Muscle power output reflects elevated viscosity in the propulsion system of flying miniature wasps

Abstract

Air viscosity compromises aerodynamic lift production in the smallest flying insects, leading to increased flight costs. Miniature insects thus utilize both lift and drag for weight support but the exact energetic costs of wing flapping at low Reynolds number are widely unexplored. We estimated flight power in the miniature wasp Eretmocerus mundus. Wing kinematics was three-dimensionally reconstructed using high-speed video and computational fluid dynamics simulated air flows, aerodynamic forces and moments. We found an asymmetrical crescent-shaped wingtip trajectory with the upstroke posterior to the downstroke path. This fore-aft distance increases with increasing horizontal flight velocity, maintaining the wings backwards rowing motion needed for drag-based propulsion. Although the wings lift-to-drag ratio is below unity, lift is the predominant force responsible for weight support and forward thrust. Elevated drag leads to mass-specific mechanical power output of 118{+/-}9.0 Wkg-1 flight muscle, which exceeds most power estimates reported for other insects, birds and bats. The elevated energetic costs for flight may have fostered the development of bristled wings in miniature insects. Altogether, our study of wingbeat control and flight costs in a miniature insect extends the scope of flight mechanisms to the smallest flying animals revealing limits of miniaturization during the evolution of flight.