Fibre type composition in the lumbar perivertebral muscles of primates: implications for the evolution of orthogrady in hominoids.

The axial musculoskeletal system is important for the static and dynamic control of the body during both locomotor and non-locomotor behaviour. As a consequence, major evolutionary changes in the positional habits of a species are reflected by morpho-functional adaptations of the axial system. Because of the remarkable phenotypic plasticity of muscle tissue, a close relationship exists between muscle morphology and function. One way to explore major evolutionary transitions in muscle function is therefore by comparative analysis of fibre type composition. In this study, the three-dimensional distribution of slow and fast muscle fibres was analysed in the lumbar perivertebral muscles of two lemuriform (mouse lemur, brown lemur) and four hominoid primate species (white-handed gibbon, orangutan, bonobo, chimpanzee) in order to develop a plausible scenario for the evolution of the contractile properties of the axial muscles in hominoids and to discern possible changes in muscle physiology that were associated with the evolution of orthogrady. Similar to all previously studied quadrupedal mammals, the lemuriform primates in this study exhibited a morpho-functional dichotomy between deep slow contracting local stabilizer muscles and superficial fast contracting global mobilizers and stabilizers and thus retained the fibre distribution pattern typical for quadrupedal non-primates. In contrast, the hominoid primates showed no regionalization of the fibre types, similar to previous observations in Homo. We suggest that this homogeneous fibre composition is associated with the high functional versatility of the axial musculature that was brought about by the evolution of orthograde behaviours and reflects the broad range of mechanical demands acting on the trunk in orthograde hominoids. Because orthogrady is a derived character of euhominoids, the uniform fibre type distribution is hypothesized to coincide with the evolution of orthograde behaviours.

The biomechanics of leaping in gibbons.

Gibbons are skilled brachiators but they are also highly capable leapers, crossing distances in excess of 10 m in the wild. Despite this impressive performance capability, no detailed biomechanical studies of leaping in gibbons have been undertaken to date. We measured ground reaction forces and derived kinematic parameters from high-speed videos during gibbon leaps in a captive zoo environment. We identified four distinct leap types defined by the number of feet used during take-off and the orientation of the trunk, orthograde single-footed, orthograde two-footed, orthograde squat, and pronograde single-footed leaps. The center of mass trajectories of three of the four leap types were broadly similar, with the pronograde single-footed leaps exhibiting less vertical displacement of the center of mass than the other three types. Mechanical energy at take-off was similar in all four leap types. The ratio of kinetic energy to mechanical energy was highest in pronograde single-footed leaps and similar in the other three leap types. The highest mechanical work and power were generated during orthograde squat leaps. Take-off angle decreased with take-off velocity and the hind limbs showed a proximal to distal extension sequence during take-off. In the forelimbs, the shoulder joints were always flexed at take-off, while the kinematics of the distal joints (elbow and wrist joints) were variable between leaps. It is possible that gibbons may utilize more metabolically expensive orthograde squat leaps when a safe landing is uncertain, while more rapid (less expensive) pronograde single-footed leaps might be used during bouts of rapid locomotion when a safe landing is more certain.

Morphological analysis of the hindlimb in apes and humans. II. Moment arms.

Flexion/extension moment arms were obtained for the major muscles crossing the hip, knee and ankle joints in the orang-utan, gibbon, gorilla (Eastern and Western lowland) and bonobo. Moment arms varied with joint motion and were generally longer in proximal limb muscles than distal limb muscles. The shape of the moment arm curves (i.e. the plots of moment arm against joint angle) differed in different hindlimb muscles and in the same muscle in different subjects (both in the same and in different ape species). Most moment arms increased with increasing joint flexion, a finding which may be understood in the context of the employment of flexed postures by most non-human apes (except orang-utans) during both terrestrial and arboreal locomotion. When compared with humans, non-human great apes tended to have muscles better designed for moving the joints through large ranges. This was particularly true of the pedal digital flexors in orang-utans. In gibbons, the only lesser ape studied here, many of the moment arms measured were relatively short compared with those of great apes. This study was performed on a small sample of apes and thus differences noted here warrant further investigation in larger populations.

Morphological analysis of the hindlimb in apes and humans. I. Muscle architecture.

We present quantitative data on the hindlimb musculature of Pan paniscus, Gorilla gorilla gorilla, Gorilla gorilla graueri, Pongo pygmaeus abelii and Hylobates lar and discuss the findings in relation to the locomotor habits of each. Muscle mass and fascicle length data were obtained for all major hindlimb muscles. Physiological cross-sectional area (PCSA) was estimated. Data were normalized assuming geometric similarity to allow for comparison of animals of different size/species. Muscle mass scaled closely to (body mass)(1.0) and fascicle length scaled closely to (body mass)(0.3) in most species. However, human hindlimb muscles were heavy and had short fascicles per unit body mass when compared with non-human apes. Gibbon hindlimb anatomy shared some features with human hindlimbs that were not observed in the non-human great apes: limb circumferences tapered from proximal-to-distal, fascicle lengths were short per unit body mass and tendons were relatively long. Non-human great ape hindlimb muscles were, by contrast, characterized by long fascicles arranged in parallel, with little/no tendon of insertion. Such an arrangement of muscle architecture would be useful for locomotion in a three dimensionally complex arboreal environment.

Locomotion in bonobos (Pan paniscus): differences and similarities between bipedal and quadrupedal terrestrial walking, and a comparison with other locomotor modes.

One of the great ongoing debates in palaeo-anthropology is when, and how, hominids acquired habitual bipedal locomotion. The newly adopted bipedal gait and the ancestral quadrupedal gait are most often considered as very distinct, with each habitual locomotor mode showing corresponding anatomical adaptations. Bonobos (Pan paniscus), along with common chimpanzees (P. troglodytes), are the closest living relatives to humans and their locomotion is valuable for comparison with other primates, and to gain an insight in the acquisition of human bipedalism. Bonobos are habitual quadrupeds, but they also engage in bipedal locomotion, both on terrestrial and in arboreal substrates. In terms of kinematics and dynamics, the contrast between bipedal and quadrupedal walking seems to be more subtle than one might expect. Apart from the trunk being approximately 37 degrees more erect during bipedal locomotion, the leg movements are rather similar. Apart from the heel, plantar pressure distributions show subtle differences between bipedal and quadrupedal locomotion. Regardless, variability is high, and various intermediate forms of locomotion (e.g. tripedal walking) exist both in captivity and in the wild. Moreover, there is overlap between the characteristics of walking and other locomotor modes, as we show with new data of walking on an inclined pole and of vertical squat jumps. We suggest that there is great overlap between the many locomotor modes in bonobos, and that the required polyvalence is reflected in their anatomy. This may hamper the development of one highly specialized gait (i.e. bipedalism), which would constrain performance of the other types of locomotion.

Mechanical properties of red and white swimming muscles as a function of the position along the body of the eel Anguilla anguilla.

The way in which muscles power steady swimming depends on a number of factors, including fibre type and recruitment, muscle strain, stimulation pattern and intensity, and the intrinsic mechanical properties of the muscle fibres. For a number of undulatory swimming fish species, in vivo studies have shown that muscles at different positions along the body are stimulated during different phases of the strain cycle. Moreover, some intrinsic contractile properties of the muscles have been found to vary according to their position along the body. We report the first results on the mechanical properties of the red and white muscles of an anguilliform swimmer, Anguilla anguilla. Small preparations (0.147-1.335 mg dry mass) were dissected from positions at fractions of 0.2, 0.4, 0.6 and 0.8 of total body length (BL). We determined the time to 50% and 100% peak force and from the last stimulus to 50% relaxation for isometric contractions; we measured the sarcomere lengths that coincided with in situ resting length. None of these quantities varied significantly with the longitudinal position from which the fibres were taken. We also measured power and work output during contractions under conditions approximating those used in vivo (cycle frequency, 1Hz; strain amplitude, +/- 10%L(0), where L(0) is the length giving maximum isometric force). During these experiments, work output was affected by stimulation phase, but did not depend on the longitudinal position in the body from which the muscles were taken. Our results indicate that red and white eel muscles have uniform properties along the body. In this respect, they differ from the muscle of most non-anguilliforms, in which muscle kinetics varies in a systematic way along the body. Uniform properties may be beneficial for anguilliform swimmers, in which the amplitude of the travelling wave can be pronounced over the entire body length.

Speed modulation in swimming frogs.

Swimming movements of 7 European green frogs (Rana esculenta) were studied, starting from the detailed analysis of the speed and timing of the propulsive, glide, and recovery phases of their intermittent swimming behavior. First, the authors identified the spatiotemporal factors used by the frogs to modulate their swimming behavior. None of the gait variables correlated strongly with average swimming speed, and no significant correlations were found between variables belonging to different phases. There did not seem to be an obvious control strategy. Instantaneous speeds at the transition of the different phases all increased significantly with average speed, however. The strong correlation between maximal speed at the end of propulsion and the speed averaged over a cycle might reflect the dominance of the propulsive phase in the determination of the overall swimming speed. The modulation of swimming speed thus seemed largely comparable with the regulation of jumping distance. That finding was confirmed in a mathematical model, in which the positive correlations between both glide and recovery speeds, on the one hand, and average speed, on the other, were shown to be only mathematical consequences of the strong impact of the propulsive phase on overall swimming performance. That finding suggests that the correlations did not result from an active control strategy.

A kinematic comparison of forward and backward swimming in the eel anguilla anguilla

In addition to forward undulatory swimming, eels (and some other elongated swimmers) can swim backwards in a similar way. We compared the kinematics (wave speed, cycle frequency, amplitude, local bending and estimated muscle strain) of forward and backward swimming in the European eel Anguilla anguilla. Both swimming modes are characterised by a wave of undulation that travels over the body in the direction opposite to that of swimming. We observe two major kinematic differences. First, the slope of wave frequency against swimming speed is significantly higher for backward than for forward swimming. Second, the amplitude profile along the body of the propulsive wave differs greatly. During forward swimming, the yaw at the head is minimal and the amplitude of the propulsive wave increases to approximately 15 % (left-to-right) of total body length towards the tail tip. During backward swimming, the amplitude profile is rather uniform along the body (with values similar to the tail-tip amplitude during forward swimming), resulting in considerable lateral head oscillation. Strikingly, the head remains approximately parallel to the swimming direction, which presumably enhances visual and acoustico-lateral perception. Furthermore, muscle strain is much higher in the rostral part of the body during backward swimming than during forward swimming. Values for stride length and propeller efficiency suggest that backward undulatory swimming is mechanically less efficient than forward swimming. We suggest that the typical anguilliform body shape is an important feature that allows these animals to swim backwards using an undulatory mechanism that resembles the forward undulatory swimming mechanism. Most other fishes, if able to swim backwards at all, do so using fin oscillations or undulations.