The scaling of myofibrillar actomyosin ATPase activity in apid bee flight muscle in relation to hovering flight energetics

Abstract

For all types of locomotion, the overall efficiency with which chemical energy is converted into mechanical work increases with increasing body size. In order to gain insight into the determinants of the scaling of overall efficiency, we measured the scaling of the rate of ATP utilisation during cyclical contractions using glycerinated fibres from the dorsolongitudinal flight muscle of several species of apid bees, covering a ninefold range in body mass. The efficiency of ATP utilisation by the crossbridges is one of the stages that determines the overall efficiency of locomotion. The mechanochemical coefficient was calculated from the ratio of the net power output to the rate of ATP hydrolysis and ranged from 6.5 to 9.7 kJ mol-1 ATP. The corresponding gross myofibrillar efficiency was 15-23%, increasing concomitantly with body mass (Mb) and decreasing with increasing wingbeat frequency (n) and scaling as Mb0.184 and n-1.168 in bumblebees and as Mb0.153 and n-0.482 in euglossine bees. Overall efficiency of hovering in bumblebees and euglossine bees was calculated using previously published metabolic power data and revised estimates of the mechanical power output to take into account the drag due to the leading edge vortex that has not been included in previous models. The scaling of overall efficiency of hovering flight in apid bees was not as pronounced as the scaling of myofibrillar efficiency. Therefore the scaling of myofibrillar efficiency with body mass (or frequency) only explained part of the scaling of overall efficiency, and it is likely that the efficiency of other steps in the transduction of chemical energy into mechanical work (e.g. the efficiency of mitochondrial oxidative recovery) may also scale with body mass.