The stimuli evoking the aerial-righting posture of falling pea aphids.

Some wingless insects possess aerial righting reflexes, suggesting that adaptation for controlling body orientation while falling through air could have preceded flight. When threatened by natural enemies, wingless pea aphids (Acyrthosiphon pisum) may drop off their host plant and assume a stereotypic posture that rotates them in midair to land on their feet. The sensory information triggering aphids to assume this posture has so far been unknown. We subjected aphids to a series of tests, isolating the sensory cues experienced during free-fall. Falling aphids assumed the righting posture and landed upright irrespective of whether the experiments were carried out in the light or in complete darkness. Detachment of the tarsi from the substrate triggered the aphids to assume the posture rapidly, but only for a brief period. Rotation (mainly roll and yaw) of the body in air, in the light, caused aphids to assume the posture and remain in it throughout rotation. In contrast, aphids rotated in the dark did not respond. Acceleration associated with falling or airflow over the body per se did not trigger the posture. However, sensing motion relative to air heightened the aphids' responsiveness to rotation in the light. These results suggest that the righting posture of aphids is triggered by a tarsal reflex, but, once the aphid is airborne, vision and a sense of motion relative to air can augment the response. Hence, aerial righting in a wingless insect could have emerged as a basic tarsal response and developed further to include secondary sensory cues typical of falling.