The Control of Mechanical Power in Insect Flight

SYNOPSIS. The cost of locomotion is rarely constant, but rather varies as an animal changes speed and direction. Ultimately, the locomotory muscles of an animal must compensate for these changing requirements by varying the amount of mechanical power that they produce. In this paper, we consider the mechanisms by which the mechanical power generated by the asynchronous flight muscles of the fruit fly, Drosophila melanogaster, is regulated to match the changing requirements during flight control behaviors. Our data come from individual flies flown in a flight arena under conditions in which stroke kinematics, total metabolic cost, and flight force are simultaneously measured. In order to increase force production, flies must increase wing beat frequency and wing stroke amplitude. Theory predicts that these kinematics changes should result in a roughly cubic increase in the mechanical power requirements for flight. However, the mechanical energy generated by muscle should increase only linearly with stroke amplitude and frequency. This discrepancy implies that flight muscles must either recruit myofibrils or increase activation in order to generate sufficient mechanical power to sustain elevated force production. By comparing respirometrically measured total metabolic power with kinematically estimated mechanical power, we have calculated that the stress in the flight muscles of Drosophila must increase by 50% to accommodate a doubling of flight force. Electrophysiological evidence suggests that this change in stress may be accomplished by an increased neural drive to the asynchronous muscles, which in turn may act to recruit additional cross bridges through an increase in cytosolic calcium.