Active control of free flight manoeuvres in a hawkmoth, Agrius convolvuli

Abstract

SUMMARYBy combining optical triangulation with the comb-fringe technique and dual-channel telemetry, wing kinematics and body attitudes accompanying muscle activities of free-flying male hawkmoths were recorded synchronously when they performed flight manoeuvres elicited by a female sex pheromone. The results indicate that the wing leading edge angular position at the ventral stroke reversal, which can be decomposed by two orthogonal angular parameters (a flapping angle and a deviation angle), is well controllable. Two specific flight muscles, the dorsal-ventral muscle (DVM, indirect muscle, a wing elevator) and the third axillary muscle (3AXM, direct muscle, a wing retractor), can modulate the flapping angle and the deviation angle, respectively, by means of regulating the firing timing of muscle activities. The firing timing can be expressed by the firing latency absolutely, which is just before the timing of ventral stroke reversal. The results illustrate that lengthening the firing latency of the DVM and of the 3AXM can increase the flapping angle and the deviation angle, respectively, which both strengthen the downstroke at the ventral stroke reversal. The relationship of bilateral asymmetry shows that the bilateral differences in the firing latency of the DVM and of the 3AXM will cause bilateral differences in the wing position, which accompany the variations of yaw and roll angles in time course. This implies the contribution of the two muscles to active steering controls during turning or banking, though the DVM being an indirect muscle was generally treated as a power generator. Finally, the relationship between the pitch angle and the 3AXM latency, deduced from the relationships between the pitch angle and the deviation angle and between the deviation angle and the 3AXM latency, shows that lengthening the 3AXM latency can increase the pitch angle at the ventral stroke reversal by moving the wing tip far away from the centre of gravity of the body, which indicates a functional role of the 3AXM in active pitching control.

Flexibility and control of thorax deformation during hawkmoth flight

“…In particular, the DVMs, located near the wing hinges, would effectively deform the lateral scutum and control the wings. Recent studies have reported the contribution of the powerproducing IFMs to lateral control in both the synchronous [4][5][6] and the asynchronous types [10]. The multiple functions of the IFMs provide flexibility for flight control and will be further elucidated by a combination of morphometry, physiology and computational structural analysis.…”

“…Therefore, Lepidoptera can use the neurogenic controllability of the IFMs for finer control of wing kinematics, while at the same time gaining mechanical benefits. Previous studies of hawkmoths have shown that phase asymmetry in the activity of bilateral IFMs can generate asymmetry in the power and kinematics of the wing beat [4][5][6]. To achieve such asymmetrical control, the single structure of the mesonotum can be locally deformed and transmit asymmetrical power to the wings.…”

Neuromuscular control of free-flight yaw turns in the hawkmothManduca sexta

“…We correlate dorsal longitudinal muscle (DLM; wing depressor muscle) and dorsal ventral muscle (DVM; wing elevator muscle) bilateral activation phase differences with yaw velocity and yaw acceleration. Though the DLM and DVM have historically been categorized as 'power' muscles (Pringle, 1957), there is growing evidence (Sponberg and Daniel, 2010;Tu and Daniel, 2004;Wang et al, 2008) that flying insects with synchronous flight muscles (e.g. moths) may, like vertebrate flyers (Hedrick and Biewener, 2007b), modulate main flight muscle power output during manoeuvres.…”

Studying the Neural Basis of Adaptive Locomotor Behavior in Insects

“…This can either be avoided by using implantable electrodes and then having the animal move on a long tether (i.e. Clarac et al, 1987;Duch & Pflüger, 1995;Böhm et al, 1997;Gruhn & Rathmayer, 2002) or by transmitting the data using telemetric devices (Kutsch et al, 1993;Fischer et al, 1996;Tsuchida et al 2004;Hama et al, 2007;Wang et al, 2008). Both of these elegant methods, which are successfully used in larger arthropods, often prove difficult to apply in smaller walking insects which either easily get entangled in the long tether or are hindered by the weight of the telemetric device and its batteries.…”