An electromyographic study of the pectoralis major in Atelines and Hylobates with special reference to the Evolution of a pars clavicularis.код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 52:13-25 (1980) An Electromyographic Study of the Pectoralis Major in Atelines and Hylobates, With Special Reference to the Evolution of a Pars Clavicularis JACK T. STERN, JR., JAMES P. WELLS, WILLIAM L. JUNGERS, ANDREA K. VANGOR, AND JOHN G. FLEAGLE Department of Anatomical Sciences, Health Sciences Center, State University of New York a t Stony Brook, Long Island, N e w York 1 1 794 KEY WORDS Electromyography, Pectoralis major, Atelines, Hylobates, Evolution ABSTRACT Among primates there is striking variation in the extent of the origin of pectoralis major from the clavicle. A significant clavicular attachment (pars clavicularis) occurs only inillouattu, Lugothrix, Hylobates, Pan (troglodytes, paniscus andgorilla), and Homo. Interpreting this trait in nonhuman primates as an adaptation to frequent use of a mobile forelimb in climbing and suspension is contraindicated by the absence of a clavicular origin in Ateles andPongo. We have undertaken a telemetered electromyographic study to determine any special role of the most cranial part of the pectoralis major in comparison to its caudal part, and to the deltoid, during vertical climbing, pronograde quadrupedalism, and armswinging in Ateles, Lagothrix, Alouatta, andHylobates. The results show that the cranial pectoralis major possesses a role not shared by the caudal fibers: initiation of the recovery phase of the locomotor cycle. When ability to execute rapid or powerful recovery of the adducted forelimb is required in an animal with a shoulder joint lying on a plane cranial to that of the manubrium, the movement will be facilitated if the origin of the pectoralis major is extended onto the clavicle. Such is the case in nonhuman primates possessing this trait. The absence of a clavicular origin in Ateles and Pongo may be related to diminished selective pressures to perfect locomotor modes such as pronograde quadrupedalism, armswinging, or climbing thick vertical trunks, that demand rapid or powerful recovery of the adducted forelimb. If the arboreal ancestor of humans had evolved a clavicular origin of pectoralis major, this animal would be preadapted for certain uses ofthe forelimb in its bipedal descendant. The anthropoid apes and prehensile-tailed New World monkeys are remarkable among primates for the high degree to which they practice behaviors such as climbing, hanging, and swinging that impose mechanical demands for a mobile forelimb able to resist tensile forces (reviewed in Stern and Oxnard, '73). The same animals share a number of anatomical traits that seem to be adaptations for these special locomotor abilities ( Washburn, '63; Erikson, '63; Oxnard, '67; Stern, '71). In 1963 Ashton and Oxnard published their now classic monograph in which the shoulder musculature of primates was examined in order to identify such adaptations. Among the muscles that were characterized by functionally interpretable morphological variation was the pectoralis major. Ashton and Oxnard emphasized differences in fiber direction, caudal extent of origin, and relative thickness of the cranial versus the caudal portions of pectoralis major. These were interpreted as reflecting a dichotomy between use of the forelimb in a low, relatively retracted posi0002-9483/80/5201-0013 $02.60 0 1980 ALAN R. LISS, INC. tion as is most common in generalized running, jumping, pronograde primates, and use of the forelimb in a raised abducted position, as in the climbing-hanging apes and prehensile-tailed cebids. One striking variation that Ashton and Oxnard did not interpret was the extent of the origin of pectoralis major from the clavicle. A noteworthy clavicular origin (pars clavicularis, Fig. 1) occurs solely in anthropoid primatesl, and within this group only among a few genera. Table 1 lists primates according to whether or not they possess a significant clavicular origin of pectoralis major. Interpretation of the distribution is difficult because the anatomical groups seem not to have any clear relation to James P Wells is presently at West Virginia School of Osteopathic Medicine, Lewisburg, West Virginia 24901 'Jouffroy ('62) reports an attachment o f t h e pectoralis major to the proximal third of the clavicle In Malagasy prosimians, but Ashton and Oxnard ('63i, and our observations on Lemur cutta, L. fuluus. and Propithecus irerreuuxi .ndicate no fibers arising more laterally than the extreme medial end of this bone. 13 JACK T. STERN, JR., ET AL. 14 WOOLLY MONKEY SPIDER MONKEY Fig. 1. The pectoralis major in the spider monkey iAtelesi and woolly monkey tlagothrinl. Note the absence of any attachment to the clavicle in the spider monkey and the presence of an origin from the medial half of the clavicle in the woolly monkey. The only other primates with a significant clavicular origin of pectoralis major are Alouatta, Hylobates, Pan troglodytes, P . paniscus, P . gorilla. and Homo. TABLE 1. Distribution of Clavicular Origin of Pectoralis Major Among Primates Significant clavicular origin present Howling monkey Woolly monkey Gibbon Siamang Chimpanzee Gorilla Human No significant clavicular origin Prosimians Old World monkeys Non-prehensile-tailed New World monkeys Spider Monkey Orangutan locomotor behavior. In particular, the absence of a clavicular origin in spider monkeys and orangutans deters one from explaining its presence as a n adaptation to frequent use of the forelimb in arboreal climbing and suspension. The failure of the classical comparative method to discover the significance of a clavicular origin of pectoralis major has prompted us to apply experimental techniques toward a solution of this problem. We have undertaken a n electromyographic study to discover any special role of the cranial part of the muscle in relation to its caudal part. To date, the only electromyographic investigation of the pectoralis major in nonhuman primates has been that of Tuttle and Basmajian ('77, '78) on the three great apes. These authors confined their examination to the sternocostal (caudal) por- tion of the muscle, observing that it is active in hoisting, is also a regular supporter of the upper body weight, and is probably also a propulsive element during quadrupedal walking. In this paper we present results of a study of both the cranial and caudal pectoralis major, along with the acromiodeltoid, in the spider monkey (Ateles), woolly monkey (Lagothrix), howling monkey (Alouatta), and gibbon (Hylohates). MATERIALS AND METHODS Subjects The subjects for t h e electromyographic experiments were three spider monkeys ( 1 d A . fusciceps, 2 ? A . belzebuth), two woolly monkeys (1d a n d 19 L. lagothricha), one howling monkey ( ? A . seniculus), and two gibbons ( l d a n d 19 H.lar.). All subjects were adult (the howling monkey rather aged) showing no obvious pathology. The New World monkeys had been housed in a large enclosure (7.3m x 3.7m x 2.7m) for at least six months prior to study. The gibbons lived in this came cage for approximately one month before study. Within the enclosure were a long horizontal tree trunk (7.3m x 9.5cm), placed approximately 60cm above the ground, a long vertical tree trunk (3.7m x 8.5cm), and a 7.3m long ladder with wooden dowel (2.8cm diameter) cross pieces spaced 40cm apart suspended from the roof of EMG OF PECTORALIS MAJOR the cage. The subjects had become well accustomed to locomotion on these supports by the time of the experiment. They were induced by means of food reward to locomote on specific substrates. Spider monkeys and gibbons readily engaged in armswinging beneath the ladder. Of the woolly monkeys, only the male would perform “pendular” armswinging; this behavior was infrequent and the wire mesh of the cage roof was the substrate. Climbing the vertical trunk was performed by the spider monkeys, woolly monkeys, and gibbons. In addition, these animals would spontaneously ascend the wire mesh sides of the cage, as would t h e howling monkey. Pronograde quadrupedalism along the horizontal branch was practiced by all three monkeys, but not by the gibbons. METHODS We employed the technique of telemetered electromyography described by Stern et al. (’77). This technique permits the subjects to locomote freely and naturally without the hindrance of wires running from the animal to a recording device. Two important modifications were incorporated into this study. One concerns the method by which proper placement of electrodes was verified, the other pertains to analysis of data. Electrode Placement In the experiments on spider and woolly monkeys, we relied on the ease with which the muscles could be palpated to satisfy the demand for accurate placement of fine wire electrodes. Although the pectoralis major and acromiodeltoid are also easily palpated in howling monkeys and gibbons, we introduced an additional means of verification by passing a small stimulating current through the fine wires following their insertion into the muscle belly (i.e.,back-stimulation). Clear contraction of the relevant muscle portion was elicited and served to confirm position of the electrode. The data presented below were derived from electrodes placed in the following three locations: a) as close as possible to the cranial edge of the pectoralis major half way between its origin and insertion; b) into the caudal edge of the pectoralis major in the anterior axillary fold; c) into the deltoid muscle half way along a line between t h e acromion process of t h e scapula and deltoid tuberosity of the humerus. Records were also obtained from the portion of the deltoid arising from the lateral end of the clavicle but are omitted here because they do 15 not add to the resolution of the questions posed in this paper. Data Analysis Because we were able to study more than one representative of three of the four genera, and often obtained data for a sizeable number of “step”cycles of each of the locomotor modes, we obtained considerable information about variability ofmuscle recruitment. In order to assess this variability in a more objective manner, the data analysis was modified from that described in Stern et al. (’77).This first involved a technical change in the videotape recording process such that a t the end of every sweep of the oscilloscope beam the superimposed picture of the subject was deleted and an unobscured image of the previous two seconds of EMG was displayed on the video monitor. A paper copy of this image was reproduced by a Tektronix 4632 video hard copy device. On the paper copy were marked exactly the times when limbs contacted the substrate and when they were in midsupport and midswing. These data were then analyzed by tracing the actual shape of the electromyographic interference pattern with the stylus of NT-501 Sonic Digitizer (Science Accessories Corporation, Southport, Connecticut) and entering this information, along with that for locomotor events, into a Hewlett-Packard 9830 computer. The computer constructed a 20 x 20 matrix with the columns representing equal intervals within a phase of support (when the tested limb is in contact with the substrate), or swing (when the tested limb is free of the substrate and moving forward to grasp a new hold), and the rows representing equal intervals of level of activity (the maximum being the largest burst of EMG observed during the entire experiment). If n samples of activity during a given phase of a given behavior are available and traced with the digitizer stylus, the computer fills in a square of the 20 x 20 matrix in every instance when activity occurs in that square. After all n samples have been digitized, the computer calculates the per cent incidence of activity of a given level at a given point in the phase. The result is an output indicating the variability in electromyographic activity. The data for different subjects of the same genus are used to derive a composite picture of variability for that genus. Text figures are reproduced from these composites. Blackened regions indicate highly consistent presence of EMG activity, occurring ?hor more of the time on the average. Enclosed white regions indicate frequent but not consistent activity, occurring a t least half of the time in one subject. JACK T. STERN, JR., ET AL. 16 This method of quantification allows accurate assessment of variability in onset and cessation of EMG activity but is somewhat novel in its approach to judging amplitude. What is digitized by our methods is the visual appearance of the EMG burst. The taller this burst appears, the greater will be judged the amplitude of EMG. Such a relationship is to be expected, since larger and more frequent spikes will summate to taller bursts. Nonetheless, in one instance we performed an experiment in which the EMG signal was passed through a full-wave rectifier and averager. Figure 2 presents five EMG bursts of increasing amplitude along with their rectified averaged signals and the shape of these bursts as we would trace them for digitization. It can be seen that the method of tracing yields a picture of relative amplitudes that in general parallels that presented by the averaged signal. We believe our method is as accur.ate as grading activity into categories of relative amplitude (e.g.,nil, negligible, slight, moderate, marked) and is less subjective. RESULTS Climbing a Vertical Trunk This mode of locomotion generally elicits the highest levels of phasic activity, and the recruitment patterns during climbing illustrate very clearly the separate roles of the cranial and caudal parts of the pectoralis major (Fig. 3). In Ateles, Lagothrix, and Hylobates the caudal portion of the pectoralis major is propulsive in its action throughout most of the support phase, or pull-up. It is worth noting (although not illustrated here) that the level of activity in caudal pectoralis major is substantially less during the support phase of climbing when this activity is performed on the wire-mesh side of the cage rather than on the vertical trunk. Such a difference may be related to the fact that there is reduced adduction at the shoulder during the pull-up of cage climbing because the animal is not constrained to grasp the substrate directly ventral to its thorax. The cranial portion of the pectoralis major shares with the caudal portion the ability t o adduct and retract the forelimb from the raised position, but, as can be noted for all genera in Fig. 3, the activity in the cranial portion ceases earlier in the support phase due to the fact that its retractive abilities disappear at a relatively more elevated position of the forelimb. Figure 3 also illustrates the fact that the propulsive activity of the cranial pectoralis major persists somewhat longer in Ateles, presumably due to the fact that in this animal the sampled fibers arise from the manubrium and not the clavicle, and therefore have an orientation that permits them to exert a retracting moment with the arm in a lower position. In all three genera, the unique role of the cranial pectoralis major is to initiate the recoueryphase of the limb as it reaches to grab a new hold higher on the vertical trunk. In the woolly monkey the fibers arising from the clavicle are predominantly active during the recovery, or swing, phase and are almost solely responsible for this movement. By contrast, in the spider monkey, the deltoid plays a major role in recovery later in the movement. This distinction is probably related to the different manners in which these animals climb (Fig. 4). The spider monkey tends to hold its arm abducted at the shoulder during the recovery phase of the cycle, whereas the woolly monkey climbs with the forelimb in a relatively adducted position. The basis for this difference might lie in the more lateral orientation of the glenoid in the spider monkey, its greater interglenoid distance relative to diameter of the support, and its longer arms. As a consequence, the spider monkey relies more on the deltoid, an abductor, to effect recovery than does the woolly monkey. The distinction is even clearer when these animals climb the wire mesh side of the cage, a behavior demanding less constant adduction. In this circumstance the activity of the cranial pectoralis during recovery is reduced in both Ateles and Lagothrix, but far more so in the former. In the gibbon, as in the spider monkey, recovery phase during climbing involves abduction at the shoulder, and this is reflected by the consistent activity of the deltoid during this phase. However, the cranial pectoralis of the gibbon plays a greater role in recovery than does that of the spider monkey. The explanation for this may be: 1)that the fibers arise from the clavicle and therefore have an orientation permitting them to continue protraction up t o a more elevated position of the arm; and 2) that the relatively long and heavy forelimb of the gibbon requires the force of both pectoralis major and deltoid to effect recovery. Pronograde Quadrupedalisrn Along a Branch That the cranial portion of the pectoralis major has as its unique role flexion of the adducted upper limb is supported by the records of muscle activity during pronograde quad- TRACED EMG EMG RECTIFIED AVERAGEDEMG Fig. 2. A comparison of two methods of “quantifying” the amplitude of EMG activity. The top curves represent electronically rectified and averaged transformations of EMG burstsjust below. The bottom curves represent the results of tracing the outlines of the bursts as we have done in this paper. I t can be seen that our method of tracing yields a picture of relative amplitudes that in general parallels that presented by the electronically averaged signal. c -3 Deltoid Cranial Pectoralis Major Major PeLtoralis Caudal I I SWING (3-52) SWING UPPORT (2-25) I(2-27) SUPPORT I R SUPPORT h I W 00 LLY MONKEY I I SWING (2-251 (2-33) SWING (2 - 26) SWING !- , GIBBON A ,UPPORT (2-6) SUPPORT (2-7) Fig. 3. Phasic activity of caudal pectoralis major, cranial pectoralis major, and middle (acromio-) deltoid in Ateles, Lagothrzx, and Hylobates during climbing a vertical tree trunk. Blackened areas indicate highly consistent presence of EMG activity; enclosed white areas indicate frequent but less consistent activity. The heights of these areas reflect amplitude of activity; the maximum amplitude observed during the experiment is represented by the height of the vertical line at the beginning of SUPPORT. Two numbers appear under the words "SUPPORT' and "SWING". The first is the number of animals from which data were derived for this phase, the second is the number of phases (support or swing, respectively) digitized to yield the composite picture of activity. Note that although the cranial pectoralis major assists the caudal portion of the muscle in pulling the animal up during climbing, the unique role of the cranial fibers are in the swing (recovery) phase of locomotion. r _ _ l SPIDER MONKEY I I L A (3-50) SUPPORT CLIMBING VERTICAL TRUNK SWIN( SWING (2-10) I c a, EMG OF PECTORALIS MAJOR rupedalism in Ateles, Lagothrix, and Alouatta (Fig. 5). As in climbing the vertical trunk, the function of the caudal portion of pectoralis major is propulsive. Furthermore, in our two woolly monkeys, which move rather quickly, the caudal pectoralis major begins its contraction substantially before touch-down in order to decelerate t h e swinging limb. I n quadrupedalism along a branch, the special role of the cranial pectoralis is in the recovery phase of the cycle. Figure 5 shows how this role is accentuated in woolly monkeys in which the forelimb is more adducted during swing than in the spider moneky (Fig. 6). The deltoid, an abductor, is more consistently active during the recovery of the limb in Ateles than in Lagothrix. The burst of deltoid activity in the second half of the swing phase in Alouatta is not accompanied by abduction of the arm at this point in locomotion. Rather, the acromiodeltoid of howling monkeys acts in swing phase probably as a simple protractor of the limb. This is due to the orientation of the scapula more along the side of a dorso-ventrally deep chest in howling monkeys. It shares this orientation, but in a less extreme manner, with more typically quad- W O O L L Y MONKEY 19 rupedal primates such as Old World monkeys and non-prehensile tailed cebids. Armswinging Although neither portion of the pectoralis major is active during quiet suspension by the forelimbs, armswinging is characterized by consistent recruitment of this muscle. Figure 7 presents the records of muscle activity during non-richochetal armswinging for Ateles, Lagothrix, and Hylobates2. The data support the conclusion drawn from the other locomotor modes. The caudal pectoralis is active a t a low level during the support phase ofmovement (our two gibbons differed dramatically in amplitude of activity). Interestingly, in gibbons there also occurs a small burst at the onset of recovery when the hand is just released from the substrate. This burst probably provides a brief impulse of acceleration to enable a rapid recovery phase. AOurgibbons also engaged in richochetal armswinging. The diNerences In muscle recruitment between this behavior and dower armswinging will be the subject of a separate paper. SPIDER MONKEY Fig. 4. Drawings of the limb positions inLag0thri.x and Ateles during climbing a narrow vertical trunk. Note that in the swing (recovery)phase of locomotion, the forelimb is held adducted in the woolly monkey but abducted in the spider monkey. Middle Deltoid Cranial Pec tora I i s Major Caudal Pectoralis Major I SWING ( 3- 67) SWING (2-83) /- I UPPORT (2-38) UPPORT (2-55) (2-40) I I 1 (1-65) SUPPORT (1-27) I I HOWLING MONKEY (1-64) I I (1-39) SWING 2 1 / 4 1 WOOLLY MONKEY Fig. 5. Phasic activity of caudal pectoralis major, cranial pectoralis major, and middle (acromio-) deltoid in Ateles, Lugothrix, and Alouattn during pronograde quadrupedalism along a horizontal tree trunk (see legend to Fig. 3 for explanation of symbols). This figure has been constructed so t h a t midsupport corresponds to placement of the shoulder directly above the wrist and midswing to placement of the wrist directly beneath the shoulder. Note that the special role of the cranial pectoralis major is in the swing (recovery)phase of the locomotor cycle, as was also the case for vertical climbing. (2-79) SUPPORT 1 SUPPORT (2-48) PRONOGRADE QUADRUPEDALISM ALONG HORIZONTAL TRUNK E3 r R .e C EMG OF PECTORALIS MAJOR WOOLLY MONKEY 21 SPIDER M O N K E Y Fig. 6. Drawings of the limb position in Lugothrix and Ateles during pronograde quadrupedalism along a horizontal tree trunk. Note that in the swing (recovery) phase of the locomotor cycle, the forelimb is held adducted in the woolly monkey but partially abducted in the spider monkey. During armswinging the cranial pectoralis major appears to serve different roles in the three different genera. In the spider monkey, this muscle segment frequently (but not consistently) contracts in the vicinity of midswing to promote elevation of the limb. However, the major work of forelimb elevation occurs later in the recovery and is effected by the deltoid. The data for Lagothrix are sparse, but suggest a rather complicated recovery stroke involving a reciprocal interaction between deltoid and cranial pectoralis major. Hylobates, the primate arm-swinger par excellence, differs from the New World genera in possessing consistent support phase activity of cranial pectoralis major. The burst at the onset of this phase occurs in both gibbons and spider monkeys, but more consistently in the former. This may be attributed to shock-absorption at touch-down, although it is possible to interpret this as evidence for a regulated abduction of the shoulder under the influence of gravity. More interesting is the regular burst of cranial pectoralis activity i n the gibbon just after midsupport. An accentuation of caudal pectoralis activity is also seen a t this time and both are related to a pull-up (Fig. 8) which occurs in the gibbon at this point during amswinging. Such a pull-up serves to elevate the center of gravity to enable the animal to rise higher a t the end of the support phase for the purpose of permitting a greater drop, and thus greater acceleration due to gravity, during the next following cycle (Fleagle, '77). The greatest amplitude of cranial pectoralis major activity during armswinging in the gibbon occurs a t midswing. Tnis burst is essential to effect a rapid recovery of the long forelimb, which is adducted a t the shoulder and flexed a t the elbow to diminish moment of inertia. It can be seen from Figure 8 that the recovery phase of the spider monkey does not involve the attempt to reduce moment of inertia that characterizes gibbons. This, along with the absence of the initial impulse provided by the caudal pectoralis major, implies a more loosely programmed recovery phase in the spider monkey. The two genera do resemble one another in the role of deltoid to produce the terminal movement of recovery. DISCUSSION Electromyographic records of the pectoralis major in Ateles, Lagothrix, Alouatta, and Hylo- Major PPctoralii Caudal I I SUPPORT (1-5) I WOOLLY MONKEY (1-12) SWlNC (1-9) SWING (2-11) SUPPORT SUPPORT (2-32) (2-17) SUPPORT I GIBBON Fig. 7 . Phasic activity of caudal pectoralis major, cranial pectoralis major, and middle (acromio-) deltoid in Aleles, Lugothrzx, and Hylobutes (see legend to Fig. 3 for explanation of symbols). This figure has been constructed so that midsupport corresponds to placement of the shoulder directly beneath the point of support and midswing corresponds to placement of the elbow directly beneath the shoulder (see Fig. 8). Note that in the gibbon, the cranial pectoralis major has a special role in the swing (recovery)phase ofthe locomotor cycle. Additionally it joins with several other muscles (not illustrated here) in effecting a pull-up just after midsupport. The late support and midswing phases of activity of cranial pectoralis major are only inconsistently present in spider monkeys. SWING (3-491 mel) SWING SUPPORT (1-11) k iUPPORT (3-44) SUPPORT SPIDER MONKEY ARM SWINGING SWING (2-45) 1 SWING (2-23) 23 EMG OF PECTORALIS MAJOR SPIDER MONKEY 2 1 3 5 4 GIBBON 1 2 c 3 4 5 _ Fig. 8. Drawings of limb positions during armswinging inAteles and Hylobates. 1 = onset of right limb support phase, 2 = midsupport by right forelimb, 3 = end of right limb support phase, 4 = midswing of right forelimb, 5 = onset of right limb support phase. Though several differences are illustrated, ofgreatest significance for the present study are: 1) the pull-up executed by the gibbon in the second half of the support phase; and 2) the adducted arm and flexed forearm of the gibbon during swing phase. Both behaviors represent part of a "perfected'mechanism for armswinging. The first serves to elevate the center ofgravity to enable the animal to rise higher a t the end of support phase for the purpose of permitting a greater drop, and thus greater acceleration due to gravity, during the following cycle (Fleagle, '77). The position of the forelimb during swing phase reduces its moment of inertia and enables a rapid execution of recovery. bates during vertical climbing, pronograde quadrupedalism, and armswinging demonstrate that although the cranial portion of the muscle assists the caudal portion during retraction of the previously protracted (elevated) forelimb, the unique role of the cranial portion is for flexion of the adducted forelimb as required in the recovery phase of the locomotor cycle. Does knowledge of this unique role help us to explain why in some primates the origin of the pectoralis major has extended far onto the clavicle,whereas in others an attachment to the manubrium suffices? A clavicular origin of pectoralis major might be necessary to promote flexion of the forelimb in animals in which the humeral insertion of the muscle is on the same transverse plane as, or cranial to, the manubrium. Such will be the case during much of the locomotor cycle in primates that have a shoulder joint cranial to t h e level of t h e manubrium. Schultz ('26, '33, '56) provides values of a " l L4 JACK T.STERN, JR., ET AL ratio called relative shoulder height, which is calculated by dividing the distance between the suprasternal notch and interacromial line by the anterior t r u n k height, then multiplying by 100. The larger the value of this index, the more cranial is the shoulder joint relative to the manubrium. Schultz notes that high values characterize the apes (Hylobates = 13, Pongo = 16, Pan troglodytes = 17, P. gorilla = 13), spider monkeys (Ateles = lo), and howling monkeys (Alouatta = 131, whereas a low value (51, indicating a shoulderjoint near the same level as the manubrium, characterizes Old World monkeys and Saimiri. Figure 3 of the monograph by Schultz ('56) indicates a similarity between Old World monkeys and prosimians. Our measurements on one spider monkey, two woolly monkeys, and one howler, all under anesthesia, yield values for the shoulder height index of 16, 13, and 11 respectively for these genera. An additional line of evidence is provided by Jenkins, et al. ('78) who demonstrated radiographically that the level of the shoulder joint lies far cranial to the sternoclavicular joint in Ateles during hanging by the forelimb, whereas in Macaca, Cercopithecus, and Saimiri even this behavior is insufficient to displace the joint cranially. The distribution of a cranially displaced shoulderjoint suggests very strongly that it is a trait associated with remodelling of the shoulder complex for the enhanced mobility required by primates that employ their upper limb in climbing and suspension.:' Among nonhuman primates, it is only those with cranially displaced shoulder joints that possess a significant clavicular origin of pectoralis major. Nonetheless, within this group, the spider monkey and orangutan have not evolved this trait. The explanation for the absence of a clavicular origin of pectoralis major inAteles and Pongo may be that the behavior of these animals does not demand particular facility for flexion of the adducted forelimb. Such facility is required for rapid pronograde progression either in the trees (Alouatta, Lagothrix) or on the ground (P. troglodytes, P. paniscus, P. gorilla). It is probably necessary for the ascent of thick tree trunks, a behavior especially important for chimpanzees (Kortlandt, '75) and bonobos (R. Susman, personal communication). In this regard it is interesting to note that such behavior is less significant for gorillas, and that gorillas possess a less extensive clavicular origin of pectoralis major than "However, Schultz 1'26) attributes the obliquity of the clavicles among howling monkeys to the presence of a greatly enlarged hyold apparatus. do chimpanzees (Ashton and Oxnard, '63). Finally, flexion of the adducted forelimb appears to be a vital element of perfected armswinging as demonstrated by Hylobates. Field studies of the spider monkey (Mittermeier and Fleagle, '76; Mittermeier, '78) and orangutan (MacKinnon, '74) indicate that these species practice pronograde quadrupedalism less frequently and either less speedily or more awkwardly than most primates. The same studies give no indication that ascent of thick vertical trunks is an habitual positional behavior of selective importance, as has been argued for chimpanzees and bonobos. Furthermore, armswinging in the orangutan is uncommon and the forelimb does not swing beneath the shoulder during recovery. The very presence of a prehensile tail in Ateles may be the single most important factor reducing the demand for mechanical perfection of armswinging. If this animal fails to reach the next support in adequate time, its safety is insured by the grasp of the tail. These considerations lead us to conclude that evolution of a cranial origin of the pectoralis major in nonhuman primates is a response to demands for strength or rapidity of flexion of the adducted forelimb in animals having undergone morphologic reconstruction of the shoulder to enhance upper limb mobility. Although the new muscular attachment has evolved in nonhuman primates only among those genera that practice behaviors emphasizing a mobile forelimb able to resist tensile forces, the need for this attachment is not related to use of the forelimb under tension in the abducted elevated position. Instead, a clavicular origin of pectoralis major may be viewed as compensating for the remodeling of the shoulder associated with these behaviors. It is a strength of the experimental method that it can elucidate such complex evolutionary mechanisms. A final consideration is whether or not studies of the cranial pectoralis major in nonhuman primates can shed light on the evolution of Homo, one of those rare primates with an extensive clavicular origin. Modern adult Caucasians have a relative shoulder height index less than 1 (Schultz, '26),i.e., their shoulder joint is on the same level as the manubrium. However, there is an ontogenetic descent of the shoulder to achieve this state. Schultz concluded that the fetal condition suggests the existence of a high shoulder in the human ancestor. One could speculate that a clavicular origin of pectoralis major was another characteristic of this ancestor. Even if the clavicular origin of pectoralis 25 EMG OF PECTORALIS MAJOR major in humans is a retention of a t r a i t evolved i n a n arboreal setting, t h e d a t a presented here do not point to one particular behavior that must have been practiced in our past. A clavicular origin of pectoralis major seems to serve as the “ideal morphology” for more than one behavior. It may have evolved to meet the demands of brachiation in gibbons and pronograde quadrupedalism in certain prehensile-tailed cebids and African apes. Further impetus to evolution of this trait in chimpanzees and bonobos can be attributed to the importance for these animals of climbing thick vertical trunks. The presence of a clavicular origin of pectoralis major in the arboreal ancestor of humans would imply a shoulder remodeled for mobility, as has been suggested on numerous other grounds (Washburn, ‘63; Oxnard, ’69), and would detract from any suggestion that portrays this ancestor as being as completely devoted to quadrumanous climbing a s the modern orangutan. Having a relatively low shoulder joint, m d ern humans might not be expected to need a clavicular pectoralis major. This muscle is still a flexor of the adducted forelimb (see Basmajian, ’781, but it might be thought that a manubrial attachment would suffice. The distinct advantage of a clavicular origin in humans probably is not related to the early stages of forelimb flexion, as in nonhuman primates, but to one or both of the following requirements: 1) the ability to resist extension of the markedly flexed arm; 2) the ability to powerfully adduct the arm without simultaneous extension. The first of these behaviors is an essential element of forelimb use in carrying large objects. The second is a component of the movement involved in throwing. Permitting ourselves to engage in extreme speculation, we conclude that the existence of a clavicular origin of pectoralis major in a human ancestor might be a preadaptation to the ways in which the forelimb would be used in a bipedal descendant. ACKNOWLEDGMENTS Invaluable technical assistance was rendered by Marcy Koltun, William Korosh, and Lorraine Rice. The illustrations were lovingly prepared by Lucille Betti. Our special thanks go to Dr. Robert Gossette, Hofstra University, who so generously permitted us to conduct experiments on his two gibbons, and to the Los Angeles Zoo for providing a specimen of the red howler. This study was supported by NSF Research grant BNS 76831141201. LITERATURE CITED Ashton, E.H., and C.E. Oxnard (1963) The musculature of the primate shoulder. Trans. Zool. SOC.(Lond.), 29:55% 650. 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