Telemetered Electromyography of Flexor Digitorum Profundus and Flexor Digitorum Superficialis in Pan troglodytes and Implications for Interpretation of the 0. H. 7 Hand RANDALL L. SUSMAN AND JACK T.STERN, JR. Department of Anatomical Sciences, School of Basic Health Sciences, Health Sciences Center, S. U.N. Y. Stony Brook, Stony Brook, New York 11 794
K E Y WORDS EMG
Pan troglodytes
.
Ape locomotion
.
Olduvai Hominid 7
ABSTRACT The importance of knuckle-walking in the locomotor repertoire of African apes raises the possibility that the long digital flexors may be specially adapted more to meet the demands of ground quadrupedalism than those of suspension. To investigate this possibility, the activities of the flexor digitorum superficialis and flexor digitorum profundus were studied by means of telemetered electromyography in three chimpanzees. Results clearly indicate that the fasciculi of these muscles to digits bearing weight in knuckle-walking are not called upon to contract in quadrupedal postures or in slow and moderately fast quadrupedal locomotion except t o help clear the fingers from the ground as the forelimb begins its recovery stroke. At the most rapid speeds, a slight t o moderate level of activity sometimes occurs in the latter half of stance phase. The long digital flexors display maximum and sustained activity during suspension. It is concluded that any role for these muscles in maintenance of stability a t the metacarpophalangeal joints during knuckle-walking must be predominantly passive. Prominent markings for insertions of these muscles in a fossil hand (such as O.H. 7) suggest use of the forelimb in suspensory climbing behaviors. The adaptation of the hands of African apes for their unique type of quadrupedal locomotion - knuckle-walking - has raised problems both for the functional morphologist and theorist of human evolution (Tuttle, '67, '69, '74; Lewis, '69, '72). Structures thought to be related to suspensory behavior may in fact be suited for quite the opposite. Similarities between hominid ancestors and the African apes need no longer be considered to support some version of a "brachiator" stage in human evolution. In the face of powerful evidence (Tuttle, '67, '69) that the hands of gorillas and chimpanzees do not function as passive hooks, there can be no surprise in the suggestion that the extrinsic flexors of the fingers (flexor digitorum superficialis = FDS and flexor digitorum profundus = FDP) are important in suspensory activities involving the forelimb. However, Tuttle ('72) has raised the interestAM. J. PHYS. ANTHROP. (1979)50: 565-574.
ing possibility that prominence of the FDS could also be related to a role for this muscle in knuckle-walking, and Preuschoft ('73) concluded that contraction of the extrinsic finger flexors would be required to maintain equilibrium a t the metacarpophalangeal joint during normal quadrupedal postures and locomotion in the African apes. This issue takes on a greater significance if one postulates knucklewalking as a major component of pre-hominid behavior (Washburn, '681,since a fossil hand (O.H. 7 ) from Olduvai Gorge shows particularly strong impressions for the insertion of FDS. In order to determine the role of the extrinsic finger flexors in knuckle-walking, and to assess the importance of osseoligamentous structures in maintenance of stability a t the wrist and metacarpophalangeal joints, Tuttle and co-workers (Tuttle et al., '72; Tuttle and Basmajian, '74, '75) have conducted electromyographic experiments on a juvenile gorilla.
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RANDALL L. SUSMAN AND JACK T. STERN, JR.
As acknowledged by the authors, the interpretation of results (particularly for FDS) is complicated by inexplicable variability. Nonetheless, the studies suggest the possibility of a significant role for FDS fasciculi to weight bearing digits in the stance phase of knuckle-walking. In one instance of quadrupedal locomotion, there occurred “evidence of notable propellent flexion of metacarpophalangeal joints 11-IV just prior to release into swing phase” (Tuttle et al., ‘72). FDP nearly always exhibited only low EMG potentials during knuckle-walking progression, but occasionally at brisk or moderate paces, higher levels of activity occurred. The recruitment of the extrinsic flexors in knuckle-walking was notably less than in some instances of suspensory behavior and voluntary grasping. We have extended electromyographic study of extrinsic finger flexors to the chimpanzee in order to clarify some of the remaining ambiguities about the role of these muscles in locomotion. We hope to shed light on (1)the degree to which evolution of these muscles in African apes has been determined by the demands of knuckle-walking, and (2) the adaptations of the hominid hand (O.H. 7) from Olduvai Gorge. MATERIALS AND METHODS
The technique of telemetered electromyography employed by us has been described elsewhere (Stern e t al., ’77).The advantage of this method is that it enables the unfettered subject to engage in a wide variety of dynamic behaviors on complex substrates. Since there is considerable independence between the digits as employed by the chimpanzee in its diverse activities, it was essential that we determine exactly into which digitation of FDS or FDP our electrodes were placed. To this end a stimulating current was
passed through each electrode following its insertion. By observing which digit moved and the nature of this movement, it was possible t o establish unequivocally in which muscle and fasciculus the electrode was situated. Attempts to judge electrode placement through manipulation of joints gave highly unreliable results. Our subjects consisted of three subadult Pan troglodytes: a female weighing approximately 32 kg (Subject A), a 20-kg male (Subject B), and a male weighing 9.5 kg (Subject C). Subjects A and B were wild caught but captive since November 1976. Subject C was born at the Yerkes Regional Primate Research Center in May 1974. All three subjects exhibited normal features of chimpanzee posture and locomotion without evidence of any musculoskeletal or neurological impairment. Subject C showed greater variability in hand postures during knuckle-walking than did the wild caught animals. For one year preceeding the experiments the subjects were housed in large quarters with a variety of apparatus permitting a full range of locomotor behaviors. Experiments were conducted in either a large cage enclosure or in a large room. The subjects were allowed t o move freely and were encouraged a t times to climb, armswing, or knuckle-walk a t various speeds. Apparatus included a vertical trunk (6.0 cm in diameter), vertical ropes (1.35 cm and 3 cm), a horizontal rope (1.35 cm), and a ladder with 5 X 10 cm rails and 2.5 cm diameter dowl rungs. The floor surfaces were painted concrete or ceramic tile, sometimes covered with pine shavings. Recording started when the subjects had regained normal patterns of movement and coordination following halothanel nitrous oxide anesthesia. Table 1presents a list of the muscles studied in the five experiments reported in this paper.
TABLE 1
Muscles studied in each experiment Experiment 1 Subject B (20kg o?
Experiment 2 Subject C
FDS IV FDS IV FDP V
FDS I11 FDP 111 FDS IV FDP I V
(9.5kgd)
Experiment 3 Subject C (9.5kg d)
Experiment 4 Subject B (20kg d)
Experiment 5 Subject A (32kgYj
FDP I1 FDS 111 FCR
FCR FDS IV FDP IV FDP V
FCR FDS IV FDP IV
FCR, flexor carpi radialis; FDP, flexor digitorum profundus; FDS, flexor digorum superficialia.
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EMG OF CHIMPANZEE FINGER FLEXORS
Morphological notes on flexor digitorum profundus and flexor digitorum superficialis FDP In chimpanzees flexor digitorum profundus consists of four partially distinct fasciculi inserting into the bases of distal phalanges 11-V on their palmar surfaces. Fasciculus 11 normally originates on the radius and interosseous membrane while 111, IV, and V emanate from the ulna and interosseous membrane (Keith, 1894).Often fasciculi (especially those t o digits 111 and IV) cannot be separated accurately (Keith, 1894; Susman, personal observation) and sometimes they are joined by a tendinous shunt (Susman, personal observation). In humans the radial portion of the deep flexor has an insertion on the pollical distal phalanx, but in great apes this segment of the muscle inserts mostly on the index finger.
At slow and moderately fast speeds there is no significant activity of FDP IV during the support phase (fig. 1).Rarely one or two small spikes occur a t mid-stance (i.e., when the
KNUCKLE -WALKING
*-+
Support
FDS The flexor digitorum superficialis of the chimpanzee is represented by four distinct fasciculi with tendons to rays 11-V. Apes and humans possess both ulnar and radial origins of this muscle in addition to the epicondylar origin found in other primates. The bifurcate insertion into the margins of the palmar surface of the middle phalanx is constant in all primates. Most variability in the structure of FDS within the Hominoidea is found in the origin and grouping of individual fasciculi. Tuttle ('72) compared the relative weights of the forearm and other muscles in a representative series of anthropoid primates. In the Old World monkeys the FDS is much smaller than FDP (FDS/FDP ranges from 0.27 in T. gelada to 0.39 in Cercocebus atys). Among pongids the FDS is approximately 0.70 times as large as FDP, and the proportion in humans (0.63) is similar. Hylobatids have relatively the largest FDS, i t being roughly equal in mass to FDP (FDS/FDP = 0.88 in HyEobates sp. and 0.99 in siamang). RESULTS
Flexor digitorum profundus IZ, HI, IV, Knuckle-walking In our chimpanzees the weight was borne by digits 111 and IV during knuckle-walking. We recorded the activity of FDP IV in all subjects, but that of FDP I11 only in Subject C.
v
Swine
FCR --
FDS IV
1
FDP IV
Fig. 1 An example of EMG from experiment 4 illustrating muscle activity during moderately fast knucklewalking in a male chimpanzee, Subject B. Channel 1 flexor carpi radialis, 2 - FDS IV, 3 - FDP IV, 4 - FDP V. Observe absence of activity in FDS IV and FDP IV during support phase and small burst that follows onset of swing phase. This burst often occurs earlier, at or just preceding the transiton from support to swing. The experiments in which FDS 111 and FDP 111 were studied show their activities to be essentially the same as the fasciculi to the fourth digit. The only difference is t h a t FDS 111 and FDP 111 contract slightly after FDS IV and FDP IV when the hand is held parallel to the direction of movement during the stance phase. This difference can be correlated to the earlier removal of digit IV from the substrate. The single experiment on FDP I1 revealed its activity in knuckle-walking to be very similar to that depicted here for FDP V.
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RANDALL L. SUSMAN AND JACK T. STERN. JR.
shoulder is directly above the point of contact of the hand with the ground). Commonly a burst of slight activity occurs in these fasciculi as the hand is lifted from the ground at the onset of swing phase (fig. 1).In subjects A and C such a burst was observed during virtually every episode of knuckle-walking in which the hand was held on the ground with its palm parallel to the line of progression. Its occurrence in Subject B was less frequent. When subjects A and C walked with the hand perpendicular to the direction of movement (a behavior not observed in Subject B) the burst usually failed to appear. This fact, and a careful examination of the timing of events, point clearly to a function of FDP IV in lifting the finger from the ground as opposed to propulsion. In subjects A and C, there occurred quite consistently a short burst of activity in FDP IV at mid-stance during the most rapid bouts
Suspension by forelimb
of knuckle-walking. The burst was of modera t e amplitude i n Subject C, whose wrist appeared to dorsiflex at such times (Jenkins and Fleagle, '75, noted 10-15" of dorsiflexion in their chimpanzees during stance phase of knuckle-walking). In Subject A, the mid-
-
FAST KNUCKLE-WALKING Swing
Suplort
Swin;
I
Support
Swing
Fig. 2 Flexor digitorum profundus IV in female chimpanzee (Subject A) during rapid knuckle-walking. Note the occurrence of slight activity in the muscle in late stance, followed by a larger burst prior to and during early swing phase.
Release of grasp followed by voluntary movement
I
FCR
FDS IV
FDP IV
FOP V .
I
-
Fig. 3 Activity of the same muscles as in figure 1 while Subject B was suspended by one forelimb. Activity observed represents maximum potential exhibited in this experiment.
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EMG OF CHIMPANZEE FINGER FLEXORS
stance burst during rapid progression was never of more than slight amplitude and was always smaller than the activity correlated with onset of swing (fig. 2). A few spikes appeared occasionally a t mid-stance in Subject B when moving quickly. In two instances in which Subject C dropped from a bipedal to tripedal stance, FDP IV exhibited moderate activity upon contact of the hand with the ground. The experiment in which data were obtained for FDP I11 showed that its behavior during knuckle-walking is identical to that of FDP IV with one exception. When the hand is held on the ground with its palm parallel to the line of progression, the burst which occurs in FDP I11 as the hand is lifted from the ground follows slightly that of FDP IV. This
-
difference can be correlated with the earlier removal of digit IV from the substrate. The fasciculus of FDP to digit V differs from those to digits I11 and IV by very often showing slight to moderate potentials during the support phase (chiefly its first half) of knuckle-walking (fig. 1). Such activity also occurs occasionally in FDP 11. Since digits I1 and V are not weight bearing during knuckle-walking in the chimpanzee, it suggests that this action functions to clear them from the ground. As with FDP I11 and IV, the fasciculi to digits I1 and V commonly exhibit activity a t the onset of swing phase when the hand is parallel to direction of movement (fig. 1.) At no time during quiescent quadrupedal and tripedal standing was significant activity of any fasciculus of FDP noted.
GRASP OF ORANGE
Pressing orangs against incisors
FDP IV
D
Fig. 4 Subject C holding an orange. Note absence of activity of FDS 111, FDP 111 and FDP IV except when fruit is forced against the incisor teeth. Activity of FDS IV persists while the orange is held after the bite has occurred.
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RANDALL L. SUSMAN A N D JACK T. STERN. JR.
Scratching thigh .
.
Scratching thigh
I
.
t
.
FDS IV
s
FDP IV
FDP V
Fig. 5 Same muscles as represented in figure 1. The level of activity of the extrinsic digital flexors in scratching is greater than in any incidence of knuckle-walking.
Suspensory behavior The four fasciculi of FDP display maximum potentials during climbing the vertical trunk and ropes and in suspension from the horizontal rope and ladder (fig. 3). During certain behaviors in which the hand loosely grasps the side of the wire cage independent activity of individual fasciculi occurs. Manipulation The fasciculi are variably active, usually at no more than a moderate level, during manipulation of small and large fruits. Often absence of potentials in a particular fasciculus could be correlated with the fact that its corresponding digit was not employed in the grasp. Of the fasciculi tested, FDP I1 was the most active in manipulation. It showed frequent moderate potentials while the subject
held and ate an orange, and slight potentials when a cylindrical object (6.4 cm diameter) was lightly grasped. However, periods of electrical silence in FDP I1 also occurred in these circumstances. When holding an orange in the hand such that digits I1 and I11 were employed in opposition to the thumb and digit IV was slightly flexed so that it was partially underneath the orange, FDP 111 and IV were silent. Both became moderately active only when the orange was forced against the incisors (fig. 4). In some instances of manipulation, and during scratching (fig. 5) the level of activity of FDP was greater than in any episode of knuckle-walking. Flexor digitorum superficialis ZZZand ZV Knuckle-walking The activity of the faciculi of FDS to digits
EMG OF CHIMPANZEE FINGER FLEXORS
571
tive of the absence of any noteworthy role for FDS in stance phase of all but the most rapid episodes of knuckle-walking. Suspensory behavior During very fast knuckle-walking in two of FDS displayed its maximum potentials dur- our subjects, slight to moderate potentials ing climbing t h e vertical trunk and ropes, and were exhibited by the extrinsic flexors of the in suspension from the horizontal rope and weight bearing digits in stance phase. Tuttle ladder (fig. 3). In such cases the activities FDS et al. ('72) interpret one instance of FDS activand FDP are essentially synchronous. During ity during stance phase as being related to certain behaviors in which the hand grasped propellent flexion of the metacarpophalangeal the side of the wire cage, brief periods of inde- joints. This may be the case for gorillas in pendent activity of FDS or FDP occurred, but which the hand is habitually placed perpenwe are unable to correlate these with the digi- dicular to the direction of movement (Tuttle, '67, '69) but we doubt this interpretation aptal position. plies to the chimpanzee because flexion of the Manipulation digits ought not to generate propellant force In manipulation, FDS usually operates si- when the hand is held parallel to the line of multaneously with FDP, but occasionally the progression. It is not possible to say if the actwo muscles may operate independently (fig. tivity we observed serves the function of 4). We could not relate episodes of indepen- maintaining stability of the metacarpophadent activity to either object dimension or langeal joints, or the wrist joints, or both. The consistency. However, in the example of eat- greater amplitude of the potentials in Subject ing an orange described above, FDS IV re- C whose wrist seemed to yield into dorsiflexion mained active even when the fruit was held at high speed, is suggestive of a role for the long finger flexors in support of the wrist. without being forced against the teeth. Activity of both extrinsic digital flexors at The activity of FDS in scratching is much greater than in any episode of knuckle-walk- t h e end of stance phase occurs commonly but is quite obviously related simply to lifting of ing (fig. 5). the fingers and hand from the ground. DISCUSSION Absence of any major active role of FDP and The prominent activity of the extrinsic FDS in the weight bearing phase of knucklefinger flexors in suspensory behavior involv- walking does not preclude important coning the forelimb is not surprising. It supports tribution of these muscles in passive or theoretical expectations, but does not entirely rheological support of the wrist and metacarconfirm the variable results of Tuttle and Bas- pophalangeal joints. Long et al. ('64) note that majian ('75). The absence of a n active role for rheologic (or viscoelastic) forces are importhese muscles during the stance phase of slow t a n t for hand control in humans for either and moderately fast knuckle-walking is unex- assisting or countering certain motions. They pected given their positions and potential for cite the FDS of humans as evidence for this maintaining equilibrium a t the metacarpo- point. With full dorsiflexion of the wrist, the phalangeal joints (Preuschoft, '73). Tuttle e t extrinsic flexors are at maximum stretch and al. ('72) and Tuttle and Basmajian ('74, '75) the long superficial flexors exhibit little activstressed the minor role of FDP in knuckle- ity. With increasing palmar flexion, the long walking in the gorilla, but report a more com- flexors are increasingly activated. Long et al. mon occurrence of low levels of activity during ('64) postulate that while the wrist is in dorstance phase than we observed among chim- siflexion t h e flexor digitorum superficialis panzees. In our studies, stance phase activity contributes force through its viscoelastic of FDP was mostly confined to the fasciculi to properties alone. As the wrist is flexed the extensors increase their tension so that the flexdigits I1 and V, which did not bear weight. Tuttle and Basmajian ('74) reported one ex- ors not only must actively compensate for periment in which FDS to a weight bearing reduced viscoelastic force, but also must digit was rather active in the stance phase of counter the effect of the opposing extensors. Straus ('40) emphasized the shortening of knuckle-walking and a second experiment in which no significant potentials were seen. the flexor digitorum profundus and superfiThey judge the first result more likely to be Rheological forces include elasticity, viscosity, friction and valid, but our observations are clearly suppor- plasticity. I11 and IV during knuckle-walking is the same as those of FDP (fig. 1).
I
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RANDALL L. SUSMAN A N D JACK T. STERN, JR.
cialis in the great apes and related this phenomenon to hook-grasp during suspension.2 However, orangutans (and hylobatid apes) do not possess “shortened flexors” (Tuttle, ’69). The shortened flexors in the African apes suggest the possibility of a rheologic role for the extrinsic finger flexors in knuckle-walking hand postures in which the wrist is in line with the forearm or slightly dorsiflexed, and in which the proximal phalanges are hyperextended. Tuttle and Basmajian (’74) suggest that “tendonization” of the long digital flexors may account for the “shortness” of these muscles in African apes. Tendinization need not be associated with a “shortness” of a muscle if one means by the latter term that joints are still quite flexed when the stretch of the muscle first begins to elicit passive resistance. On the other hand, if the actual contractile portions of the long digital flexors are short, then the passive length-tension curve will rise steeply upon extension of the joints. The same effect will occur if the muscles are highly pinnate. Dissections of two chimpanzees and two orangutans did reveal that pinnation of the FDS I11 and IV is greater in the chimpanzee (Susman, personal observation). The conclusion to be reached from these considerations is that absence of anactive role for the long flexors in the support phase of slow and moderately fast knuckle-walking and the low level of such activity in rapid movement does not preclude the possibility that these muscles provide substantial passive forces to support the hand against ground reaction forces encountered in knuckle-walking (Tuttle, ’67; Tuttle et al., ’72; Susman, ’79). Olduvai Hominid 7 hand The Olduvai Hominid 7 hand, first described by Napier (‘621, exhibits exceptionally large areas for insertion for FDS on the middle phalanges. The impressions for this muscle are greater in relative area than in any living ape or modern humans (fig. 6). In addition other pongid affinities are noted in t h e following features: (a) the curvature of the proximal and middle phalanges, (b) the stout, robust proportions of the middle phalanges, and (c) the thickened cortices of middle and proximal phalanges. Although the middle phalanges are unique, they compare most closely with those of gorillas among the extant Hominoidea (Napier, ’62; Susman and Creel, ’79).
The proximal phalangeal fragments are most like those of chimpanzees among extant Hominoidea. The distal phalanges, however, (FLK NN-B, C) are most similar to those of modern humans on the basis of a variety of multivariate statistical comparisons (Susman and Creel, ’79). We infer the functional capacities of O.H. 7 to include suspensory behaviors on the basis of both osteological and experimental evidence. EMG data suggest the recruitment of FDS in powerful grasping and to a lesser extent manipulation. The sign t h a t this was a well developed muscle in the fossil argues for some degree of climbing or other arboreal activity in hominids a t this time. We cannot attribute a large flexor digitorum superficialis muscle primarily to selection for manipulation for two reasons: (1) judged by its markings the muscle is apparently larger in O.H. 7 than in modern humans but we can reasonably assume that manipulation has increased in importance in the last 1.76 million years in the hominid line, and (2) the most suspensory hominoids, the Hylobatidae, have the largest flexor digitorum superficialis muscles (Tuttle, ’72) and they are far less dextrous than humans and no more so than the African apes. Evidence exists that Plio-Pleistocene hominids retained long forelimbs (Taieb et al., ’75; McHenry, ’781, but we do not feel that the suspensory features of the O.H. 7 hand indicate simply a primitive retention of pongidlike features (McHenry, ’78). Secondary osteological features such as large muscle insertions on the middle phalanges may be gained or lost ontogentically or as a result of mechanical or systemic aberrations within an animal’s lifetime. No doubt they would be quickly lost in animals which did not utilize them. If we are correct, then early hominids may have retained a capacity for climbing even past the point a t which t h e foot became adapted for bipedalism. ACKNOWLEDGMENTS
We thank t h e following people for their help in various supportive and technical roles: Ms However, like many others, Straus mcorrectly lumped orangutans with the chimpanzee and gorilla with respect to knucklewalking. The identification of these bones has been revised by Duy (‘76). The O.H. 7 hand now includes a capitate fragment, trapezium, scaphoid. fragmentary second metacarpal, 3 distal phalanges, 2 fragmentary proximal phalanges, and 4 middle phalanges. All this material, with the exception of the capitate, may represent the right hand of a single individual.
EMG OF CHIMPANZEE FINGER FLEXORS
573
Fig. 6 Middle phalanges of O.H. 7. FLK NN-G, E, F, D rays V, IV, 111, 11, respectively (left to right). Note missing epiphyses and the large impressions for the insertion of the flexor digitorum superficialis muscle on the palmar surfaces (below).
Marcy Koltun, Mr. William Korosh, Ms Lorraine Rice, Ms. Sukie Davis, and Mr. Phillip Vollono. We also thank Sue Savage-Rumbaugh and the staff of the Yerkes Regional Primate Center for their cooperation and support of this project. The illustrations were prepared by Ms Lucille Betti and Ms Joan Kelly typed the manuscript. This work was supported by NSF Grant BNS 76-83114 and by a General Research Support Grant from N.I.H. administered by the School of Basic Health Sciences, S.U.N.Y., Stony Brook. Study of 01duvai Hominid 7 was made possible by a grant to R. L. Susman from the L. S. B. Leakey Foundation and from the Henry Hinds Fund, Com-
mittee on Evolutionary Biology, University of Chicago. We are grateful to all of these individuals and organizations for their support. LITERATURE CITED Day, M. H. 1976 Hominid postcranial material from Bed I. Olduvai Gorge. In: Human Origins. G. Issac and E. McCowan, eds. W.A. Benjamin, Menlo Park, California, pp. 363-374. Jenkins, F. A,, Jr., and J. G. Fleagle 1975 Knuckle-walking and t h e functional anatomy of the wrists in living apes. In: Primate Functional Morphology and Evolution. R. H. Tuttle, ed. Mouton Publ., Hague, pp. 213-227. Keith, A. 1894 The Myology of the Catarrhini: A Study in Evolution. Doctoral Thesis, university of Aberdeen. Lewis, 0. J. 1969 The hominoid wrist joint. Am. J. of Phys. Anthrop., 30: 251-268.
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1972 Evolution of the hominoid wrist. In: Functional and Evolutionary Biologyof Primates. R. H. Tuttle, ed. Aldine-Atherton, Chicago, pp. 207-222. Long, C., D. Thomas and W. J. Crochetiere 1964 Viscoelastic factors in hand control. Proc. IVth Intl. Cong. Phys. Med., Paris, pp. 440-445. McHenry, H. M. 1978 Fore- and hindlimb proportions in plio-Pleistocene hominids. Am. J. of Phys. Anthrop., 49: 15-22. Napier, J. R. 1962 Fossil hand bones from Olduvai Gorge. Nature, 196: 409-411. Preuschoft, H. 1973 Functional anatomy of the upper extremity. In: The Chimpanzee. Vol. 6. G. H. Bourne, ed. Karger, Basel, pp. 34-120. Stern, J. T., Jr., J. P. Wells, A. Vangor and J. G. Fleagle 1977 Electromyography of some muscles of the upper limb in Ateles and Lagothrix. Yrbk. Phys. Anthro., 20: 498-507. Straus, W. L. 1940 The posture of the great ape hand in locomotion, and its phylogenetic implication. Am. J. Phys. Anthrop., 27: 199-207. Susman, R. L. 1979 Comparative and functional morphology of hominoid fingers. Am. J. Phys. Anthrop., 50: 215-236. Susman, R. L., and N. Creel (1979, ,submitted) Functional and morphological affinities of t h e subadult hand (0.H. 7) from Olduval Gorge. Am. J. Phys. Anthrop. Taieb. M., D. C. Johanson and Y. Coppens 1975 Exp6dition
internationale de l'afar Ethiopie (3e campagne 1974): decourverte d'hominides plio-pleistocenes a Hadar. C . R. Acad. Sci., Paris, 281: 1297-1300. Tuttle, R. H. 1967 Knuckle-walking and the evolution of hominoid hands. Am. J. Phys. Anthrop., 26: 171-206. 1969 Quantitative and functional studies on the hands of the Anthropoidea. I. The Hominoidea. J. Morph., 128: 309-364. 1972 Relative mass of cheiridial muscles in catarrhine primates. In: Functional and Evolutionary Biology of the Primates. R. H. Tuttle, ed. Aldine, Chicago, pp. 262-291. 1974 Darwin's apes, dental apes and the descent of man: normal science in evolutionary anthropology. Curr. Anthrop., 15: 389-398. Tuttle, R. H., and J. V. Basmajian 1974 Electromyography of forearm musculature in gorilla and problems related t o knuckle-walking, In: Primate Locomotion. F. A. Jenkins, ed. Academic Press, New York, pp. 293-347. 1975 Electromyography of Pan gorilla: a n experimental approach to the problem of hominization. Symp. 5th Cong. Intl. Primat. SOC.,pp. 303-314. Tuttle, R. H., J. V. Basmajian, E. Regenos and G. Shine 1972 Electromyography of knuckle-walking: results of four experiments on the forearm of Pun gorilla, Am. J. Phys. Anthrop., 37: 255-266. Washburn, S. L. 1968 The study of human evolution. Condon lecture, University of Oregon.
K E Y WORDS EMG
Pan troglodytes
.
Ape locomotion
.
Olduvai Hominid 7
ABSTRACT The importance of knuckle-walking in the locomotor repertoire of African apes raises the possibility that the long digital flexors may be specially adapted more to meet the demands of ground quadrupedalism than those of suspension. To investigate this possibility, the activities of the flexor digitorum superficialis and flexor digitorum profundus were studied by means of telemetered electromyography in three chimpanzees. Results clearly indicate that the fasciculi of these muscles to digits bearing weight in knuckle-walking are not called upon to contract in quadrupedal postures or in slow and moderately fast quadrupedal locomotion except t o help clear the fingers from the ground as the forelimb begins its recovery stroke. At the most rapid speeds, a slight t o moderate level of activity sometimes occurs in the latter half of stance phase. The long digital flexors display maximum and sustained activity during suspension. It is concluded that any role for these muscles in maintenance of stability a t the metacarpophalangeal joints during knuckle-walking must be predominantly passive. Prominent markings for insertions of these muscles in a fossil hand (such as O.H. 7) suggest use of the forelimb in suspensory climbing behaviors. The adaptation of the hands of African apes for their unique type of quadrupedal locomotion - knuckle-walking - has raised problems both for the functional morphologist and theorist of human evolution (Tuttle, '67, '69, '74; Lewis, '69, '72). Structures thought to be related to suspensory behavior may in fact be suited for quite the opposite. Similarities between hominid ancestors and the African apes need no longer be considered to support some version of a "brachiator" stage in human evolution. In the face of powerful evidence (Tuttle, '67, '69) that the hands of gorillas and chimpanzees do not function as passive hooks, there can be no surprise in the suggestion that the extrinsic flexors of the fingers (flexor digitorum superficialis = FDS and flexor digitorum profundus = FDP) are important in suspensory activities involving the forelimb. However, Tuttle ('72) has raised the interestAM. J. PHYS. ANTHROP. (1979)50: 565-574.
ing possibility that prominence of the FDS could also be related to a role for this muscle in knuckle-walking, and Preuschoft ('73) concluded that contraction of the extrinsic finger flexors would be required to maintain equilibrium a t the metacarpophalangeal joint during normal quadrupedal postures and locomotion in the African apes. This issue takes on a greater significance if one postulates knucklewalking as a major component of pre-hominid behavior (Washburn, '681,since a fossil hand (O.H. 7 ) from Olduvai Gorge shows particularly strong impressions for the insertion of FDS. In order to determine the role of the extrinsic finger flexors in knuckle-walking, and to assess the importance of osseoligamentous structures in maintenance of stability a t the wrist and metacarpophalangeal joints, Tuttle and co-workers (Tuttle et al., '72; Tuttle and Basmajian, '74, '75) have conducted electromyographic experiments on a juvenile gorilla.
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As acknowledged by the authors, the interpretation of results (particularly for FDS) is complicated by inexplicable variability. Nonetheless, the studies suggest the possibility of a significant role for FDS fasciculi to weight bearing digits in the stance phase of knuckle-walking. In one instance of quadrupedal locomotion, there occurred “evidence of notable propellent flexion of metacarpophalangeal joints 11-IV just prior to release into swing phase” (Tuttle et al., ‘72). FDP nearly always exhibited only low EMG potentials during knuckle-walking progression, but occasionally at brisk or moderate paces, higher levels of activity occurred. The recruitment of the extrinsic flexors in knuckle-walking was notably less than in some instances of suspensory behavior and voluntary grasping. We have extended electromyographic study of extrinsic finger flexors to the chimpanzee in order to clarify some of the remaining ambiguities about the role of these muscles in locomotion. We hope to shed light on (1)the degree to which evolution of these muscles in African apes has been determined by the demands of knuckle-walking, and (2) the adaptations of the hominid hand (O.H. 7) from Olduvai Gorge. MATERIALS AND METHODS
The technique of telemetered electromyography employed by us has been described elsewhere (Stern e t al., ’77).The advantage of this method is that it enables the unfettered subject to engage in a wide variety of dynamic behaviors on complex substrates. Since there is considerable independence between the digits as employed by the chimpanzee in its diverse activities, it was essential that we determine exactly into which digitation of FDS or FDP our electrodes were placed. To this end a stimulating current was
passed through each electrode following its insertion. By observing which digit moved and the nature of this movement, it was possible t o establish unequivocally in which muscle and fasciculus the electrode was situated. Attempts to judge electrode placement through manipulation of joints gave highly unreliable results. Our subjects consisted of three subadult Pan troglodytes: a female weighing approximately 32 kg (Subject A), a 20-kg male (Subject B), and a male weighing 9.5 kg (Subject C). Subjects A and B were wild caught but captive since November 1976. Subject C was born at the Yerkes Regional Primate Research Center in May 1974. All three subjects exhibited normal features of chimpanzee posture and locomotion without evidence of any musculoskeletal or neurological impairment. Subject C showed greater variability in hand postures during knuckle-walking than did the wild caught animals. For one year preceeding the experiments the subjects were housed in large quarters with a variety of apparatus permitting a full range of locomotor behaviors. Experiments were conducted in either a large cage enclosure or in a large room. The subjects were allowed t o move freely and were encouraged a t times to climb, armswing, or knuckle-walk a t various speeds. Apparatus included a vertical trunk (6.0 cm in diameter), vertical ropes (1.35 cm and 3 cm), a horizontal rope (1.35 cm), and a ladder with 5 X 10 cm rails and 2.5 cm diameter dowl rungs. The floor surfaces were painted concrete or ceramic tile, sometimes covered with pine shavings. Recording started when the subjects had regained normal patterns of movement and coordination following halothanel nitrous oxide anesthesia. Table 1presents a list of the muscles studied in the five experiments reported in this paper.
TABLE 1
Muscles studied in each experiment Experiment 1 Subject B (20kg o?
Experiment 2 Subject C
FDS IV FDS IV FDP V
FDS I11 FDP 111 FDS IV FDP I V
(9.5kgd)
Experiment 3 Subject C (9.5kg d)
Experiment 4 Subject B (20kg d)
Experiment 5 Subject A (32kgYj
FDP I1 FDS 111 FCR
FCR FDS IV FDP IV FDP V
FCR FDS IV FDP IV
FCR, flexor carpi radialis; FDP, flexor digitorum profundus; FDS, flexor digorum superficialia.
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EMG OF CHIMPANZEE FINGER FLEXORS
Morphological notes on flexor digitorum profundus and flexor digitorum superficialis FDP In chimpanzees flexor digitorum profundus consists of four partially distinct fasciculi inserting into the bases of distal phalanges 11-V on their palmar surfaces. Fasciculus 11 normally originates on the radius and interosseous membrane while 111, IV, and V emanate from the ulna and interosseous membrane (Keith, 1894).Often fasciculi (especially those t o digits 111 and IV) cannot be separated accurately (Keith, 1894; Susman, personal observation) and sometimes they are joined by a tendinous shunt (Susman, personal observation). In humans the radial portion of the deep flexor has an insertion on the pollical distal phalanx, but in great apes this segment of the muscle inserts mostly on the index finger.
At slow and moderately fast speeds there is no significant activity of FDP IV during the support phase (fig. 1).Rarely one or two small spikes occur a t mid-stance (i.e., when the
KNUCKLE -WALKING
*-+
Support
FDS The flexor digitorum superficialis of the chimpanzee is represented by four distinct fasciculi with tendons to rays 11-V. Apes and humans possess both ulnar and radial origins of this muscle in addition to the epicondylar origin found in other primates. The bifurcate insertion into the margins of the palmar surface of the middle phalanx is constant in all primates. Most variability in the structure of FDS within the Hominoidea is found in the origin and grouping of individual fasciculi. Tuttle ('72) compared the relative weights of the forearm and other muscles in a representative series of anthropoid primates. In the Old World monkeys the FDS is much smaller than FDP (FDS/FDP ranges from 0.27 in T. gelada to 0.39 in Cercocebus atys). Among pongids the FDS is approximately 0.70 times as large as FDP, and the proportion in humans (0.63) is similar. Hylobatids have relatively the largest FDS, i t being roughly equal in mass to FDP (FDS/FDP = 0.88 in HyEobates sp. and 0.99 in siamang). RESULTS
Flexor digitorum profundus IZ, HI, IV, Knuckle-walking In our chimpanzees the weight was borne by digits 111 and IV during knuckle-walking. We recorded the activity of FDP IV in all subjects, but that of FDP I11 only in Subject C.
v
Swine
FCR --
FDS IV
1
FDP IV
Fig. 1 An example of EMG from experiment 4 illustrating muscle activity during moderately fast knucklewalking in a male chimpanzee, Subject B. Channel 1 flexor carpi radialis, 2 - FDS IV, 3 - FDP IV, 4 - FDP V. Observe absence of activity in FDS IV and FDP IV during support phase and small burst that follows onset of swing phase. This burst often occurs earlier, at or just preceding the transiton from support to swing. The experiments in which FDS 111 and FDP 111 were studied show their activities to be essentially the same as the fasciculi to the fourth digit. The only difference is t h a t FDS 111 and FDP 111 contract slightly after FDS IV and FDP IV when the hand is held parallel to the direction of movement during the stance phase. This difference can be correlated to the earlier removal of digit IV from the substrate. The single experiment on FDP I1 revealed its activity in knuckle-walking to be very similar to that depicted here for FDP V.
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RANDALL L. SUSMAN AND JACK T. STERN. JR.
shoulder is directly above the point of contact of the hand with the ground). Commonly a burst of slight activity occurs in these fasciculi as the hand is lifted from the ground at the onset of swing phase (fig. 1).In subjects A and C such a burst was observed during virtually every episode of knuckle-walking in which the hand was held on the ground with its palm parallel to the line of progression. Its occurrence in Subject B was less frequent. When subjects A and C walked with the hand perpendicular to the direction of movement (a behavior not observed in Subject B) the burst usually failed to appear. This fact, and a careful examination of the timing of events, point clearly to a function of FDP IV in lifting the finger from the ground as opposed to propulsion. In subjects A and C, there occurred quite consistently a short burst of activity in FDP IV at mid-stance during the most rapid bouts
Suspension by forelimb
of knuckle-walking. The burst was of modera t e amplitude i n Subject C, whose wrist appeared to dorsiflex at such times (Jenkins and Fleagle, '75, noted 10-15" of dorsiflexion in their chimpanzees during stance phase of knuckle-walking). In Subject A, the mid-
-
FAST KNUCKLE-WALKING Swing
Suplort
Swin;
I
Support
Swing
Fig. 2 Flexor digitorum profundus IV in female chimpanzee (Subject A) during rapid knuckle-walking. Note the occurrence of slight activity in the muscle in late stance, followed by a larger burst prior to and during early swing phase.
Release of grasp followed by voluntary movement
I
FCR
FDS IV
FDP IV
FOP V .
I
-
Fig. 3 Activity of the same muscles as in figure 1 while Subject B was suspended by one forelimb. Activity observed represents maximum potential exhibited in this experiment.
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EMG OF CHIMPANZEE FINGER FLEXORS
stance burst during rapid progression was never of more than slight amplitude and was always smaller than the activity correlated with onset of swing (fig. 2). A few spikes appeared occasionally a t mid-stance in Subject B when moving quickly. In two instances in which Subject C dropped from a bipedal to tripedal stance, FDP IV exhibited moderate activity upon contact of the hand with the ground. The experiment in which data were obtained for FDP I11 showed that its behavior during knuckle-walking is identical to that of FDP IV with one exception. When the hand is held on the ground with its palm parallel to the line of progression, the burst which occurs in FDP I11 as the hand is lifted from the ground follows slightly that of FDP IV. This
-
difference can be correlated with the earlier removal of digit IV from the substrate. The fasciculus of FDP to digit V differs from those to digits I11 and IV by very often showing slight to moderate potentials during the support phase (chiefly its first half) of knuckle-walking (fig. 1). Such activity also occurs occasionally in FDP 11. Since digits I1 and V are not weight bearing during knuckle-walking in the chimpanzee, it suggests that this action functions to clear them from the ground. As with FDP I11 and IV, the fasciculi to digits I1 and V commonly exhibit activity a t the onset of swing phase when the hand is parallel to direction of movement (fig. 1.) At no time during quiescent quadrupedal and tripedal standing was significant activity of any fasciculus of FDP noted.
GRASP OF ORANGE
Pressing orangs against incisors
FDP IV
D
Fig. 4 Subject C holding an orange. Note absence of activity of FDS 111, FDP 111 and FDP IV except when fruit is forced against the incisor teeth. Activity of FDS IV persists while the orange is held after the bite has occurred.
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RANDALL L. SUSMAN A N D JACK T. STERN. JR.
Scratching thigh .
.
Scratching thigh
I
.
t
.
FDS IV
s
FDP IV
FDP V
Fig. 5 Same muscles as represented in figure 1. The level of activity of the extrinsic digital flexors in scratching is greater than in any incidence of knuckle-walking.
Suspensory behavior The four fasciculi of FDP display maximum potentials during climbing the vertical trunk and ropes and in suspension from the horizontal rope and ladder (fig. 3). During certain behaviors in which the hand loosely grasps the side of the wire cage independent activity of individual fasciculi occurs. Manipulation The fasciculi are variably active, usually at no more than a moderate level, during manipulation of small and large fruits. Often absence of potentials in a particular fasciculus could be correlated with the fact that its corresponding digit was not employed in the grasp. Of the fasciculi tested, FDP I1 was the most active in manipulation. It showed frequent moderate potentials while the subject
held and ate an orange, and slight potentials when a cylindrical object (6.4 cm diameter) was lightly grasped. However, periods of electrical silence in FDP I1 also occurred in these circumstances. When holding an orange in the hand such that digits I1 and I11 were employed in opposition to the thumb and digit IV was slightly flexed so that it was partially underneath the orange, FDP 111 and IV were silent. Both became moderately active only when the orange was forced against the incisors (fig. 4). In some instances of manipulation, and during scratching (fig. 5) the level of activity of FDP was greater than in any episode of knuckle-walking. Flexor digitorum superficialis ZZZand ZV Knuckle-walking The activity of the faciculi of FDS to digits
EMG OF CHIMPANZEE FINGER FLEXORS
571
tive of the absence of any noteworthy role for FDS in stance phase of all but the most rapid episodes of knuckle-walking. Suspensory behavior During very fast knuckle-walking in two of FDS displayed its maximum potentials dur- our subjects, slight to moderate potentials ing climbing t h e vertical trunk and ropes, and were exhibited by the extrinsic flexors of the in suspension from the horizontal rope and weight bearing digits in stance phase. Tuttle ladder (fig. 3). In such cases the activities FDS et al. ('72) interpret one instance of FDS activand FDP are essentially synchronous. During ity during stance phase as being related to certain behaviors in which the hand grasped propellent flexion of the metacarpophalangeal the side of the wire cage, brief periods of inde- joints. This may be the case for gorillas in pendent activity of FDS or FDP occurred, but which the hand is habitually placed perpenwe are unable to correlate these with the digi- dicular to the direction of movement (Tuttle, '67, '69) but we doubt this interpretation aptal position. plies to the chimpanzee because flexion of the Manipulation digits ought not to generate propellant force In manipulation, FDS usually operates si- when the hand is held parallel to the line of multaneously with FDP, but occasionally the progression. It is not possible to say if the actwo muscles may operate independently (fig. tivity we observed serves the function of 4). We could not relate episodes of indepen- maintaining stability of the metacarpophadent activity to either object dimension or langeal joints, or the wrist joints, or both. The consistency. However, in the example of eat- greater amplitude of the potentials in Subject ing an orange described above, FDS IV re- C whose wrist seemed to yield into dorsiflexion mained active even when the fruit was held at high speed, is suggestive of a role for the long finger flexors in support of the wrist. without being forced against the teeth. Activity of both extrinsic digital flexors at The activity of FDS in scratching is much greater than in any episode of knuckle-walk- t h e end of stance phase occurs commonly but is quite obviously related simply to lifting of ing (fig. 5). the fingers and hand from the ground. DISCUSSION Absence of any major active role of FDP and The prominent activity of the extrinsic FDS in the weight bearing phase of knucklefinger flexors in suspensory behavior involv- walking does not preclude important coning the forelimb is not surprising. It supports tribution of these muscles in passive or theoretical expectations, but does not entirely rheological support of the wrist and metacarconfirm the variable results of Tuttle and Bas- pophalangeal joints. Long et al. ('64) note that majian ('75). The absence of a n active role for rheologic (or viscoelastic) forces are importhese muscles during the stance phase of slow t a n t for hand control in humans for either and moderately fast knuckle-walking is unex- assisting or countering certain motions. They pected given their positions and potential for cite the FDS of humans as evidence for this maintaining equilibrium a t the metacarpo- point. With full dorsiflexion of the wrist, the phalangeal joints (Preuschoft, '73). Tuttle e t extrinsic flexors are at maximum stretch and al. ('72) and Tuttle and Basmajian ('74, '75) the long superficial flexors exhibit little activstressed the minor role of FDP in knuckle- ity. With increasing palmar flexion, the long walking in the gorilla, but report a more com- flexors are increasingly activated. Long et al. mon occurrence of low levels of activity during ('64) postulate that while the wrist is in dorstance phase than we observed among chim- siflexion t h e flexor digitorum superficialis panzees. In our studies, stance phase activity contributes force through its viscoelastic of FDP was mostly confined to the fasciculi to properties alone. As the wrist is flexed the extensors increase their tension so that the flexdigits I1 and V, which did not bear weight. Tuttle and Basmajian ('74) reported one ex- ors not only must actively compensate for periment in which FDS to a weight bearing reduced viscoelastic force, but also must digit was rather active in the stance phase of counter the effect of the opposing extensors. Straus ('40) emphasized the shortening of knuckle-walking and a second experiment in which no significant potentials were seen. the flexor digitorum profundus and superfiThey judge the first result more likely to be Rheological forces include elasticity, viscosity, friction and valid, but our observations are clearly suppor- plasticity. I11 and IV during knuckle-walking is the same as those of FDP (fig. 1).
I
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RANDALL L. SUSMAN A N D JACK T. STERN, JR.
cialis in the great apes and related this phenomenon to hook-grasp during suspension.2 However, orangutans (and hylobatid apes) do not possess “shortened flexors” (Tuttle, ’69). The shortened flexors in the African apes suggest the possibility of a rheologic role for the extrinsic finger flexors in knuckle-walking hand postures in which the wrist is in line with the forearm or slightly dorsiflexed, and in which the proximal phalanges are hyperextended. Tuttle and Basmajian (’74) suggest that “tendonization” of the long digital flexors may account for the “shortness” of these muscles in African apes. Tendinization need not be associated with a “shortness” of a muscle if one means by the latter term that joints are still quite flexed when the stretch of the muscle first begins to elicit passive resistance. On the other hand, if the actual contractile portions of the long digital flexors are short, then the passive length-tension curve will rise steeply upon extension of the joints. The same effect will occur if the muscles are highly pinnate. Dissections of two chimpanzees and two orangutans did reveal that pinnation of the FDS I11 and IV is greater in the chimpanzee (Susman, personal observation). The conclusion to be reached from these considerations is that absence of anactive role for the long flexors in the support phase of slow and moderately fast knuckle-walking and the low level of such activity in rapid movement does not preclude the possibility that these muscles provide substantial passive forces to support the hand against ground reaction forces encountered in knuckle-walking (Tuttle, ’67; Tuttle et al., ’72; Susman, ’79). Olduvai Hominid 7 hand The Olduvai Hominid 7 hand, first described by Napier (‘621, exhibits exceptionally large areas for insertion for FDS on the middle phalanges. The impressions for this muscle are greater in relative area than in any living ape or modern humans (fig. 6). In addition other pongid affinities are noted in t h e following features: (a) the curvature of the proximal and middle phalanges, (b) the stout, robust proportions of the middle phalanges, and (c) the thickened cortices of middle and proximal phalanges. Although the middle phalanges are unique, they compare most closely with those of gorillas among the extant Hominoidea (Napier, ’62; Susman and Creel, ’79).
The proximal phalangeal fragments are most like those of chimpanzees among extant Hominoidea. The distal phalanges, however, (FLK NN-B, C) are most similar to those of modern humans on the basis of a variety of multivariate statistical comparisons (Susman and Creel, ’79). We infer the functional capacities of O.H. 7 to include suspensory behaviors on the basis of both osteological and experimental evidence. EMG data suggest the recruitment of FDS in powerful grasping and to a lesser extent manipulation. The sign t h a t this was a well developed muscle in the fossil argues for some degree of climbing or other arboreal activity in hominids a t this time. We cannot attribute a large flexor digitorum superficialis muscle primarily to selection for manipulation for two reasons: (1) judged by its markings the muscle is apparently larger in O.H. 7 than in modern humans but we can reasonably assume that manipulation has increased in importance in the last 1.76 million years in the hominid line, and (2) the most suspensory hominoids, the Hylobatidae, have the largest flexor digitorum superficialis muscles (Tuttle, ’72) and they are far less dextrous than humans and no more so than the African apes. Evidence exists that Plio-Pleistocene hominids retained long forelimbs (Taieb et al., ’75; McHenry, ’781, but we do not feel that the suspensory features of the O.H. 7 hand indicate simply a primitive retention of pongidlike features (McHenry, ’78). Secondary osteological features such as large muscle insertions on the middle phalanges may be gained or lost ontogentically or as a result of mechanical or systemic aberrations within an animal’s lifetime. No doubt they would be quickly lost in animals which did not utilize them. If we are correct, then early hominids may have retained a capacity for climbing even past the point a t which t h e foot became adapted for bipedalism. ACKNOWLEDGMENTS
We thank t h e following people for their help in various supportive and technical roles: Ms However, like many others, Straus mcorrectly lumped orangutans with the chimpanzee and gorilla with respect to knucklewalking. The identification of these bones has been revised by Duy (‘76). The O.H. 7 hand now includes a capitate fragment, trapezium, scaphoid. fragmentary second metacarpal, 3 distal phalanges, 2 fragmentary proximal phalanges, and 4 middle phalanges. All this material, with the exception of the capitate, may represent the right hand of a single individual.
EMG OF CHIMPANZEE FINGER FLEXORS
573
Fig. 6 Middle phalanges of O.H. 7. FLK NN-G, E, F, D rays V, IV, 111, 11, respectively (left to right). Note missing epiphyses and the large impressions for the insertion of the flexor digitorum superficialis muscle on the palmar surfaces (below).
Marcy Koltun, Mr. William Korosh, Ms Lorraine Rice, Ms. Sukie Davis, and Mr. Phillip Vollono. We also thank Sue Savage-Rumbaugh and the staff of the Yerkes Regional Primate Center for their cooperation and support of this project. The illustrations were prepared by Ms Lucille Betti and Ms Joan Kelly typed the manuscript. This work was supported by NSF Grant BNS 76-83114 and by a General Research Support Grant from N.I.H. administered by the School of Basic Health Sciences, S.U.N.Y., Stony Brook. Study of 01duvai Hominid 7 was made possible by a grant to R. L. Susman from the L. S. B. Leakey Foundation and from the Henry Hinds Fund, Com-
mittee on Evolutionary Biology, University of Chicago. We are grateful to all of these individuals and organizations for their support. LITERATURE CITED Day, M. H. 1976 Hominid postcranial material from Bed I. Olduvai Gorge. In: Human Origins. G. Issac and E. McCowan, eds. W.A. Benjamin, Menlo Park, California, pp. 363-374. Jenkins, F. A,, Jr., and J. G. Fleagle 1975 Knuckle-walking and t h e functional anatomy of the wrists in living apes. In: Primate Functional Morphology and Evolution. R. H. Tuttle, ed. Mouton Publ., Hague, pp. 213-227. Keith, A. 1894 The Myology of the Catarrhini: A Study in Evolution. Doctoral Thesis, university of Aberdeen. Lewis, 0. J. 1969 The hominoid wrist joint. Am. J. of Phys. Anthrop., 30: 251-268.
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1972 Evolution of the hominoid wrist. In: Functional and Evolutionary Biologyof Primates. R. H. Tuttle, ed. Aldine-Atherton, Chicago, pp. 207-222. Long, C., D. Thomas and W. J. Crochetiere 1964 Viscoelastic factors in hand control. Proc. IVth Intl. Cong. Phys. Med., Paris, pp. 440-445. McHenry, H. M. 1978 Fore- and hindlimb proportions in plio-Pleistocene hominids. Am. J. of Phys. Anthrop., 49: 15-22. Napier, J. R. 1962 Fossil hand bones from Olduvai Gorge. Nature, 196: 409-411. Preuschoft, H. 1973 Functional anatomy of the upper extremity. In: The Chimpanzee. Vol. 6. G. H. Bourne, ed. Karger, Basel, pp. 34-120. Stern, J. T., Jr., J. P. Wells, A. Vangor and J. G. Fleagle 1977 Electromyography of some muscles of the upper limb in Ateles and Lagothrix. Yrbk. Phys. Anthro., 20: 498-507. Straus, W. L. 1940 The posture of the great ape hand in locomotion, and its phylogenetic implication. Am. J. Phys. Anthrop., 27: 199-207. Susman, R. L. 1979 Comparative and functional morphology of hominoid fingers. Am. J. Phys. Anthrop., 50: 215-236. Susman, R. L., and N. Creel (1979, ,submitted) Functional and morphological affinities of t h e subadult hand (0.H. 7) from Olduval Gorge. Am. J. Phys. Anthrop. Taieb. M., D. C. Johanson and Y. Coppens 1975 Exp6dition
internationale de l'afar Ethiopie (3e campagne 1974): decourverte d'hominides plio-pleistocenes a Hadar. C . R. Acad. Sci., Paris, 281: 1297-1300. Tuttle, R. H. 1967 Knuckle-walking and the evolution of hominoid hands. Am. J. Phys. Anthrop., 26: 171-206. 1969 Quantitative and functional studies on the hands of the Anthropoidea. I. The Hominoidea. J. Morph., 128: 309-364. 1972 Relative mass of cheiridial muscles in catarrhine primates. In: Functional and Evolutionary Biology of the Primates. R. H. Tuttle, ed. Aldine, Chicago, pp. 262-291. 1974 Darwin's apes, dental apes and the descent of man: normal science in evolutionary anthropology. Curr. Anthrop., 15: 389-398. Tuttle, R. H., and J. V. Basmajian 1974 Electromyography of forearm musculature in gorilla and problems related t o knuckle-walking, In: Primate Locomotion. F. A. Jenkins, ed. Academic Press, New York, pp. 293-347. 1975 Electromyography of Pan gorilla: a n experimental approach to the problem of hominization. Symp. 5th Cong. Intl. Primat. SOC.,pp. 303-314. Tuttle, R. H., J. V. Basmajian, E. Regenos and G. Shine 1972 Electromyography of knuckle-walking: results of four experiments on the forearm of Pun gorilla, Am. J. Phys. Anthrop., 37: 255-266. Washburn, S. L. 1968 The study of human evolution. Condon lecture, University of Oregon.
