Beyond the vertebrates: achieving maximum power during flight in insects and hummingbirds

Hummingbirds and insects are clearly extreme aerobic athletes. Hovering hummingbirds and insects exhibit the highest mass-specific metabolic rates found in vertebrates and invertebrates, respectively. Both groups of fliers have high mitochondrial volume densities in their locomotor muscles, but these do not exceed 35-40% of the fiber volume, presumably from a need to conserve myofibrils for force generation. A possible adaptation to this constraint is the observed greater packing of the inner mitochondrial membranes than occurs in mammalian mitochondria. Both hummingbirds and insects show higher rates of oxygen consumption per unit volume of mitochondria than do mammals. Additionally, volume-specific mitochondrial oxygen consumption in insects increases as body size decreases, unlike the size-independent pattern in mammals. Aerodynamic analysis of power output during hovering flight strongly suggests that both insects and hummingbirds operate with considerable elastic storage of kinetic energy, thereby decreasing their inertial power requirements. Both groups appear to hover with muscle power output close to 100 W kg-1. Muscle efficiency in hummingbirds is near 10%; in insects, muscle efficiency varies with body size, but at similarly low values. Scaling of efficiency with body size has also been reported in terrestrial mammals, suggesting a possible common mechanism. Both groups of hovering fliers can markedly increase their metabolic power inputs and mechanical power outputs above those required for basic hovering flight. These elite aerial athletes offer considerable insight into the constraints and demands on animal design for maximal aerobic capacity. Additionally, the similarities shown between the different phyla suggest the existence of common mechanisms and limitations in metabolic and mechanical performance. Insects in particular offer a number of advantages in pursuing questions such as the cause of the allometric scaling of muscle efficiency; this scaling can be examined within families, genera, or species with the additional benefit that insect muscles also perform well in vitro.