Patterns of strain in the macaque tibia during functional activity.

The strain environment of the tibial midshaft of two female macaques was evaluated through in vivo bone strain experiments using three rosette gauges around the circumference of the bones. Strains were collected for a total of 123 walking and galloping steps as well as several climbing cycles. Principal strains and the angle of the maximum (tensile) principal strain with the long axis of the bone were calculated for each gauge site. In addition, the normal strain distribution throughout the cross section was determined from the longitudinal normal strains (strains in the direction of the long axis of the bone) at each of the three gauge sites, and at the corresponding cross-sectional geometry of the bone. This strain distribution was compared with the cross-sectional properties (area moments) of the midshaft. For both animals, the predominant loading regime was found to be bending about an oblique axis running from anterolateral to posteromedial. The anterior and part of the medial cortex are in tension; the posterior and part of the lateral cortex are in compression. The axis of bending does not coincide with the maximum principal axis of the cross section, which runs mediolaterally. The bones are not especially buttressed in the plane of bending, but offer the greatest strength anteroposteriorly. The cross-sectional geometry therefore does not minimize strain or bone tissue. Peak tibial strains are slightly higher than the peak ulnar strains reported earlier for the same animals (Demes et al. [1998] Am J Phys Anthropol 106:87-100). Peak strains for both the tibia and the ulna are moderate in comparison to strains recorded during walking and galloping activities in nonprimate mammals.

Telemetered electromyography of the supinators and pronators of the forearm in gibbons and chimpanzees: implications for the fundamental positional adaptation of hominoids.

Extant apes are similar to one another, and different from monkeys, in features granting them greater range of forearm rotation and greater size of the muscles that produce this motion. Although these traits may have been independently acquired by the various apes, the possibility arises that such features reflect adaptation to the stem behavior of the hominoid lineage. Anticipating that knowledge of forearm rotatory muscle recruitment during brachiation, vertical climbing, arm-hanging during feeding, and voluntary reaching might point to this stem behavior, we undertook telemetered electromyographic experiments on the supinator, pronator quadratus, ulnar head of pronator teres, and a variety of other upper limb muscles in two gibbons and four chimpanzees. The primary rotator muscles of the hominoid forearm were recruited at high levels in a variety of behaviors. As had been suspected by previous researchers, the supinator is usually active during the support phase of armswinging, but we observed numerous instances of this behavior during which the muscle was inactive. No other muscle took over its role. Kinetic analyses are required to determine how apes can execute body rotation of armswinging without active muscular effort. The one behavior that is common to most extant apes, is rare in monkeys, and which places a consistently great demand on the primary forearm rotatory muscles, is hang-feeding. The muscles of the supporting limb are essential to properly position the body; those of the free limb are essential for grasping food. Since the greater range of forearm rotation characterizing apes is also best explained by adaptation to this behavior, we join previous authors who assert that it lies at the very origin of the Hominoidea.

Function and cytochemical characteristics of postural limb muscles of the rhesus monkey: A telemetered EMG and immunofluorescence study.

Using telemetered electromyography and immunocytochemical fibre typing (of both fresh frozen and preserved specimens), the present paper demonstrates clearly that at the elbow, knee, and ankle joints, the rhesus monkey (Macaca mulatta) is endowed with one extensor-muscle head specialized for posture. These postural heads are distinguished by (a) recruitment at low levels to maintain joint position against the effect of gravity, (b) recruitment near maximum levels during walking, and (c) high content and relatively large size of slow, fatigue-resistant (type I) muscle fibres. The nonpostural heads of the investigated muscles were recruited at levels correlated to the strenuousness of the effort and are notable by the small percentage and size of slow muscle fibres. The postmortem stability of the structural properties of myosin makes immunocytochemical fibre typing suitable for the study of preserved cadavers.

Patterns of strain in the macaque ulna during functional activity.

In vivo bone strain experiments were performed on the ulnae of three female rhesus macaques to test how the bone deforms during locomotion. The null hypothesis was that, in an animal moving its limbs predominantly in sagittal planes, the ulna experiences anteroposterior bending. Three rosette strain gauges were attached around the circumference of the bone slightly distal to midshaft. They permit a complete characterization of the ulna's loading environment. Strains were recorded during walking and galloping activities. Principal strains and strain directions relative to the long axis of the bone were calculated for each gauge site. In all three animals, the lateral cortex experienced higher tensile than compressive principal strains during the stance phase of walking. Compressive strains predominated at the medial cortex of two animals (the gauge on this cortex of the third animal did not function). The posterior cortex was subject to lower strains; the nature of the strain was highly dependent on precise gauge position. The greater principal strains were aligned closely with the long axis of the bone in two animals, whereas they deviated up to 45 degrees from the long axis in the third animal. A gait change from walk to gallop was recorded for one animal. It was not accompanied by an incremental change in strain magnitudes. Strains are at the low end of the range of strain magnitudes recorded for walking gaits of nonprimate mammals. The measured distribution of strains in the rhesus monkey ulna indicates that mediolateral bending, rather than anteroposterior bending, is the predominant loading regime, with the neutral axis of bending running from anterior and slightly medial to posterior and slightly lateral. A variable degree of torsion was superimposed over this bending regime. Ulnar mediolateral bending is apparently caused by a ground reaction force vector that passes medial to the forearm. The macaque ulna is not reinforced in the plane of bending. The lack of buttressing in the loaded plane and the somewhat counterintuitive bending direction recommend caution with regard to conventional interpretations of long bone cross-sectional geometry.

Quantifying phalangeal curvature: an empirical comparison of alternative methods.

It has been generally assumed and theoretically argued that the curvature of finger and toe bones seen in some nonhuman primates is associated with cheiridial use in an arboreal setting. Assessment of such curvature in fossil primates has been used to infer the positional behavior of these animals. Several methods of quantifying curvature of bones have been proposed. The measure most commonly applied to phalanges is that of included angle, but this has come under some criticism. We consider various other approaches for quantifying phalangeal curvature, demonstrating that some are equivalent to use of included angle, but that one--normalized curvature moment arm (NCMA)--represents a true alternative. A comparison of NCMA to included angle, both calculated on manual and pedal proximal phalanges of humans, apes, some monkeys, and the Hadar fossils, revealed that these two different measures of curvature are highly correlated and result in very similar distributional patterns.

EMG of the digastric muscle in gibbon and orangutan: functional consequences of the loss of the anterior digastric in orangutans.

Unlike all other primates, the digastric muscle of the orangutan lacks an anterior belly; the posterior belly, while present, inserts directly onto the mandible. To understand the functional consequences of this morphologic novelty, the EMG activity patterns of the digastric muscle and other potential mandibular depressors were studied in a gibbon and an orangutan. The results suggest a significant degree of functional differentiation between the two digastric bellies. In the gibbon, the recruitment pattern of the posterior digastric during mastication is typically biphasic. It is an important mandibular depressor, active in this role during mastication and wide opening. It also acts with the anterior suprahyoid muscles to move the hyoid prior to jaw opening during mastication. The recruitment patterns of the anterior digastric suggest that it is functionally allied to the geniohyoid and mylohyoid. For example, although it transmits the force of the posterior digastric during mandibular depression, it functions independent of the posterior digastric during swallowing. Of the muscles studied, the posterior digastric was the only muscle to exhibit major differences in recruitment pattern between the two species. The posterior digastric retains its function as a mandibular depressor in orangutans, but is never recruited biphasically, and is not active prior to opening. The unique anatomy of the digastric muscle in orangutans results in decoupling of the mechanisms for hyoid movement and mandibular depression, and during unilateral activity it potentially contributes to substantial transverse movements of the mandible. Hypotheses to explain the loss of the anterior digastric should incorporate these functional conclusions.

Further evidence for the role of supraspinatus in quadrupedal monkeys.

Differences in the degree of projection of the greater tubercle above the level of the humeral head in primate proximal humeri have been associated with differing leverage requirements for supraspinatus during arboreal vs. terrestrial quadrupedal locomotion. Since most workers have assumed that supraspinatus acts as a humeral protractor, interpretations of the variation in greater tubercle height have focused on the need for powerful vs. rapid humeral protraction during the swing phase of quadrupedal locomotion. However, in an EMG study on the activity patterns of supraspinatus in the vervet monkey, Larson and Stern (Am. J. Phys. Anthropol. 79:369-377, 1989) reported that although supraspinatus is active during arm elevations against gravity, it is silent during the swing phase of quadrupedal locomotion, and instead acts as a joint stabilizer during support phase. They suggested that the pattern of activity for supraspinatus observed in the vervet was common for all quadrupedal primates, and that differences in greater tubercle projection could be related to the degree of mobility of the shoulder. In the current study, we present additional EMG data on a baboon and three macaques supporting the suggestions offered by Larson and Stern (1989).

EMG of serratus anterior and trapezius in the chimpanzee: scapular rotators revisited.

The importance of arm-raising has been a major consideration in the functional interpretation of differences in shoulder morphology among species of nonhuman primates. Among the characters that have been associated with enhancement of the arm-raising mechanism in hominoid primates are the relative enlargement of cranial trapezius and caudal serratus anterior, as the main scapular rotators, as well as changes in scapular morphology associated with their improved leverage for scapular rotation. Yet in an EMG study of cranial trapezius and caudal serratus anterior function in the great apes, Tuttle and Basmajian (Yrbk. Phys. Anthropol. 20:491-497, 1977) found these muscles to be essentially inactive during arm-raising. Although Tuttle and Basmajian suggest that the cranial orientation of the glenoid fossa in apes has reduced the demand for scapular rotation during arm-raising, subsequent EMG studies on other primate species suggest that these muscles do play a significant role in arm motion during active locomotion. This paper presents a reexamination of muscle recruitment patterns for trapezius and caudal serratus anterior in the chimpanzee. All but the lowest parts of caudal serratus anterior were found to be highly active during arm-raising motions, justifying earlier morphological interpretations of differences in caudal serratus anterior development. The lowest digitations of this muscle, while inactive during arm-raising, displayed significant activity during suspensory postures and locomotion, presumably to control the tendency of the scapula to shift cranially relative to the rib cage. Cranial trapezius did not appear to be involved in arm-raising; instead, its recruitment was closely tied to head position.

The capitular joint of the first rib in primates: a re-evaluation of the proposed link to locomotion.

Evidence exists that in Australopithecus afarensis the head of the first rib articulated with the body of the first thoracic vertebra but not with the body of the seventh cervical vertebra (Ohman, 1983, 1986). Thus, the Hadar hominid would have differed from most primates, in which both these vertebrae are involved in formation of the first costal capitular joint. Indeed, Ohman (1986) has claimed that a univertebral pattern is unique to modern and fossil hominids among primates. He offered various theories on the adaptive significance of this trait, chief among which was a link to freeing the upper limb from any role in locomotion. Believing that Ohman's statement about the distribution of the univertebral pattern in living forms was based on inadequate samples, we have compiled data on the first costal capitular joint in a wider range of primate genera. Our observations demonstrate that the univertebral pattern, rather than being unique to hominids, is common among siamangs, occurs in an occasional gibbon, and is typical of the larger indriids. Consequently, one can no longer accept any contention that the univertebral first costal capitular joint of A. afarensis implies that it did not use its upper limbs for locomotion. Rather, the formation of this joint is correlated with orthogrady and body size. We discuss a possible explanation of this correlation in terms of movement of the first rib during breathing in an orthograde primate, be it one that stands on two legs, swings by two arms, or clings to trunks using all four appendages.

The role of propulsive muscles of the shoulder during quadrupedalism in vervet monkeys (Cercopithecus aethiops): implications for neural control of locomotion in primates.

In comparative anatomical studies of the shoulder, the humeral retractors are often grouped together as propulsive muscles, which are important in the propulsive stroke of the forelimb during quadrupedal locomotion. Electromyographic (EMG) analyses of these muscles in opossums, cats, and dogs in general have confirmed such conclusions. An EMG study of chimpanzee shoulder muscles during knuckle-walking found, however, that the humeral retractors are either inactive or perform a function unrelated to propulsion (Larson & Stern, 1987). This contrast in muscle recruitment patterns between chimpanzees and more "typical" mammalian quadrupeds was attributed to the derived morphology of the chimpanzee shoulder. The present study examines the activity patterns of the humeral retractors in the vervet monkey, a primate more closely resembling nonprimate mammals in its shoulder morphology. The results of this EMG analysis show that despite the significant differences in anatomy between chimpanzees and vervets, the two species display very similar muscle recruitment patterns during quadrupedalism, and there is evidence for this same pattern in other species of primates. These differences in muscle activity patterns between primates and nonprimate mammals may be related to changes in the neurological control of locomotion in primates due to the evolutionary development of manipulative abilities in the primate forelimb.

Use of contralateral rectus femoris flap: an alternative for covering exposed femoral vessels of the thigh.

Myocutaneous coverage of large defects in the thigh following resection of tumors is necessary to ensure adequate protection of the underlying femoral vessels. The usual muscles employed as flaps to achieve this protection are ipsilateral sartorius, rectus femoris, tensor fasciae latae, gracilis, rectus abdominis, or vastus lateralis. However, for situations in which these muscles are not available, the surgeon needs an alternative flap. This report details the successful use of the contralateral rectus femoris muscle to cover exposed femoral vessels in the upper and middle thirds of the thigh. Findings of anatomical dissections confirm that, by freeing the muscle at its origin, its reach can be extended about 6 cm. Postoperatively, no functional deficits resulted from the flap and no damage to the skin graft occurred with radiation therapy. Use of the contralateral rectus femoris flap should therefore be considered when a reliable alternative to conventional flaps must be employed.

Role of supraspinatus in the quadrupedal locomotion of vervets (Cercopithecus aethiops): implications for interpretation of humeral morphology.

Various researchers have noted that terrestrial and arboreal monkeys often differ in the degree to which the greater tubercle of the humerus projects proximally beyond the profile of the humeral head. These differences have been associated with differing leverage requirements for supraspinatus during quadrupedal locomotion. Although Jolly (The Baboon in Medical Research, Vol. II., pp. 23-50, 1967) suggested that a projecting tubercle can be related to the ability of supraspinatus to control more exactly the passive humeral retraction that occurs during support phase of quadrupedalism, most workers emphasize a link between this bony trait and the need for powerful or rapid protraction of the forelimb during swing phase of terrestrial quadrupedalism. We report on an EMG analysis of supraspinatus function showing that the muscle does not act as a brachial protractor during quadrupedalism, even in the relatively cursorial vervet monkey. We suggest that differences in greater tubercle projection can be related to the degree of mobility of the shoulder, and that supraspinatus size is determined by the interaction of greater tubercle height, adaptive importance of brachial elevation, and body size.

EMG of scapulohumeral muscles in the chimpanzee during reaching and "arboreal" locomotion.

Current views on the function of the deltoid and rotator cuff muscles emphasize their roles in arm-raising as participants in a scapulohumeral force "couple." The acceptance of such a mechanism is based primarily on a 1944 EMG study of human shoulder muscle action. More recently, it has been suggested that shoulder joint stabilization constitutes a second and equally important function of the cuff musculature, especially in nonhuman primates which habitually use their forelimbs in overhead postural and locomotor activities. Few comparative data exist, however, on the actual recruitment patterns of these muscles in different species. In order to assess the general applicability of a scapulohumeral force couple model, and the functional significance of the differential development of the scapulohumeral musculature among primate species, we have undertaken a detailed study of shoulder muscle activity patterns in nonhuman primates employing telemetered electromyography, which permits examination of unfettered natural behaviors and locomotion. The results of our research on the chimpanzee, Pan troglodytes, on voluntary reaching and two forms of "arboreal" locomotion reveal four ways in which previous perceptions of the function of the scapulohumeral muscles must be revised: 1) the posterior deltoid is completely different in function from the middle and anterior regions of this muscle; 2) the integrity of the glenohumeral joint during suspensory postures is not maintained solely by osseoligamentous structures; 3) the function of teres minor is entirely different from that of the other rotator cuff muscles and is more similar to the posterior deltoid and teres major; and 4) each remaining member of the rotator cuff plays a distinct, and often unique, role during natural behaviors. These results clearly refute the view that the muscles of the rotator cuff act as a single functional unit in any way, and an alternative to the force couple model is proposed.

Arboreality and bipedality in the Hadar hominids.

Numerous studies of the locomotor skeleton of the Hadar hominids have revealed traits indicative of both arboreal climbing/suspension and terrestrial bipedalism. These earliest known hominids must have devoted part of their activities to feeding, sleeping and/or predator avoidance in trees, while also spending time on the ground where they moved bipedally. In this paper we offer new data on phalangeal length and curvature, morphology of the tarsus and metatarsophalangeal joints, and body proportions that further strengthen the argument for arboreality in the Hadar hominids. We also provide additional evidence on limb and pedal proportions and on the functional anatomy of the hip, knee and foot, indicating that the bipedality practiced at Hadar differed from that of modern humans. Consideration of the ecology at Hadar, in conjunction with modern primate models, supports the notion of arboredality in these earliest australopithecines. We speculate that selection for terrestrial bipedality may have intensified through the Plio-Pleistocene as forests and woodland patches shrunk and the need arose to move increasingly longer distances on the ground. Only with Homo erectus might body size, culture and other factors have combined to 'release' hominids from their dependence on trees.

Electromyographic studies of the human foot: experimental approaches to hominid evolution.

Theories about the functions of the foot muscles have centered on their role in arch support. Previous anatomical and electromyographic studies (reviewed herein) have demonstrated that the arches are normally maintained by bones and ligaments. This study reports an electromyographic investigation of five foot muscles (flexor digitorum longus, flexor digitorum brevis, flexor accessorius, abductor hallucis, and abductor digiti quinti) conducted on four humans. The three toe flexors act together to resist extension of the toes during the stance phase of locomotion. Despite the large flexor accessorius in humans, neither this muscle nor the flexor digitorum brevis are preferentially recruited over the flexor digitorum longus for any normal posture or locomotion. The abductors affect the mediolateral distribution of pressure by positioning the forefoot. We suggest that the foot muscles play an important role in positioning of the forces on the foot in both posture and locomotion. Future electromyographic experiments on human and ape foot muscles in conjunction with detailed studies of early hominid fossils promise to elucidate the pathways of human locomotor evolution.

The locomotor anatomy of Australopithecus afarensis.

The postcranial skeleton of Australopithecus afarensis from the Hadar Formation, Ethiopia, and the footprints from the Laetoli Beds of northern Tanzania, are analyzed with the goal of determining (1) the extent to which this ancient hominid practiced forms of locomotion other than terrestrial bipedality, and (2) whether or not the terrestrial bipedalism of A. afarensis was notably different from that of modern humans. It is demonstrated that A. afarensis possessed anatomic characteristics that indicate a significant adaptation for movement in the trees. Other structural features point to a mode of terrestrial bipedality that involved less extension at the hip and knee than occurs in modern humans, and only limited transfer of weight onto the medial part of the ball of the foot, but such conclusions remain more tentative than that asserting substantive arboreality. A comparison of the specimens representing smaller individuals, presumably female, to those of larger individuals, presumably male, suggests sexual differences in locomotor behavior linked to marked size dimorphism. The males were probably less arboreal and engaged more frequently in terrestrial bipedalism. In our opinion, A. afarensis from Hadar is very close to what can be called a "missing link." We speculate that earlier representatives of the A. afarensis lineage will present not a combination of arboreal and bipedal traits, but rather the anatomy of a generalized ape.

Functional Morphology of Homo habilis.

Olduvai hominid (O.H.) fossils 7, 8, and 35 represent the earliest species of the genus Homo dated at 1.76 million years. The O.H. 7 hand, jaw, and skull and the O.H. 8 foot come from one subadult individual, and the O.H. 35 leg are also those of Homo habilis. The skeleton represents a mosaic of primitive and derived features, indicating an early hominid which walked bipedally and could fabricate stone tools but also retained the generalized hominoid capacity to climb trees.

Function of the subclavius muscle in a nonhuman primate, the spider monkey (Ateles).

Within the primate order, the morphology of the subclavius muscle is known to be unique among the prehensile-tailed South American monkeys. 3 spider monkeys, Ateles, were monitored electromyographically to determine the recruitment of this muscle during various locomotor and postural activities. Rather than indicating a static stabilizing function, which has typically been inferred from classical anatomical studies, results from this study suggest that the subclavius performs more as a dynamic element in movements of the pectoral girdle during brachiation, vertical climbing, pronograde quadrupedalism and leaping. Complementary activity patterns were also identified between the subclavius and the caudal fibers of the trapezius indicating that the subclavius is used when the animal must depress, or resist cranial displacement, of the protracted shoulder girdle, while the caudal trapezius is recruited when the girdle is retracted on the chest wall.