Muscle Action During Locomotion: A Comparative Perspective

This essay explores how the properties of striated muscles are matched to the tasks they perform during running, swimming and flying. During exercise the major locomotory muscles undergo alternate cycles of lengthening and shortening. Force development is greatly influenced by the timing of stimulation in relation to the length-change cycle and by the nature of elastic structures connecting the muscle fibres to the skeleton. The storage and recovery of elastic strain energy by the tendons (apodema in insects) results in a considerable saving of metabolic energy. Strain is independent of locomotory frequency, body size and muscle temperature. In contrast, the frequency of cycles, and hence strain rate, generally increases with speed and is inversely proportional to body size. The maximum isometric stress (P₀) striated muscles can exert is rather similar. During steady running or hopping in mammals the peak muscle stress is around one-third of P_0. Behaviours such as vertical jumping impose higher stresses requiring disproportionately larger muscles and tendons, which may limit the storage of elastic strain energy. Muscles of small animals consume significantly more energy per gram than do those of large ones. This may be because they need to activate and deactivate their muscles at a higher rate to move at an equivalent speed. When differences in force production are normalised, by multiplying the energy consumed per stride by stride frequency, similar values for the mass-specific cost of locomotion are found in animals with different leg architectures, numbers of legs, skeletal type, body sizes and muscle temperatures.

The power output of isolated muscle fibres can be measured by imposing cyclical strain fluctuations and stimulating briefly during each cycle to approximate normal operating conditions in vivo. This approach yields values for maximum power output of 76–130 W kg⁻¹ for synchronous insect flight muscles at temperatures and wingbeat frequencies appropriate for flight. Frog sartorius muscle produces 20 W kg⁻¹ at the hopping frequency used during escapes at 20°C. The strain rates and deactivation rates of muscle fibres are optimised to produce maximum power over a particular range of locomotory frequencies. In vertebrates this necessitates the sequential recruitment of muscle fibre types with faster maximum strain rates and shorter contraction times as speed increases. Estimates of overall muscle efficiency during locomotion in insects, fish and small mammals are mostly in the range 6–20%.