Limitations of rotational manoeuvrability in insects and hummingbirds: evaluating the effects of neuro-biomechanical delays and muscle mechanical power

Abstract

Flying animals ranging in size from fruit flies to hummingbirds are nimble fliers with remarkable rotational manoeuvrability. The degrees of manoeuvrability among these animals, however, are noticeably diverse and do not simply follow scaling rules of flight dynamics or muscle power capacity. As all manoeuvres emerge from the complex interactions of neural, physiological and biomechanical processes of an animal's flight control system, these processes give rise to multiple limiting factors that dictate the maximal manoeuvrability attainable by an animal. Here using functional models of an animal's flight control system, we investigate the effects of three such limiting factors, including neural and biomechanical (from limited flapping frequency) delays and muscle mechanical power, for two insect species and two hummingbird species, undergoing roll, pitch and yaw rotations. The results show that for animals with similar degree of manoeuvrability, for example, fruit flies and hummingbirds, the underlying limiting factors are different, as the manoeuvrability of fruit flies is only limited by neural delays and that of hummingbirds could be limited by all three factors. In addition, the manoeuvrability also appears to be the highest about the roll axis as it requires the least muscle mechanical power and can tolerate the largest neural delays.