 1979; Susman et al., 1980; Sugardjito, 1982; Hollihn, 1984; Kano and Mulavwa, 1984; Susman, 1984; Fleagle and Kay, 1985; Sug- ardjito and van Hooff, 1986; Cant, 1987a,b; Fleagle, 1988; Hunt 1989a,b, l990,1991a,b). EMG research demonstrated that the digital flexors were virtually the only active muscles during a~-m-hanging.~ This implies sig- nificant skeletal and ligamentous (but not muscular) adaptations (ibid.) to arm-hanging to assure that body weight is borne by skeleton, ligaments, intramuscular septa, and/or passive muscular tension (Tuttle and Basmajian, 197413, 1977, 1978a,b; Tuttle e t al., 1977, 1983; Preuschoft and Demes, 1984; Hollihn, 1984).

Recent data on chimpanzees suggests that arm-hanging and vertical climbing are the most distinctive chimpanzee positional modes; arm-hanging was reasoned to influence upper body anatomy more because it is kinematically different in chimpanzees and Old World monkeys, whereas vertical climbing is not (Hunt, 1991b).

Arm-hanging has several unusual mechanical requirements. Whereas most postures typically exert compressive forces on skeletal elements, unimanual arm-hanging places the supporting limb in net tension (Stern and Oxnard, 1973), a situation for which the mammalian body plan (and indeed bone itself) is poorly adapted. Unlike, for example, standing, during suspension the body weight must be supported by a grip, which requires powerful and long-lasting muscle action. The majority of the body weight is suspended beneath an eccentri- cally placed forelimb and borne by the glenohumeral joint capsule. The humerus, adducted and attached to the body via a rather ventrolaterally facing glenoid fossa in most mammals, must be completely abducted. During arm-hanging a ventrolateral orientation of the glenoid fossa potentially causes the caudal aspect of the joint capsule to be much tauter than other parts, differentially straining it. Because the shoulder is lateral to both the spinal column and the point normally directly over the center of gravity, the vertebral column must bend as the body settles under the shoulder. Body weight cre- ates shear stress between the shoulder and the spine in the sagittal plane. When the bony, ligamentous, and muscular links be-

'Unless otherwise indicated arm-hanging refers to unimanual suspension.

tween the torso and the arm bear the body weight they create bending forces on the ribs and tensile stress on vertebrocostal ligaments, ultimately resulting in fatigue (Bas- majian, 1965; MacConnaill and Basmajian, 1969).

Here, mechanical hypotheses explaining chimpanzee anatomical specializations (many of which are shared by all apes) are examined in the context of chimpanzee positional behavior data (Hunt, 1991b). An attempt is made to follow the tenet that anatomy evolves to reduce muscular demand and strain in bone and ligaments during common positional behaviors, thereby reducing fatigue and conserving energy (Basmajian, 1965; MacConnaill and Basmajian, 1969; Cartmill et al., 1987). Some chimpanzee specializations are discussed as possible adaptations to unimanual arm-hanging, including the following: broad manubrium of the sternum, ventrally placed vertebral column, shallow, wide, cone-shaped torso (Schultz, 1930, 1936, 19611, narrow ~ c a p u l a , ~ cranially oriented glenoid fossa, ulnocarpal dissociation, and long, curved fingers.

MATERIALS AND METHODS

Observations were made on chimpanzees at the Mahale Mountains (571 hours of observations) and Gombe Stream (130 hours) National Parks, Tanzania, resulting in 16,303 instantaneous, two-minute focal observations (Altmann, 1974) on 26 well habit- uated prime adults spanning all social ranks. Observations were made throughout the ranges of the respective community unit groups at all hours chimpanzees were active (see Hunt, 1989b, 1991b, for more detail). At the two-minute mark the animal was instan- taneously sighted and positional mode, angle that supporting WBS made with the horizontal, WBS diameter, and grip type (as applicable) were recorded for each cheiridium and/or the ischia (Hunt, 1989b). Other quantitative results are reported elsewhere (Hunt, 1989b, 1991b).

RESULTS AND DISCUSSION Manus and carpus

Chimpanzee rays 11-V are elongated and have a marked ventral curvature (Jones,

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 Oxnard, 1963, 1964a) has been disproved (Larson and Stern, 1986; Larson e t 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 olecranon process.

1942; Straus, 1940, 1949; Schultz, 1927, 1930,1956; Susman, 1979). Long fingers are generally presumed to be an adaptation for gripping larger diameter WBS during either suspension (Preuschoft and Demes, 1984) or climbing. If the former, one would expect the diameter of a typical WBS from which a chimpanzee suspends itself to be larger than that which a typical primate hand might circumduct. Yet, most ecological hypotheses (e.g., Avis, 1962; Grand, 1972) purport suspensory behavior to be an adaptation to small, terminal branch milieus, a perspec- tive strongly supported in naturalistic studies of orangutans (Cant, 1987a,b) and chimpanzees (of all postures in chimpanzees, arm-hanging occurs on the smallest WBS; Hunt, 1991b). The hook grip, a common suspensory grip, was used on WBS with a median diameter of only 2.5 cm (Table l), and over 96% of all WBS were smaller than 6.5 cm. Long fingers might be argued to be merely a pleiotropic or linkage effect of selection for elongated arms; if so, fingers should be equal to or shorter than the remainder of the forelimb in relation to some other body part. In relation to trunk height chimpanzee fingers are relatively even longer than their arms, whereas among other hominoids the same is true only for orangutans (Schultz, 1936: Figs. 15,16). Such elongation suggests that some positive selective force maintains digit length.

The chimpanzee wrist exhibits extensive volar flexion, whereas the range of ulnar deviation is great but not remarkably so (Tuttle, l965,1969b, c; Jenkins and Fleagle, 1975; Sarmiento, 1988). Radial and dorsal mobility are rather severely restricted (radial more so), presumably to stabilize the wrist during forceful retraction of the arm during quadrupedal knuckle-walking (ibid.). Per- haps the only specific explanation offered for

the adductible wrist in chimpanzees, that it allows the hand to clear the WBS in knuckle- walking (Conroy and Fleagle, 19721, is disproved (Jenkins and Fleagle, 1975). Since the limit of ulnar deviation occurs with contact between the styloid process of the ulna and the carpus (Tuttle, l965,1969b, c), ulnocarpal dissociation may be an adaptation to retain a large range of ulnar deviation in a wrist generally adapted for stabilization. U1- nar deviation may be necessary during arm- hanging and vertical climbing.

Of those positional modes that require strong digital flexion to support the body weight (arm-hanging, arm-hanging with support, clinging, vertical climbing, and suspensory locomotion) only arm-hanging (all modes = 4.4%) and vertical climbing (0.9%) constitute >0.3% of chimpanzee positional behavior (Table 2; Hunt, 1991b). Both arm- hanging (>19% of WBS were within 30" of true vertical, Table 3) and vertical climbing (88% of WBS were within 30" of true vertical, Table 3) commonly involve supporting a sig- nificant portion of the body weight by gripping subvertical WBS. Because the forearm is near vertical during these behaviors, it approaches being parallel to the WBS. If the wrist cannot be adducted, the fingers will be parallel to the WBS and therefore unable to grip it. The more nearly parallel the fingers are to the WBS, the larger is its effective diameter, and the longer fingers must be to circumduct it. For example, when the long axis of the hand makes an angle of 45" with a vertical WBS the effective diameter of the branch is 40% greater than when the hand is perpendicular to the WBS. The ability to ulnar-deviate the wrist therefore is particularly valuable for animals that grip vertical branches.

Two aspects of climbing work to reduce weight depending on the carpus and pes

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526 K.D. HUNT

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

Weight bearing stratum angle Positional 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 Knuckle-walk (13) 0.0 15.4 69.2

Brachiate5 (14) 0.0 14.2 78.5 Vertical climb (93) 88.2 9.7 0.0

0.0 0.0 2.2 7.1

3.2 0.0 0.0 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-hand suspensory 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 a t the beginning of the propulsive stroke. During unimanual arm-hanging the entire body weight depends on the manus, and the forearm is always parallel to a vertical WBS. Among chimpanzees suspensory behavior occurred among terminal branches on WBS with median diameters of 2.5 cm (n = 376; Hunt, 1991b). This diameter branch is small enough that it is often bent to near vertical from the weight of the animal (Grand, 1972; Hunt, 1991b), which in turn increases its effective diameter so that it may require longer fingers and an adductible wrist.

Ray curvature in the apes parallels degree of arboreality and frequency of suspensory activity (Susman, 1979; Hunt, 1991a). Sarmiento (1988) showed that ray curvature serves a muscle-sparing function during suspensory behavior. Ventral curvature may also be an adaptation to distributing gripping force more evenly around the circumfer- ence of vertical WBS and thereby reducing tissue strain. The weight of the body, when supported by a single manus in arm-hanging, tends to pull digital and palmar tissue contacting the WBS in an upward direction, or radially. The body weight pulls the phalanges downward while the WBS pulls the

Human Chimpanzee

Fig. 1. Gripping in humans and chimpanzees. Note that with curved phalanges a more uniform distance is maintained between bone (black bars) and a gripped vertical WBS (stippled area) than with straight phalanges. In a straight-fingered individual pressure on the WBS is higher near the middle of the phalanx where the bone is closer to the WBS, whereas in a curved-finger individual pressure is more uniformly applied along the length ofthe digit. Note that with curved phalanges even though the distance between bone and WBS remains the same (arrows) a larger WBS may be gripped.

volar skin upward, thus creating radial torsion in the volar tissue, which may fatigue or damage tissue during sustained arm- hanging. Straight phalanges put much of the pressure of a strong grip on a relatively small surface area of volar tissue near the middle of the phalanx, whereas other tissue is relatively unstressed (Fig. 1). Curved phalanges maintain a constant distance between the phalanx and the WBS along the entire volar aspect of the finger, thereby assuring similar pressures along the length of the digit. Be-


Monkey

Chimpanzee

Fig. 2. Schematic transverse section of monkey and chimpanzee torsos. The vertebral column is represented at the top, the sternum at the bottom. Because the shoulder joint is lateral to the center of gravity (C,) the force of gravity (F,) and the counteracting force of the anchored arm (Fah) tend to create forces compressing the

cause a greater surface area bears weight, the maximum strain on midphalangeal tissue is reduced and torsional strain is reduced as well.

Ventrally curved phalanges also allow fingers of a given length to circumduct larger WBS. With straight phalanges, bone near the middle of the phalanx approximates the WBS more closely than does that near the joints (Fig. 1). This proximity limits the size of the WBS a finger can circumduct. Curved phalanges have this area of bone “moved” farther from the WBS. When human and chimpanzee fingers circumduct a WBS so that the fingertip touches the palm, the cir- cumference spanned by the curved digit is greater (Fig. 1). Although gripping larger WBS may be rare, a rather simple modifica- tion that allows it may be advantageous, and such an adaptation may be necessary for gripping more commonly encountered, mod- erately sized WBS that are subvertical.

This line of reasoning suggests that long, curved rays and an adductible wrist may be a functionally related adaptation to strongly gripping vertical or subvertical WBS during arm-hanging and vertical climbing, positional behaviors hypothesized to exert the strongest selective pressure on the chimpanzee positional apparatus (Hunt, 1991b).

Thorax Although the chimpanzee thorax is con-

stricted dorsoventrally (i.e., shallow) through-

rib cage (Fc). Even when body weights are equal [i.e., F ,m) = F I making the tension in the arms equal I#,,,,, = ~ ~ h ~ , , l , the forces compressing the torso are greater in the monkey than in the chimpanzee LF,,,, > F,,,,].

out its length, it is constricted most superi- orly, both in coronal and sagittal section (Erikson, 1963; Schultz, 1961). This gives the rib cage a rather cone-shaped appearance compared to the more barrel-shaped appearance in monkeys. Perhaps the most widely accepted explanation for a broad thorax is that it separates the shoulders and orients the glenoid fossae laterally, thereby increasing the span of the arms and allowing circumduction of larger tree trunks when climbing (Cartmill and Milton, 1977); however, large-WBS-vertical-climbing is rare among Mahale and Gombe chimpanzees (Hunt, 1991b), suggesting that selection to maximize mechanical efficiency for it may be insignificant.

This feature may be an adaptation to arm- hanging. Stresses on the torso during arm- hanging may be viewed in the transverse and the sagittal planes in order to examine the influence of shape on tissue strain. Be- cause the shoulder joint is lateral to the center of gravity during arm-hanging (Fig. 2: transverse section) there is a lateral compo- nent to the forces acting on the rib cage, and as a consequence the torso is stressed as if the shoulderjoint were being pulled laterally against the force of the body weight, stress- ing the torso dorsoventrally (i.e., causing the sternum and spinal column to be pressed together). The greater the anteroposterior diameter of the torso, the greater is this force.

528 K.D. HUNT

t 'ah(m)

convex ---)

Fig. 3. Schematic side view of monkey and chimpanzee torsos (sagittal section). Note that the force ofgravity (F,) and the counteracting force of the anchored arm (F& create forces compressing the rib cage (FJ that are greater the greater the distance between the anchor points on the torso. Even when body weights are equal

A similar situation applies in the sagittal plane. When the arm is raised above the head, the muscles of the shoulder, the scapula, and the clavicle are oriented in a tent- like configuration (Fig. 3). The anchors of the tent are the thoracohumeral muscles, the sternoclavicular joint, the scapulohumeral muscles, and the scapula (attached to the torso in part by trapezius and serratus anterior). At the peak of the tent are the direct and indirect attachments of these structures to the humerus. As in the transverse plane, the tension in these structures caused by the body weight compresses the torso, and a deep torso is under greater dorsoventral stress than is a shallow torso. By reducing the dorsoventral diameter of the thorax, the ribs, ligaments, and muscles of the torso are less strained. A monkey-like profile, with a deep upper torso, results in a concentration of strain on the upper region of the rib cage. Tension in structures that attach to the humerus will tend to straighten them, thereby compressing the convex-profiled upper torso of monkeys differentially. A shallower upper torso presents a straighter profile and is more evenly stressed. A similar dynamic applies in coronal section. By narrowing the upper torso, making for narrower shoulders, stresses compressing the torso mediolaterally are reduced.

Scapula Recent primate field studies have not sup-

ported the hypothesis that vertical climbing

t

Chimpanzee

[i.e., F,,,, = F ,,,J the forces compressing the torso are greater in &e deeper (i.e., monkeydike) torso IF,,,, > F,,,J. Note also that the convex area of the monkey torso is subjected to compressive stress by tension in structures that attach to the humerus.

and large WBS vertical climbing are responsible for shoulder mobility or intermembral proportions in orangutans (Cant, 1987a,b) and chimpanzees (Hunt, 1989a,b, 1991a,b). Among chimpanzees vertical climbing involved little humeral abduction (Hunt, 1989a, 1991b), and arm-hanging (all modes = 4.4%) was the only behavior with a frequency of >0.2% in which full humeral abduction was observed. Shoulder mobility is poorly quantified in primates, but qualitative ob- servation indicates that humeral abduction (i.e., elevation in coronal plane) is consider- ably more restricted in nonhominoids than is protraction (= flexion, i.e., elevation in the sagittal plane). Humeral abductibility has been linked to vertical climbing (Fleagle et al., 19811, but evidence from both labora- tory (Larson and Stern, 1986) and natural settings (Hunt, 1989a,b, 1990, 1991b) suggests forelimb elevation during vertical climbing is anterior, with a kinematic similar to that of walking, not lateral (i.e., the humerus is protracted rather than abducted). This kinematic is similar in baboons (Hunt, 1989b, 1991b) and other monkeys (personal observations), and is therefore un- likely to be responsible for chimpanzee hum- era1 abductibility and accompanying shoulder specializations.

Arm-hanging (including arm-hanging with support) is the only common chimpanzee positional behavior requiring complete abduction of the arm (Hunt, 1989a,b, 1990, 1991b1, and is therefore the most likely ex-


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. A cranially oriented glenoid fossa may be an adaptation to distributing strain more evenly over the glenohumeral joint capsule during unimanual arm-hanging, since a laterally or ventrally oriented glenoid fossa concentrates strain on the caudal aspect of the glenohumeral joint capsule (Fig. 4).

Anarrow scapula may maximize the range of rotation so that during arm-hanging the glenoid fossa may approach a point more directly over the center of gravity (Hunt, 1989a,b, 1990). Scapular rotation approximates the vertebral border of the scapula and spinous processes of the vertebrae (and attached tissues). In humans a close approximation of the shoulder joint to the midline would bring the large supraspinous area of the scapula into contact with structures associated with the vertebrae before it achieved the degree of rotation possible for the chimpanzee (Fig. 4). When the glenoid fossa approximates the spinal column during arm-hanging, and is thus close to a position directly over the center of gravity, there are three benefits. First, there is less bending of the spinal column. Second, the amount

of shear stress in the structures between the glenoid fossa and the spine is reduced. The greater the distance between the glenoid fossa and the spinal column the greater the moment arm the lower body weight, via the spinal column, has on the area between the spinal column and the lateral link between the scapula and the rib cage, serratus anterior. Third, compressive stress is more evenly distributed on the rib cage. A cone- shaped rib cage reduces strain in the upper rib cage. The close approximation of the shoulder to the midline in chimpanzees can be seen by observing that during arm-hanging the shoulder seems to disappear behind the neck in ventral view, whereas in humans the shoulder remains well lateral. It is suggested, therefore, that a long, narrow scapula is an adaptation to arm-hanging. A relatively great superoinferior length may be retained to allow the origin of serratus anterior and caudal trapezius muscles to remain inferior, making a more direct link with the lower body, while maintaining a constant area for the origin of the scapular muscles.

The scapula is anchored ventrally by the clavicle, and therefore the acromioclavicular

530 K.D. HUNT

attachment might be expected to be espe- cially robust in an arm-hanger; it is strongly anchored by the conoid ligament (Swindler and Wood, 1982). This robust attachment is an adaptation to transmit weight from the glenohumeral capsule to the manubrium via the clavicle. The manubrium is particularly broad in chimpanzees and other arm-hang- ers (including Ateles: Schultz, 1930, 1936, 1961). Since weight borne by bone requires no muscular effort and does not fatigue ligaments, the broad manubrium of arm-hang- ers may be an adaptation to reducing thorac- ical fatigue.

Corruccini and Ciochon (1976) noted two features that distinguish hominoids from other catarrhines: the presence of a cora- coacromial ligament, and a more distal loca- tion of the greater and lesser tubercles of the humerus. The former was suggested to pre- vent vertical dislocation of the humerus and to increase muscular leverage during abduction, and the latter was hypothesized to function to increase muscular leverage during arm raising and to allow greater abduction. Such features are useful adaptations to arm- raising necessary during vertical climbing and while foraging during arm-hanging.

Spinal column Rapid, ricocheting brachiation was not

seen in chimpanzees, and other brachiation (sensu stricto) was too rare (0.1% of all positional behavior; Hunt, 198913, 1991b) to explain the short lumbar region of the spinal column of the African apes as a response to reducing torsion during rapid suspensory locomotion (Hildebrand, 1974).

A short trunk has been hypothesized as functioning to maintain truncal rigidity when the lower body is fixed to a support when reaching out to cross gaps; a top-heavy tendency in apes would tend to increase such bending stresses (Cartmill and Milton, 1977). However, bridging with truncal rigidity is rare among chimpanzees (Hunt, 1989b). Most transferring occurs in small- branch milieus where reaching out while holding the lower body rigid is impossible (Hunt, 1991b).

A short lumbar region has been hypothesized to better resist buckling strain pro- duced by propulsive forces from the hind limbs during climbing (Jungers, 1984). Tut- tle and Basmajian (1977) hypothesized that a short torso and an iliac origin of latissimus dorsi together serve to form a direct link between the lower body and the humerus

during climbing. Although vertical climbing constituted only 0.9% of all positional behavior, it had the highest of all behaviors for which the short lumbar region of apes has been hypothesized to be adapted. This functional complex also may function to provide a more direct link between the suspended lower body and the weight-bearing humerus during unimanual arm-hanging.

Intermembral index The low incidence of large WBS vertical

climbing (0.06%; Hunt, 1991b) makes it un- likely that the high intermembral index of chimpanzees evolved as an adaptation to this positional mode. Given the high frequency of arm-hanging, the hypothesis that long forelimbs are an adaptation to increase reach in the terminal branches during suspensory feeding is more likely (Kortlandt, 1968, 1974; Cartmill and Milton, 1977; Hol- lihn, 1984; Cant, 1987a). Reach may scale with body weight (Jungers, 1985; Cant, 1987a) to increase the number of supporting structures and the number of food items within reach of an individual feeding among terminal branches (Grand, 1972). Attenu- ated hind limbs have been (Jungers, 1984) suggested as functioning to bring the center of gravity closer to arboreal WBS during quadrupedal walking, thereby decreasing the chance of falling (Jungers, 1984; Cant, 1987a). Short legs also may function to lighten the lower body, allowing suspensory feeding among smaller branches by reducing fatigue andor energy expenditure.

Musculature The hypothesis that muscles that are dis-

tinctively large in apes (i.e., “brachiating” muscles) function as propulsors during brachiation (sensu stricto) has not been borne out. EMG studies show that brachiation requires relatively little muscular activity (Jungers and Stern, 1980, 1981, 1984), implying that it cannot select for distinctively large muscle masses (Preuschoft and Demes, 1984: 101; Hollihn, 1984). Nor is it likely that “brachiating” muscles are adapted to arm- hanging; most muscles are either silent during arm-hanging (Tuttle and Basmajian, 1974, 1977, 1978a,b), or modestly active (caudal serratus anterior, caudal trapezius, and intermediate deltoid are active during some passive hanging, Jungers and Stern, 1984; Larson and Stern, 1986; Larson et al., 1991).

Vertical climbing is typically accompanied

CHIMPANZEE BIOMECHANICS 53 1

by considerable muscle activity in species for which it has been measured. Furthermore, muscles that are large in apes are generally more active during vertical climbing motions than during other common positional behaviors, implying that it is for this behavior that the large size of these muscles has been maintained (Jungers and Stern, 1980,1981, 1984). Such a conclusion assumes that the kinematics of vertical climbing are not found in other important (= high frequency) positional behaviors. Some movements typical of vertical climbing are also common during arm-hanging, and muscles associated with these movements may be adapted to both. Kmematics, positional mode frequency, muscle size, and muscle activity may be considered together to address this issue.

Relative muscle size, when considered with information on limb motion and EMG activity during common positional behaviors such as vertical climbing, quadrupedal walking, arm-hanging, and arm-raising (either protraction or abduction), suggests the adaptive function of muscle specializations in chimpanzees (summarized in Table 4). It is presumed that muscles that are active during a positional mode shown to be selectively important in chimpanzees, that are particularly large in chimpanzees, and that are not active in any other common behavior are evolved for or maintained for that positional behavior. If exactly the same muscles are active in two or more behaviors, each with similar selective importance, large muscle mass is likely to be adapted to all of those behaviors.

Several hypotheses are supported. A flexor of the elbow (biceps brachii) and a major humeral retractor (latissimus dorsi) are unambiguously correlated with vertical climbing alone (VC, Table 4). Teres minor, middle caudal serratus anterior, and cranial trapezius are unambiguously correlated with arm-raising, a motion observed both during the swing phase of vertical climbing and in reaching out for food while arm-hanging (VC, AH, Table 4). Intermediate deltoid is active in abduction, not protraction, and therefore is suggested to be an adaptation to reaching out during arm-hanging (AH, Table 4).

In some cases precise comparisons between apes and monkeys muscle masses or EMG data during critical behaviors are un- available, but likely adaptations are suggested (positional mode keys followed by a question mark, Table 4). Although separate

quantitative data on relative size of cranial and caudal pectoralis major are lacking, the greater size of the entire muscle suggests both are relatively large in apes. Caudal pectoralis major and pectoralis minor are most active during humeral retraction in the support phase of vertical climbing, and are therefore probably adaptations to vertical climbing. Likewise, if posterior deltoid is larger in chimpanzees, it is associated with vertical climbing. Cranial pectoralis was active in rapid non-weight-bearing protraction of the arm during climbing; it may also aid in reaching out during feeding. Lowest caudal serratus anterior is active during both arm- hanging and arm-retraction and may function to fix the lower scapula to the torso against cranialward suspensory forces. Bra- chialis and brachioradialis, elbow flexors, are active during humeral retraction and are therefore probably adapted to climbing, but EMG data are missing.

CONCLUSIONS

Chimpanzee positional behavior, considered in light of the mechanical arguments above and previous research on EMG activity and relative muscle mass, provides strong support for the contention that most osteoligamentous specializations of the chimpanzee upper body are adaptations to arm-hanging and most muscular specializations are adaptations to vertical climbing (cf. Tuttle and Basmajian, 1977; Preuschoft and Demes, 1984; Hollihn, 1984).

Long, narrow scapulae, cone-shaped rib cages, robust clavicular anchors, anteropos- teriorly flattened thoraxes (and accompanying strongly curved ribs), mobile, abductible humeri, wide manubria of the sterna, and cranially oriented glenoid fossae are hypothesized to be a functionally related adaptive complex related to arm-hanging. These features are hypothesized to have evolved to reduce muscular activity and ligamentous and skeletal strain during unimanual suspension. The lack of a tail reflects the relative unimportance of leaping in chimpanzees. Liberal ulnar deviation of the manus, long, curved metacarpals and phalanges, and a short lumbar region are likely to be adaptations to both vertical climbing and arm-hanging.

Large elbow flexors and humeral retractors are best explained as adaptations to vertical climbing (Stern et al., 1977; Fleagle et al., 1981). Humeral protractors are likely to be adaptations to arm-raising both during

TAB

LE 4. M

uscl

e si

ze a

nd f

unct

ion

in c

him

panz

ees

Act

ive

in

Lar

ger

Act

ive

duri

ng

Act

ive

Act

ive

Lik

ely

in

hum

eral

du

ring

du

ring

pr

otra

ctio

n M

uscl

e ad

apta

tion

? ch

imps

? re

trac

tion?

w

alki

ng?

arm

-han

ging

? or

abd

uctio

n?

Bic

eps b

rach

ii

Bra

chia

lis

Bra

chio

radi

alis

D

elto

id (

who

le)

-ant

erio

r -i

nter

med

iate

-p

oste

rior

In

fras

pina

tus

Lat

issi

mus

dor

sii

Pect

oral

is m

ajor

-c

lavi

cula

r -s

tern

acos

tal

Pect

oral

is m

inor

R

hom

boid

s Se

rrat

us a

nter

ior

-mid

dle

caud

al

-low

est c

auda

l Su

bsca

pula

ris

Supr

aspi

natu

s T

eres

-m

ajor

Tra

pezi

us c

rani

al

Tri

rpns

-min

or

caud

al

vc

VC

? V

C?

VC

, AH

? A

H

VC

? 0 vc

V

C,A

H?

VC

?

+++a

++

8,-1

0

+++I

34

+++Z

0' -4

+++9

+8,1

7,-1

0

++;1

,16

0 0'

X

+2

VC

,AH

++

I3

VC

,AH

++

'.9

0 -4

VC

,AH

+4

X ++

4 n

--9

0 01

, ++

2,6

--

0 01

,4 '

VC,

AH

++

1.4.

9

4

-(11j

.15

--11

1).1

5 -(

11).1

5 --

(11)

.15

+++6

.'4

++&

I4

++I4

+6

J4

--I4

+(5)

,6

++15

),6,1

4

++6

+14

--14

+(l

I),l

S

(-3.

5)

Sim

plif

icat

ions

and

inte

rpre

tati

ons w

ere

mad

e in

com

pilin

g th

is re

view

. Mus

cle c

ompa

riso

ns w

ith

Old

Wor

ld m

onke

ys w

ere

ofte

n m

ade

with

ape

dat

a po

oled

. Det

ails

are

give

n be

low

. Mos

t EM

G d

ata

are f

or c

him

panz

ees,

but w

here

chi

mpa

nzee

data

are

unav

aila

ble

data

from

oth

er a

pes a

re of

fere

d (i

n pa

rent

hese

s). W

here

resu

lts a

redi

amet

rica

lly

oppo

sed,

twov

alue

s ar

e giv

en;

an a

ttem

pt w

as m

ade

to g

ive

a si

ngle

val

ue if

pos

sibl

e. L

ikel

y ad

apti

on (b

old

face

): a

n ad

apti

on to

a s

ingl

e po

sitio

nal

beha

vior

is s

ugge

sted

. Und

erlin

e: a

dapt

ion

to tw

o be

havi

ors

sugg

este

d. P

osit

iona

l mod

e fol

low

ed by

a q

uest

ionm

ark:

som

e dat

a mis

sing

, but

ada

ptio

n lik

ely.

0: m

uscl

e siz

e sm

alle

r in

apes

, so

no b

ehav

iora

l spe

cial

izat

ion

iden

tifia

ble;

X t

oo li

ttle

data

, or

not d

istin

ctiv

e. V

C: v

ertic

al c

limbi

ng, A

H: r

each

ing

duri

ng a

rm-h

angi

ng. E

MG

act

ivit

y: ++

+, m

arke

d in

mos

t or a

ll st

udie

s; ++

, vari

ably

hig

h (b

y st

udy

or e

xper

imen

t) o

r con

sist

ently

m

oder

ate;

+, lo

w 0

rvar

iabl

ymod

erat

e;-,

ina

ctiv

einm

osts

tudi

esor

very

low

act

ivity

; --,

inac

tive

in

all s

tudi

es. M

uscl

esiz

e: ++

+, m

uchl

arge

rin

apes

bym

ostm

easu

res;

++, la

rger

in a

pes

by m

ost m

easu

reso

rlar

geri

n m

osta

pes;

+,s

omew

hatl

arge

rin

apes

bym

ostm

easu

res;

0, n

olar

geri

nape

s or

var

iabl

eacc

ordi

ngto

mea

sure

; -,s

mal

leri

n ap

esor

vari

ably

smal

lera

ccor

ding

to

mea

sure

; --,

muc

h sm

alle

r in

apes

in m

ost

stud

ies.

'A

shto

n an

d O

xnar

d, 1

963(

apes

); W

orru

ccin

i and

cioc

hon,

197

6;"F

leag

leet

al.,

1981

(gib

bons

); 'I

nman

et a

l., 19

44 (m

uscl

ecom

pari

son f

or c

him

ps ag

ains

t oth

er p

rim

ates

; EM

G o

n hu

man

s on

ly);

5Jun

gers

ands

tern

, 1980,1984(gibbons);6Larson an

d St

ern,

l986,1987(chimps);'Larsonet

al.,

1991

(chi

mps

);R

Mill

er, 1

932(

chi1

nps)

;~O

xnar

d, 1963(apes);'"Swindlerand W

ood,

198

2 (c

him

p co

mpa

red

to P

upio

); I'

Tut

tle a

nd B

asm

ajia

n, 1

974 (

gori

lla)

; 12T

uttle

and

Bas

maj

ian,

197

7 (gr

eat a

pes)

; '3T

uttle

and

Bas

maj

ian,

197

8a (c

him

ps u

nles

s in

pare

nthe

ses)

; "T

uttl

e an

d B

asm

ajia

n, 1

9781

3 (c

him

ps);

'jT

uttl

e et

al.,

197

7; I6

Zieg

ler,

1964

.


vertical climbing and arm-hanging. High frequencies of arm-hanging and vertical climbing support the hypothesis that large digital flexors and an iliac origin of latissimus dorsi are adaptations to both behaviors. A humeral abductor (intermediate deltoid) appears to be adapted to reaching out during suspensory food gathering. A high intermembral index may increase reach into the terminal branches while retaining a low center of gravity and reducing body weight. Although the relatively low activity of most muscles during brachiation (sensu stricto) and low frequencies of suspensory locomotion preclude a general hominoid muscular brachiating adaptation, skeletal and ligamentous adaptations for suspensory posture still may function similarly during suspensory locomotion.

Humerus-abducted suspensory behaviors (predominantly unimanual arm-hanging) and vertical climbing are the shared, distinctive positional behaviors of the apes (Hunt, 1991a). This suggests that muscular specializations shared by all apes may be adaptations to vertical climbing and reaching out during arm-hanging, and that hominoid skeletal synapomorphies are principally adaptations to arm-hanging.

ACKNOWLEDGMENTS

This work benefited from comments by C.L. Brace, J.G.H. Cant, J.G. Fleagle, M.G. Hunt, F.A. Jenkins Jr., F.B. Livingstone, D.J. Meldrum, D.R. Pilbeam, R.L. Susman, R.H. Tuttle, D.P. Watts, R.W. Wrangham, and two anonymous reviewers. The Univer- sity of Michigan Museum of Anthropology and the Harvard University Department of Anthropology provided financial support and facilities during preparation. R.W. Wrangham provided additional support. Re- search was aided by grants from the Horace C. Rackham Graduate School (U.M.), Sigma Xi, the Leakey Foundation, and National Science Foundation grant BNS-86-09869.

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