Free-fall Hoverfly

Mutli-sensory fusion and verticality perception

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.

We have been able to simulate free-fall conditions to find out how swiftly the insects responded to the loss of the sensation of gravity and attempted to fly ((Goulard et al., 2016)). In the dark rarely, if ever, hoverflies began beating their wings in time to rescue themselves from a crash. In presence of a stripy wallpaper, the majority of flies triggered flight and avoided a crash within 150 ms of release. Hoverflies clearly have no gravity sensors – accelerometers – and must be relying on the sensation of air flow to rectify their fall, as well their leg proprioception and vision.

Therefore two questions arise: how is the verticality represented in terms of sensori modlities? How are the various modalities merged to obtain a robust verticality perception?

A first hypothesis is that during the long evolutionary history of insect flight, the brightest part of the visual field has been the sky and the darkest is the ground, and thus it makes a robust indicator of which way is up (see Why flying insects gather at artificial light ). In this paradigm, hoverflies’ flight stabilization strategies were investigated ((Goulard et al., 2018)) here for the first time under two different positions of the light source (overhead and bottom lighting). The crash rates were higher in bottom lighting conditions than with top lighting.

Then, we moved to a new paradigm where hoverflies taking off from a sloping surface have to reorient themselves dorsoventrally and stabilize their body by actively controlling their flapping wings ((Verbe et al., 2020)). We observed for the first time that hoverfly reorientation is entirely achieved within 6 wingbeats (48.8 ms).

Finally, we studied how falling hoverflies use sensory cues to trigger appropriate roll righting behavior ((Verbe et al., 2023)). Before being released in a free fall, flies were placed upside-down with their legs contacting the substrate. The prior leg proprioceptive information about their initial orientation sufficed for the flies to right themselves properly. Surprisingly, in one of the experimental conditions tested, hoverflies flew upside-down while still actively flapping their wings.

However, the way hoverflies merge the sensory cues remains an open question. We are moving now to a new experimental setup that will place the fly in a free-fall condition without any prior information provided by the leg proprioception.

Fly reorientation captured by a high-speed camera filming at 1600 images per second. Photo credit: A. Verbe

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Hoverflies were exposed during these experiments to three different visual scenes: a completely dark environment, a uniformly illuminated white box, and a box in which two sides were lined with a regular pattern of black and white stripes. Typical trajectories of free-falling hoverflies exposed to the three visual conditions are presented (yellow and blue lines). Dotted green trajectories correspond to wing flapping resulting in a successful flight, i.e. in no crashing of the flies onto the floor, whereas dotted red curves correspond to crashes due to late wingbeat onset or no wingbeats at all. Hoverflies were said to have crashed when they touched the floor, as indicated by red asterisks (From ((Goulard et al., 2016)).

References

2023

  1. Sensory fusion in the hoverfly righting reflex
    Anna Verbe, Dominique Martinez, and Stéphane Viollet
    Scientific Reports, 2023

2020

  1. How do hoverflies use their righting reflex?
    Anna Verbe, Léandre P Varennes, Jean-Louis Vercher, and 1 more author
    Journal of Experimental Biology, 2020

2018

  1. Role of the light source position in freely falling hoverflies’ stabilization performances
    Roman Goulard, Anna Verbe, Jean-Louis Vercher, and 1 more author
    Biology letters, 2018

2016

  1. To crash or not to crash: how do hoverflies cope with free-fall situations and weightlessness?
    Roman Goulard, Jean-Louis Vercher, and Stéphane Viollet
    Journal of Experimental Biology, 2016