Biology and physics of locust flight IV. Notes on sensory mechanisms in locust flight

The wing stroke of locusts is remarkably constant and independent of external conditions. Is this rigid rhythmicity due to a rhythmicity of the central nervous system or is it determined by peripheral factors? The flight behaviour of the desert locust (Schistocera gregaria ) was studied under various experimental conditions in order to find which external factors can initiate, maintain or alter the wing movements, excluding reactions which depend upon higher nervous centres. The ‘tarsal reflex’ and the response seen when the aerodynamic sense organ on the head is stimulated (Weis-Fogh 1949, 1950) were reinvestigated in order to relate them to two hitherto unknown reactions: the maintenance of flapping when the wings are exposed to wind and the regulation of the lift when the body angle ( = angle of pitch) is changed during forward flight. Both depend on receptors whose nature is still unknown. Inhibition. As in most other insects, the flight of a locust cannot be started when the legs, or only part of one leg, have contact with a rigid body; flight stops when such contact is regained. Amputation of the legs abolishes these reactions, showing that some leg proprioceptors inhibit flight. Initiation. A suspended locust can be induced to fly in three ways. (1) By application of a sufficiently strong stimulus which normally provokes escape reactions; the flight lasts only a few seconds. Adaptation is generally quick. (2) By sudden removal of the support for the legs (‘ tarsal reflex’ although not confined to the tarsi). The flight lasts 5 s on average, corresponding to one hundred wing strokes. There is practically no adaptation. (3) By blowing upon the wind-sensitive hairs on the head. The wind must exceed 2 m/s, but its direction is of little importance. Since the static bending has no effect, the adequate stimulus seems to be minute vibrations of the hairs. The flight lasts as long as the wind blows and the hairs are therefore also involved in the maintenance of flight. When the locust has stopped, the legs begin to flutter, and eventually remain still, but normally flight is not resumed unless one of the above stimuli is applied. Maintenance. Two receptor systems are involved. (1) The wind-sensitive hairs on the head. In a wind they emit impulses irrespectively of whether the locust has any chance of flapping its wings or not. ‘Wind on the head’ is therefore an extrinsic flight stimulus. The flight posture is never complete. (2) A hitherto unknown receptor system in the pterothorax which was studied in insects whose supra-oesophageal ganglia were cauterized (‘decerebrate’). It maintains the movements when the wings oscillate in a wind but cannot initiate them; the adequate stimulus is the rhythmically changing wind pressure on the wings. ‘Wind on the wings’ is therefore an intrinsic flight stimulus. When the average lift exceeds half the body weight, flight continues in complete flight posture but stops when the lift approaches zero. The experiments indicate that the stimulation ceases when the lift becomes negative during the upstroke. The receptors are unknown; it is suggested that they are situated at the wing hinge. The locust does not adapt to either of these stimuli and invariably stops a few seconds after they have ceased. Control of lift. The locust tends to keep the lift constant during a given performance. This observation, together with the constancy of most stroke parameters, made it possible to investigate the mechanism involved. The method was to make the insect fly steadily against a horizontal wind and then alter the inclination to the wind (= the body angle) at regular intervals. The data permitted an estimate of the mean change in wing twisting Δθ. Δθ increased (wings pronated) by 15 ± 3° when the body angle was increased from 0 to 15°. This is the main factor in the control of lift. The discussion shows that this presupposes a system of lift-sensitive receptors (probably campaniform sensilla at the wing hinge). If present in other insects, the homoeostatic character of the wing stroke of Drosophila (Chadwick 1953) may therefore be caused by a nervous mechanism and need not be a consequence of the energetics of flight. Central rhythm. It is concluded that the central nervous system ( does not initiate flight rhythm de novo; (b) does neither determine the stroke frequency nor the strength of the contractions of the controller-depressor muscles; ( c) may control the phasing of the contractions, although a simpler hypothesis is advanced; (d) may control the indirect flight muscles but only as far as to produce stimuli of constant (maximum? ) strength.