Muscle architecture of the common chimpanzee (Pan troglodytes): perspectives for investigating chimpanzee behavior

Thorpe et al. (Am J Phys Anthropol 110:179–199, 1999) quantified chimpanzee (Pan troglodytes) muscle architecture and joint moment arms to determine whether they functionally compensated for structural differences between chimpanzees and humans. They observed enough distinction to conclude that musculoskeletal properties were not compensatory and suggested that chimpanzees and humans do not exhibit dynamically similar movements. These investigators based their assessment on unilateral limb musculatures from three male chimpanzees, of which they called one non-adult representative. Factors such as age, sex, and behavioral lateralization may be responsible for variation in chimpanzee muscle architecture, but this is presently unknown. While the full extent of variation in chimpanzee muscle architecture due to such factors cannot be evaluated with data presently available, the present study expands the chimpanzee dataset and provides a preliminary glimpse of the potential relevance of these factors. Thirty-seven forelimb and 36 hind limb muscles were assessed in two chimpanzee cadavers: one unilaterally (right limbs), and one bilaterally. Mass, fiber length, and physiological cross-sectional area (PCSA) are reported for individual muscles and muscle groups. The musculature of an adult female is more similar in architectural patterns to a young male chimpanzee than to humans, particularly when comparing muscle groups. Age- and sex-related intraspecific differences do not obscure chimpanzee-human interspecific differences. Side asymmetry in one chimpanzee, despite consistent forelimb directional asymmetry, also does not exceed the magnitude of chimpanzee-human differences. Left forelimb muscles, on average, usually had higher masses and longer fiber lengths than right, while right forelimb muscles, on average, usually had greater PCSAs than left. Most muscle groups from the left forelimb exhibited greater masses than right groups, but group asymmetry was significant only for the manual digital muscles. The hind limb exhibited less asymmetry than the forelimb in most comparisons. Examination of additional chimpanzees would clarify the full range of inter- and intra-individual variation.     

Dimensions and moment arms of the hind- and forelimb muscles of common chimpanzees (Pan troglodytes).

This paper supplies quantitative data on the hind- and forelimb musculature of common chimpanzees (Pan troglodytes) and calculates maximum joint moments of force as a contribution to a better understanding of the differences between chimpanzee and human locomotion. We dissected three chimpanzees, and recorded muscle mass, fascicle length, and physiological cross-sectional area (PCSA). We also obtained flexion/extension moment arms of the major muscles about the limb joints. We find that in the hindlimb, chimpanzees possess longer fascicles in most muscles but smaller PCSAs than are predicted for humans of equal body mass, suggesting that the adaptive emphasis in chimpanzees is on joint mobility at the expense of tension production. In common chimpanzee bipedalism, both hips and knees are significantly more flexed than in humans, necessitating muscles capable of exerting larger moments at the joints for the same ground force. However, we find that when subject to the same stresses, chimpanzee hindlimb muscles provide far smaller moments at the joints than humans, particularly the quadriceps and plantar flexors. In contrast, all forelimb muscle masses, fascicle lengths, and PCSAs are smaller in humans than in chimpanzees, reflecting the use of the forelimbs in chimpanzee, but not human, locomotion. When subject to the same stresses, chimpanzee forelimb muscles provide larger moments at the joints than humans, presumably because of the demands on the forelimbs during locomotion. These differences in muscle architecture and function help to explain why chimpanzees are restricted in their ability to walk, and particularly to run bipedally.     

Electromyography of back muscles during quadrupedal and bipedal walking in primates

Despite the extensive electromyographic research that has addressed limb muscle function during primate quadrupedalism, the role of the back muscles in this locomotor behavior has remained undocumented. We report here the results of an electromyographic (EMG) analysis of three intrinsic back muscles (multifidus, longissimus, and iliocostalis) in the baboon (Papio anubis), chimpanzee (Pan troglodytes), and orangutan (Pongo pygmaeus) during quadrupedal walking. The recruitment patterns of these three back muscles are compared to those reported for the same muscles during nonprimate quadrupedalism. In addition, the function of the back muscles during quadrupedalism and bipedalism in the two hominoids is compared. Results indicate that the back muscles restrict trunk movements during quadrupedalism by contracting with the touchdown of one or both feet, with more consistent activity associated with touchdown of the contralateral foot. Moreover, despite reported differences in their gait preferences and forelimb muscle EMG patterns, primates and nonprimate mammals recruit their back muscles in an essentially similar fashion during quadrupedal walking. These quadrupedal EMG patterns also resemble those reported for chimpanzees, gibbons and humans (but not orangutans) walking bipedally. The fundamental similarity in back muscle function across species and locomotor behaviors is consistent with other data pointing to conservatism in the evolution of the neural control of tetrapod limb movement, but does not preclude the suggestion (based on forelimb muscle EMG and spinal lesion studies) that some aspects of primate neural circuitry are unique. © 1994 Wiley-Liss, Inc.     

Telemetered electromyography of flexor digitorum profundus and flexor digitorum superficialis in Pan troglodytes and implications for interpretation of the O. H. 7 hand.

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 possibiltiy, 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 the 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 to help clear the fingers from the ground as the forelimb begins its recovery stroke. At the most rapid speeds, a slight to 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 at 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.     

Uniqueness of primate forelimb posture during quadrupedal locomotion

Among the characteristics that are thought to set primate quadrupedal locomotion apart from that of nonprimate mammals are a more protracted limb posture and larger limb angular excursion. However, kinematic aspects of primate or nonprimate quadrupedal locomotion have been documented in only a handful of species, and more widely for the hind than the forelimb. This study presents data on arm (humerus) and forelimb posture during walking for 102 species of mammals, including 53 nonhuman primates and 49 nonprimate mammals. The results demonstrate that primates uniformly display a more protracted arm and forelimb at hand touchdown of a step than nearly all other mammals. Although primates tend to end a step with a less retracted humerus, their total humeral or forelimb angular excursion exceeds that of other mammals. It is suggested that these features are components of functional adaptations to locomotion in an arboreal habitat, using clawless, grasping extremities.     

Understanding hind limb weight support in chimpanzees with implications for the evolution of primate locomotion

Most quadrupedal mammals support a larger amount of body weight on their forelimbs compared with their hind limbs during locomotion, whereas most primates support more of their body weight on their hind limbs. Increased hind limb weight support is generally interpreted as an adaptation that reduces stress on primates' highly mobile forelimb joints. Thus, increased hind limb weight support was likely vital for the evolution of primate arboreality. Despite its evolutionary importance, the mechanism used by primates to achieve this important kinetic pattern remains unclear. Here, we examine weight support patterns in a sample of chimpanzees (Pan troglodytes) to test the hypothesis that limb position, combined with whole body center of mass position (COM), explains increased hind limb weight support in this taxon. Chimpanzees have a COM midway between their shoulders and hips and walk with a relatively protracted hind limb and a relatively vertical forelimb, averaged over a step. Thus, the limb kinematics of chimpanzees brings their feet closer to the COM than their hands, generating greater hind limb weight support. Comparative data suggest that these same factors likely explain weight support patterns for a broader sample of primates. It remains unclear whether primates use these limb kinematics to increase hind limb weight support, or whether they are byproducts of other gait characteristics. The latter hypothesis raises the intriguing possibility that primate weight support patterns actually evolved as byproducts of other traits, or spandrels, rather than as adaptations to increase forelimb mobility. Am J Phys Anthropol, 2009. © 2008 Wiley‐Liss, Inc.     

The effect of branch diameter on primate gait sequence pattern

Most mammals use lateral sequence gaits during quadrupedal locomotion, a pattern characterized by the touchdown of a forelimb directly following the ipsilateral hind limb in a given stride cycle. Primates, however, tend to use diagonal sequence (DS) gaits, whereby it is the touchdown of a contralateral forelimb that follows that of a given hind limb most closely in time. A number of scenarios have been offered to explain why primates favor DS gaits, most of them relating to the use of the arboreal habitat and, in particular, the exploitation of a narrow branch niche. This experimental study explores the potential explanation for the use of DS gaits by examining the relationship between branch diameter and gait patterns in 360 strides collected from six species of quadrupedal strepsirrhine primates on broad and narrow diameter supports. Gait sequence is quantified using limb phase, or the percentage of time during a stride cycle that a forelimb touchdown follows an ipsilateral hind limb touchdown. Although Loris, Nycticebus and Eulemur rubriventer individuals in this study did exhibit significantly lower locomotor velocities on narrower supports (P<0.01 in all three species), analyses of covariance showed no significant differences in limb phase values between broad and narrow diameter supports. Hence, results indicate surprisingly little evidence to suggest that alterations in gait sequence pattern provide a specific advantage for negotiating narrow supports.     

Muscle architectural properties in the common marmoset (<Emphasis Type="Italic">Callithrix jacchus</Emphasis>)

The common marmoset, Callithrix jacchus, is a small New World monkey that has recently gained attention as an important experimental animal model in the field of neuroscience as well in rehabilitative and regenerative medicine. This attention reflects the closer phylogenetic relationship between humans and common marmosets compared to that between humans and other experimental animals. When studying the neuronal mechanism behind various types of neurological motor disorders using the common marmoset, possible differences in muscle parameters (e.g., the force-generating capacity of each of the muscles) between the common marmoset and other animals must be taken into account to permit accurate interpretation of observed motor behavior. Differences in the muscle architectural properties are expected to affect biomechanics, and hence to affect neuronal control of body movements. Therefore, we dissected the forelimbs and hind limbs of two common marmosets, including systematic analysis of the muscle mass, fascicle length, and physiological cross-sectional area (PCSA). Comparisons of the mass fractions and PCSA fractions of the forelimb and hind limb musculature among the common marmoset, human, Japanese macaque, and domestic cat demonstrated that the overall muscle architectural properties of the forelimbs and hind limbs in the common marmoset are very similar to those of the Japanese macaque, a typical quadrupedal primate. However, muscle architectural properties of the common marmoset differ from those of the domestic cat, which has relatively larger hamstrings and pedal digital flexor muscles. Compared to humans, the common marmoset exhibits relatively smaller shoulder protractor, retractor, and abductor muscles and larger elbow extensor and rotator-cuff muscles in the forelimb, and smaller plantarflexor muscles in the hind limb. These differences in the muscle architectural properties must be taken into account when interpreting motor behaviors such as locomotion and arm-reaching movements in the common marmoset.     

Subscapularis function in gibbons and chimpanzees: Implications for interpretation of humeral head torsion in hominoids

Chimpanzees and gibbons, along with other hominoids, share a number of features in the morphology of their shoulders that have generally been associated with use of the upper limb in overhead postural and locomotor activities. These include the position and shape of the scapula, as well as the morphology of the proximal end of the humerus. Results of an electromyographic (EMG) analysis of shoulder muscle activity patterns indicate that these two species of hominoids also share broad similarities in shoulder muscle function during locomotion and voluntary movements. Differences do exist, however, in the activity patterns of subscapularis, a medial rotator of the arm. These differences mainly involve a greater participation by the gibbon subscapularis in free arm movements. This greater participation is characterized by earlier onset of muscle activity, higher amplitude of recruitment, and involvement of more of the total mass of the muscle. These differences in muscle recruitment suggest that the shoulder of gibbons differs from that of chimpanzees in some manner that necessitates the greater contribution of a medial rotator to the production of motion in the upper limb. I suggest that the low degree of humeral head torsion in gibbons, compared to that of other hominoids, gives their elbow a “lateral set” that must be overcome by the action of subscapularis during free arm movements. I propose that this modest degree of humeral head torsion in gibbons reflects a compromise between necessary changes caused by the repositioning of the scapula onto the dorsum of the thorax and the demands for extreme positioning of the elbow during brachiation. In addition, I suggest that the greater amount of torsion in the chimpanzee humerus is an accommodation to quadrupedal habits, and finally, that the high degree of torsion in human humeri is an independently acquired trait related to use of the upper limb as a manipulatory organ.     

Electromyography of pongid shoulder muscles III. Quadrupedal positional behavior

Electromyographic (EMG) recordings were taken from 14 shoulder muscles (or major parts of them) in a gorilla, a chimpanzee and an orangutan as they stood quadrupedally and tripedally, descended from elevated substrates, crutch-walked, and progressed quadrupedally on inclined and level substrates. In the African apes, low potentials commonly (but not always) occurred in the sternocostal pectoralis major, anterior deltoid, supraspinatus and subscapularis muscles during quadrupedal stance. The quadrupedal orangutan always exhibited low potentials in the pectoralis major muscle and EMG activity commonly occurred in her supraspinatus and subscapularis muscles. Quiescent tripedal stances were not accompanied by striking changes in EMG patterns from those which characterized quadrupedal stances. Per contra, eccentric loadings of the forelimb during descents from elevated substrates generally recruited notable EMG activity in the deltoid, supraspinatus and, to a lesser extent, infraspinatus muscles of the three pongid apes. The pectoralis major and caudal serratus anterior muscles were much more active in Pongo and Pan during these descents. Supportive segments of quadrupedal locomotive cycles were generally accompanied by EMG activity in the pectoralis major, intermediate and posterior deltoid and supraspinatus muscles. The intermediate and posterior deltoid muscles were characteristically active during pre-release of the hand and early swing phase. The cranial trapezius and supraspinatus muscles also may act during early swing phase. We conclude that the pectoralis major and perhaps the supraspinatus and subscapularis might serve regularly as postural muscles during static terrestrial quadrupedalism in pongid apes. The lack of dramatic differences between the EMG patterns exhibited during fist-walking versus knuckle-walking indicates that an evolutionary transformation from a shoulder complex like that of Pongo to ones like Pan or vice versa need not entail major changes in myological features.     

Electromyographic activity in the Rhesus monkey forelimb muscles during a goal directed movement and locomotion before, during and after spaceflight

The aim of the present study was to analyse the effects of microgravity on i) the achievement of goal-directed arm movements and ii) the quadrupedal non-human primate locomotion. A reaching movement in weightlessness would require less muscle contraction since there is no need to oppose gravity. Consequently the electromyographic (EMG) activity of the monkey forelimb muscles should be changed during or after spaceflight. EMG activity of the biceps and triceps muscles during goal-directed arm movements were studied in Rhesus monkeys before, during and after 14 days of spaceflight and flight simulation at normal gravity. The EMG activity was also recorded during treadmill locomotion before and after spaceflight. When performing arm motor tasks, the delay values of the EMG bursts were unchanged during the flight. On the contrary, mean EMG was significantly decreased during the flight comparatively to the pre- and post-flight values, which were very similar. Compared with flight animals, the control ground monkey showed no change in the burst durations and mean EMG. After spaceflight, quadrupedal locomotion was modified. The animals had some difficulty in moving, and abnormal steps were numerous. The integrated area of triceps bursts was increased for the stance phase during locomotion. Taken together these data showed that spaceflight induces a dual adaptative process: first, the discharge of the motor pools of the forelimb musculature was modified during exposure to microgravity, and then upon return to Earth, monkeys changed their new motor strategy and re-adapt to normal gravity.     

Ontogeny of limb force distribution in squirrel monkeys (Saimiri boliviensis): insights into the mechanical bases of primate hind limb dominance

The distribution of peak vertical forces between the forelimbs and the hind limbs is one of the key traits distinguishing primate quadrupedal locomotion from that of other mammals. Whereas most mammals generate greater peak vertical forelimb forces, primates generate greater peak vertical hind limb forces. At the ultimate level, hind limb dominance in limb force distribution is typically interpreted as an adaptation to facilitate fine-branch arboreality. However, the proximate biomechanical bases for primate limb force distribution remain controversial. Three models have been previously proposed. The Center of Mass (COM) Position model attributes primates’ unique mode of limb loading to differences in the position of the whole-body COM relative to the hands and feet. The Active Weight Shift model asserts that primates actively redistribute body weight to their hind limbs by pitching the trunk up via the activation of hind limb retractor muscles. Finally, the Limb Compliance model argues that primates selectively mitigate forelimb forces by maintaining a compliant forelimb and a flat shoulder trajectory. Here, a detailed dataset of ontogenetic changes in morphology and locomotor mechanics in Bolivian squirrel monkeys (Saimiri boliviensis) was employed as a model system to evaluate each of these proposed models in turn. Over the first 10 months of life, squirrel monkeys transitioned from forelimb dominant infants to hind limb dominant juveniles, a change that was precipitated by decreases in peak vertical forelimb forces and increases in peak vertical hind limb forces. Results provided some support for all three of the models, although the COM Position and Active Weight Shift models were most strongly supported by the data. Overall, this study suggests that primates may use a variety of biomechanical strategies to achieve hind limb dominance in limb force distribution.     

Hopping and swimming in the leopard frog,Rana pipiens: I. Step cycles and kinematics

This study presents a model for the step cycle patterns used during both hopping and swimming by the leopard frog, Rana pipiens. The two behaviors are essentially similar in movement pattern and in the ways they are modified from quadrupedal gaits. In hopping, there is marked hind limb extension throughout stance. The swing begins with a suspension equivalent to the leap that occurs in a galloping or bounding quadruped. Following suspension, as the frog descends from the apex of its leap, the hind limbs remain posterior and in line with the spine while they flex. Near the end of flexion, there is a rapid downward rotation of the hindquarters to bring the hind feet underneath the body. This movement utilizes the planted forelimb as a pivot. A similar pattern of movement occurs in swimming; the stance (propulsion) phase involves extension at all hind limb joints. The swing (recovery) phase begins with the hind feet fully extended and includes a protracted gliding phase, equivalent to the suspension in the hop. The hind limb then recovers to its initial position during a flexion phase. Since there is no landing and the hind limbs remain lateral rather than ventral to the pelvis, less flexion occurs in the spine or the limb joints. In both behaviors, the extensor muscles of hip (M. semimembranosus), knee (M. cruralis), and ankle (M. plantaris longus) achieve their longest lengths, when they likely can produce near maximal force, at the beginning of extension. All three muscles shorten during extension, but, because they are multiple-joint muscles, the amount of shortening is relatively small (≈ 15%). Hopping and swimming in frogs are comparable asymmetrical gaits with the same relative contact intervals (25% of stride). The step cycles in both gaits are modified from quadrupedal locomotion in the same ways: by 1) loss of knee and ankle extension toward the ground prior to landing (or end of flexion in swimming), 2) loss of a yield phase on landing (or end of flexion in swimming), and 3) inclusion of extended suspensions in both gaits. © 1996 Wiley-Liss, Inc.     

Tripedal knuckle-walking: a proposal for the evolution of human locomotion and handedness.

A comparative morphological analysis of human and non-human hominoids was conducted in an attempt to determine the mode of locomotion of the protohominid. Although the generalized hominoid anatomy permits variation of locomotion: brachiation, knuckle-walking, etc., minor variations in structure determine which behavior is favored. Arboreal arm swinging requires a flexible forelimb while terrestrial fist or knuckle-walking demands more rigidity of the hand and wrist. It is demonstrated that the large human thumb accompanied by the strong adduction of the thenar, hypothenar, and palmar interosseous muscles offer powerful rigidity to the hand, while fusion of the os centrale with the scaphoid during gestation permits the formation of an arch of carpals which imbue the wrist with the stability necessary for weight bearing. Fascialization of the contrahentes and dorsiepitrochlearis muscles in the human as well as depilation of the middle phalanges; the webbing (syndactyly) of the palm; the direction of the fibers of the interosseous membrane of the forearm; the shape of the puerile annular ligament, and the direction of the human glenoid fossa strongly suggest that the ancestor of man used a knuckle-walking form of locomotion prior to becoming bipedal. A model is presented that suggests that bipedalism was attained through an intermediate stage of tripedalism. The model is based on the fact that man's anatomy is much more asymmetric than that of the great apes. A presumption is made that due to the absence of trees for climbing in the transition from forest to open plain, the protohominid needed to carry tools (stones) at all times for protection. Stones could be carried for long distances on the posterior iliac crest since the weight would be shifted posteriorly over the legs. Pick up, medial rotation and adduction of the stone would employ a two-muscle chain of biceps brachii and latissimus dorsi. On the iliac crest, the stone is posterior to the coronal plane of the glenohumeral joint, and with the contraction of this two-muscle chain, the shoulder on one side is moved posteriorly effecting a semi-erect posture. It is proposed that tripedalism of the protohominid may be an explanation for the handedness unique to hominids.     

Sexual selection on forelimb muscles of western grey kangaroos (Skippy was clearly a female)

Studies of sexual selection have tended to concentrate on obvious morphological dimorphisms such as crests, horns, antlers, and other physical displays or weapons; however, traits that show no obvious sexual dimorphism may nevertheless still be under sexual selection. Sexual selection theory generally predicts positive allometry for sexually selected traits. When fighting, male kangaroos use their forelimbs to clasp and hold their opponent and, standing on their tail, bring up their hind legs to kick their opponent. This action requires substantial strength and balance. We examined allometry of forelimb musculature in male and female western grey kangaroos (Macropus fuliginosus) to determine whether selection through male–male competition is associated with sex differences in muscle development. Forelimbs of males are more exaggerated than in females, with relatively greater muscle mass in males than the equivalent muscles in females. Furthermore, while muscles generally showed isometric growth in female forelimbs, every muscle demonstrated positive allometry in males. The significant positive allometry in male forelimb musculature, particularly those muscles most likely involved in male–male combat (a group of muscles involved in grasping: shoulder adduction, elbow flexion; and pulling: arm retraction, elbow flexion), clearly suggests that this musculature is subject to sexual selection. In addition to contributing to locomotion, the forelimbs of male kangaroos can also act as a signal, a weapon, and help in clasping, features that would contribute towards their importance as a sexually selected trait. Males would therefore benefit from well‐developed musculature of the arms and upper body during competition for mates. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 923–931.     

Elbow joint adductor moment arm as an indicator of forelimb posture in extinct quadrupedal tetrapods

Forelimb posture has been a controversial aspect of reconstructing locomotor behaviour in extinct quadrupedal tetrapods. This is partly owing to the qualitative and subjective nature of typical methods, which focus on bony articulations that are often ambiguous and unvalidated postural indicators. Here we outline a new, quantitatively based forelimb posture index that is applicable to a majority of extant tetrapods. By determining the degree of elbow joint adduction/abduction mobility in several tetrapods, the carpal flexor muscles were determined to also play a role as elbow adductors. Such adduction may play a major role during the stance phase in sprawling postures. This role is different from those of upright/sagittal and sloth-like creeping postures, which, respectively, depend more on elbow extensors and flexors. Our measurements of elbow muscle moment arms in 318 extant tetrapod skeletons (Lissamphibia, Synapsida and Reptilia: 33 major clades and 263 genera) revealed that sprawling, sagittal and creeping tetrapods, respectively, emphasize elbow adductor, extensor and flexor muscles. Furthermore, scansorial and non-scansorial taxa, respectively, emphasize flexors and extensors. Thus, forelimb postures of extinct tetrapods can be qualitatively classified based on our quantitative index. Using this method, we find that Triceratops (Ceratopsidae), Anhanguera (Pterosauria) and desmostylian mammals are categorized as upright/sagittally locomoting taxa.     

Hindlimb dominance during primate high-speed locomotion

Quadrupedal locomotion was mechanically studied for four species of primates, the chimpanzee, the rhesus macaque, the tufted capuchin, and the ring-tailed lemur, from low to high speeds of about two to ten times the anterior trunk length per second. A wide variety of locomotor patterns was observed during the high-speed locomotion of these primates. Positive correlations were observed between the peak magnitude of foot force components and speed. The differentiation of the foot force between the forelimb and the hindlimb did not largely change with a change of speed for each species. The vertical component and the accelerating component for the rhesus macaque were relatively large in the forelimb from low- to high-speed locomotion. The rhesus macaque, which habitually locomotes on the ground, differed in the quadrupedal locomotion from the other relatively arboreal primates, for which the hindlimb was clearly dominant in their dynamic force-producing distribution between the forelimbs and the hindlimbs. The previously reported locomotor difference, which was indicated among primates from the foot force pattern between the forelimb and the hindlimb during walking, also applied to high-speed locomotion.     

Fiber architecture of the intrinsic muscles of the shoulder and arm in semiterrestrial and arboreal guenons

The internal organization of myofibers and connective tissues has important physiologic implications for muscle function and for naturalistic behavior. In this study of forelimb muscle morphology and primate locomotion, fiber architecture is examined in the intrinsic muscles of the shoulder (musculi deltoideus, infraspinatus, supraspinatus, subscapularis, teres major, and t. minor) and arm (m. coracobrachialis, biceps brachii, brachialis, and triceps brachii) in the semiterrestrial vervets (Chlorocebus aethiops) and arboreal red-tailed guenons (Cercopithecus ascanius). Wet weights and lengths of whole muscles, lengths of fasciculi and their associated proximal and distal tendons, and angles of pinnation were measured to estimate morphologic correlates of physiologic properties of individual muscles: force, velocity/excursion, energy expense, and relative isometric or isotonic contraction. Neither mean total-shoulder:total-arm ratios for muscle mass nor total reduced physiological cross-sectional area exhibited significant (P < 0.05) interspecific differences, thus emphasizing the importance of fine-tuning musculoskeletal analyses by the data collected here. The results generally support those previously published for quadriceps femoris and triceps surae of the hind limb in these species (Anapol and Barry [1996] Am. J. Phys. Anthropol. 99:429-447). The fiber architecture of the semiterrestrial vervets is largely suited for higher velocity while running on the ground. By contrast, the architectural configuration of red-tailed monkeys implies relatively isometric muscle contraction and passive storage of elastic strain energy for exploitation of the compliant canopy, where substrate components are situated beneath the sagittal plane of the animal. With respect to relative distribution of maximum potential force output among muscles of either shoulder or arm groups in these otherwise hind limb-dominated quadrupedal primates, statistically significant interspecific differences are best interpreted in light of braking, climbing, and, for vervets, the transition between ground and canopy.The interspecific differences shown here for the intrinsic muscles of the shoulder and arm underscore the significance of intramuscular morphology in reconciling structure and function with regard to locomotor behavior. Its analysis and interpretation lend support to consideration of "semiterrestrial" as a bona fide locomotor category uniquely different from what is practiced by dedicated arboreal and terrestrial quadrupeds that occasionally visit the habitat of one another. Data from a more committed terrestrial species would clarify this enigma.     

Interlimb coordination and gait in the brown lemur (Lemur fulvus) and the talapoin monkey (Miopithecus talapoin)

Patterns of interlimb coordination based on telemetered electromyography of extensor muscles are described for the brown lemur (Lemur fulvus) and the talapoin monkey (Miopithecus talapoin) in order to address the issue of possible motor programs for quadrupedal stepping in primates. Differences in modal patterns of ipsilateral limb coupling (phase intervals) between walking and galloping indicate that gait-specific programs do exist in primates, especially for symmetrical gaits. These preferred patterns distinguish primates from most other mammals (e.g., the domestic cat), but do not rule out the possibility of subtle differences among primates in species-specific mechanisms of neural control. Variability about the preferred modes is better interpreted as an expression of the flexibility or facultative capabilities of the neural mechanisms controlling locomotion than as “errors” in the motor program.     

Knuckle-walking and the evolution of hominoid hands

Knuckle-walking is a pattern of digitigrade locomotion unique to African apes among Primates. Only chimpanzees and gorillas are specially adapted for supporting weight on the dorsal aspects of middle phalanges of flexed hand digits II–V. When forced to the ground, most orangutans assume one of a variety of flexed hand postures, but they cannot knuckle-walk. Some orangutans place their hands in palmigrade postures which are impossible to African apes. The knuckle-walking hands and plantigrade feet of African apes are both morphologically and adaptively distinct from those of Pongo, their nearest relative among extant apes. These features are associated with a common adaptive shift to terrestrial locomotion and support placing chimpanzees and gorillas in the same genus Pan. It is further suggested than Pan comprises the subgenera (a) Pan, including P. troglodytes and pygmy chimpanzees, and (b) Gorilla, including mountain and lowland populations of P. gorilla. African apes probably diverged from ancestral pongids that were specially adapted for distributing their weight in terminal branches of the forest canopy. Early adjustments to terrestrial locomotion may have involved fist-walking which later evolved into knuckle-walking. Orangutans continued to adapt to feeding and locomotion in the forest canopy and their hands and feet became highly specialized for four-digit prehension. Although chimpanzees retained arboreal feeding and nesting habits, they moved from tree to tree by terrestrial routes and became less restricted in habitat. While adapting to a diet of ground plants gorillas increased in size to the point that arboreal nesting is less frequent among them than among chimpanzees and orangutans. Early hominids probably diverged from pongids that had not developed prospective adaptations to knuckle-walking, and therefore did not evolve through a knuckle-walking stage. Initial adjustments to terrestrial quadrupedal locomotion and resting stance probably included palmigrade hand posturing. Their thumbs may have been already well developed as an adaptation for grasping during arboreal climbing. A combination of selection pressures for efficient terrestrial locomotor support and for object manipulation further advanced early hominid hands toward modern human configuration.