To crash or not to crash: how do hoverflies cope with free-fall situations and weightlessness?

Abstract

ABSTRACT Insects’ aptitude to perform hovering, automatic landing and tracking tasks involves accurately controlling their head and body roll and pitch movements, but how this attitude control depends on an internal estimation of gravity orientation is still an open question. Gravity perception in flying insects has mainly been studied in terms of grounded animals' tactile orientation responses, but it has not yet been established whether hoverflies use gravity perception cues to detect a nearly weightless state at an early stage. Ground-based microgravity simulators provide biologists with useful tools for studying the effects of changes in gravity. However, in view of the cost and the complexity of these set-ups, an alternative Earth-based free-fall procedure was developed with which flying insects can be briefly exposed to microgravity under various visual conditions. Hoverflies frequently initiated wingbeats in response to an imposed free fall in all the conditions tested, but managed to avoid crashing only in variably structured visual environments, and only episodically in darkness. Our results reveal that the crash-avoidance performance of these insects in various visual environments suggests the existence of a multisensory control system based mainly on vision rather than gravity perception.