The Control of Mechanical Power in Insect Flight

SYNOPSIS. The cost of locomotion is rarely constant, but rathervaries as an animal changes speed and direction. Ultimately,the locomotory muscles of an animal must compensate for thesechanging requirements by varying the amount of mechanical powerthat they produce. In this paper, we consider the mechanismsby which the mechanical power generated by the asynchronousflight muscles of the fruit fly, Drosophila melanogaster, isregulated to match the changing requirements during flight controlbehaviors. Our data come from individual flies flown in a flightarena under conditions in which stroke kinematics, total metaboliccost, and flight force are simultaneously measured. In orderto increase force production, flies must increase wing beatfrequency and wing stroke amplitude. Theory predicts that thesekinematics changes should result in a roughly cubic increasein the mechanical power requirements for flight. However, themechanical energy generated by muscle should increase only linearlywith stroke amplitude and frequency. This discrepancy impliesthat flight muscles must either recruit myofibrils or increaseactivation in order to generate sufficient mechanical powerto sustain elevated force production. By comparing respirometricallymeasured total metabolic power with kinematically estimatedmechanical power, we have calculated that the stress in theflight muscles of Drosophila must increase by 50% to accommodatea doubling of flight force. Electrophysiological evidence suggeststhat this change in stress may be accomplished by an increasedneural drive to the asynchronous muscles, which in turn mayact to recruit additional cross bridges through an increasein cytosolic calcium.