Neuromuscular and biomechanical compensation for wing asymmetry in insect hovering flight

Wing damage is common in flying insects and has been studied using a variety of approaches to assess its biomechanical and fitness consequences. Results of these studies range from strong to nil effect among the variety of species, fitness measurements and damage modes studied, suggesting that not all damage modes are equal and that insects may be well adapted to compensate for some types of damage. Here, we examine the biomechanical and neuromuscular means by which flying insects compensate for asymmetric wing damage, which is expected to produce asymmetric flight forces and torques and thus destabilize the animal in addition to reducing its total wing size. We measured the kinematic and neuromuscular responses of hawkmoths (Manduca sexta) hovering in free flight with asymmetrically damaged wings via high-speed videography and extracellular neuromuscular activity recordings. The animals responded to asymmetric wing damage with asymmetric changes to wing stroke amplitude sufficient to restore symmetry in lift production. These asymmetries in stroke amplitude were significantly correlated with bilateral asymmetries in the timing of activation of the dorsal ventral muscle among and within trials. Correspondingly, the magnitude of wing asymmetry was significantly, although non-linearly, correlated with the magnitude of the neuromuscular response among individuals. The strongly non-linear nature of the relationship suggests that active neural compensation for asymmetric wing damage may only be necessary above a threshold (>12% asymmetry in wing second moment of area in this case) below which passive mechanisms may be adequate to maintain flight stability.