Rolling with the flow: bumblebees flying in unsteady wakes.

Our understanding of how variable wind in natural environments affects flying insects is limited because most studies of insect flight are conducted in either smooth flow or still air conditions. Here, we investigate the effects of structured, unsteady flow (the von Karman vortex street behind a cylinder) on the flight performance of bumblebees (Bombus impatiens). Bumblebees are 'all-weather' foragers and thus frequently experience variable aerial conditions, ranging from fully mixed, turbulent flow to unsteady, structured vortices near objects such as branches and stems. We examined how bumblebee flight performance differs in unsteady versus smooth flow, as well as how the orientation of unsteady flow structures affects their flight performance, by filming bumblebees flying in a wind tunnel under various flow conditions. The three-dimensional flight trajectories and orientations of bumblebees were quantified in each of three flow conditions: (1) smooth flow, (2) the unsteady wake of a vertical cylinder (inducing strong lateral disturbances) and (3) the unsteady wake of a horizontal cylinder (inducing strong vertical disturbances). In both unsteady conditions, bumblebees attenuated the disturbances induced by the wind quite effectively, but still experienced significant translational and rotational fluctuations as compared with flight in smooth flow. Bees appeared to be most sensitive to disturbance along the lateral axis, displaying large lateral accelerations, translations and rolling motions in response to both unsteady flow conditions, regardless of orientation. Bees also displayed the greatest agility around the roll axis, initiating voluntary casting maneuvers and correcting for lateral disturbances mainly through roll in all flow conditions. Both unsteady flow conditions reduced the upstream flight speed of bees, suggesting an increased cost of flight in unsteady flow, with potential implications for foraging patterns and colony energetics in natural, variable wind environments.