Bumblebees actively compensate for the adverse effects of sidewind during visually-guided landings

Abstract

Flying animals often encounter winds during visually guided landings. However, how winds affect their flight control strategy during landing is unknown. Here, we investigated how sidewind affects the landing strategy, sensorimotor control, and landing performance of foraging bumblebees (Bombus terrestris). For this, we trained a hive of bumblebees to forage in a wind tunnel, and used high-speed stereoscopic videography to record 19,421 landing flight maneuvers in six sidewind speeds (0 to 3.4 m s-1), which correspond to winds encountered in nature. Bumblebees landed less often in higher windspeeds, but the landing duration from free flight was not increased by wind. We then tested how bumblebees adjusted their landing control to compensate for the adverse effects of sidewind on landing. This showed that the landing strategy in sidewind was similar to that in still air, but with important adaptations. In the highest windspeeds, more hover phases occurred than during landings in still air. The rising hover frequency did not increase landing duration because bumblebees flew faster in between hover phases. Hence, they negated the adverse effects of increased hovering in high windspeeds. Using control theory, we revealed how bumblebees integrate information from the wind-mediated mechanosensory modality with their vision-based sensorimotor control loop. The proposed multi-sensory flight control system may be commonly used by insects landing in windy conditions and it may inspire the development of landing control strategies onboard man-made flying systems. Summary statementBumblebees foraging in strong sidewinds can still land precisely on artificial flowers, allowing them to be efficient and robust pollinators in these adverse environmental conditions.