Flight in the dark: different responses to darkness in flying insects

Vision-based stabilization is crucial for flying animals, and among these, flying insects provide a range of experimental systems for studying vision-related locomotion resilience and sensory integration; for example, under low-light conditions. Behavioral experiments on flying insects can provide a top-down approach for setting limits to their sensory capabilities in such conditions, yet the flight kinematics of insects with minimal visual cues has received little attention. Here, we compared the flight of fruit flies, mosquitoes and honey bees under continuous low light and upon sudden mid-flight darkness. While honey bees typically do not fly in the dark and upon a sudden mid-flight darkness crash within 100 ms, fruit flies and mosquitoes can fly under continuous low-light levels and upon sudden darkness exhibit a well-defined response maneuver. The sequence consists of a visual-motor delay, increasing wingbeat frequency, pitching-up, slowing down and changing course, all within a 250 ms observation time. A similar response was also observed under a sudden transition to partial darkness, which better mimics naturally occurring conditions. The stark differences between the honey bees' and dipterans' responses can be attributed to the dipterans' higher light sensitivity and to the fact that they have halteres - gyroscopic organs that enable them to measure their body attitude regardless of vision. Such free-flight experiments could be combined with further electrophysiological characterization of insect light sensitivity and adaptation to better understand the dynamic role of vision and sensory fusion in flight.