The significance of spiracle conductance and spatial arrangement for flight muscle function and aerodynamic performance in flyingDrosophila

Abstract

During elevated locomotor activity such as flight, Drosophila satisfies its increased respiratory demands by increasing the total spiracle opening area of the tracheal gas exchange system. It has been assumed that in a diffusion-based system, each spiracle contributes to oxygen flux into and carbon dioxide flux out of the tracheal system according to the size of its opening. We evaluated this hypothesis by determining how a reduction in size and interference with the spatial distribution of gas exchange areas impair flight muscle function and aerodynamic force production in the small fruit fly Drosophila melanogaster. This was done by selectively blocking thoracic spiracles of tethered flies flying inside a flight simulator. Flow-through respirometry and simultaneous measurements of flight force production and wing kinematics revealed a negligible functional safety margin for respiration. Maximum locomotor performance was only achieved by unmanipulated flies, supporting the general assumption that at the animal's maximum locomotor capacity, maximum spiracle opening area matches respiratory need. The maximum total buffer capacity for carbon dioxide in Drosophila amounts to approximately 33.5 mul g(-1) body mass, estimated from the temporal integral of carbon dioxide release rate during the resting period after flight. By comparing flight variables in unmanipulated and 'spiracle-blocked' flies at comparable flight forces, we found that (i) stroke amplitude, stroke frequency and the chemo-mechanical conversion efficiency of the indirect flight musculature were broadly independent of the arrangement of spiracle conductance, while (ii) muscle mechanical power significantly increased, and (iii) mean lift coefficient and aerodynamic efficiency significantly decreased up to approximately 50% with an increasing number of blocked spiracles. The data suggest that Drosophila apparently maximizes the total efficiency of its locomotor system for flight by allowing oxygen delivery to the flight musculature through multiple spiracles of the thorax.