Foraging in an unsteady world: bumblebee flight performance in field-realistic turbulence

Abstract

Natural environments are characterized by variable wind that can pose significant challenges for flying animals and robots. However, our understanding of the flow conditions that animals experience outdoors and how these impact flight performance remains limited. Here, we combine laboratory and field experiments to characterize wind conditions encountered by foraging bumblebees in outdoor environments and test the effects of these conditions on flight. We used radio-frequency tags to track foraging activity of uniquely identified bumblebee (Bombus impatiens) workers, while simultaneously recording local wind flows. Despite being subjected to a wide range of speeds and turbulence intensities, we find that bees do not avoid foraging in windy conditions. We then examined the impacts of turbulence on bumblebee flight in a wind tunnel. Rolling instabilities increased in turbulence, but only at higher wind speeds. Bees displayed higher mean wingbeat frequency and stroke amplitude in these conditions, as well as increased asymmetry in stroke amplitude-suggesting that bees employ an array of active responses to enable flight in turbulence, which may increase the energetic cost of flight. Our results provide the first direct evidence that moderate, environmentally relevant turbulence affects insect flight performance, and suggest that flying insects use diverse mechanisms to cope with these instabilities.

Impact of turbulence on flying insects in tethered and free flight: High-resolution numerical experiments

“…This particular intermediate value of I does not require a large number of flow realizations for any tested value of Λ, which allows keeping the computational cost within acceptable limits. Furthermore, field experiments [11] show a large flight activity of bumblebees for this value of I. Fig.…”

“…Vortex shedding in von Kármán wakes, however, differs from turbulence since, at moderate Reynolds numbers, vortices are shed periodically in time and the flow has strong spatial correlations. Few numerical [18] and experimental [10,11] studies addressed flapping flight in turbulent flow and estimated flow conditions at body and wings. In heavy turbulence, for example, bumblebees are highly prone to changes in roll stability and crash if roll velocity exceeds a maximum value [10].High maneuverability in flight is likely key in coping with turbulence, at the cost of low stability [26,27].…”

Insect and insect-inspired aerodynamics: unsteadiness, structural mechanics and flight control

“…However, recent efforts have begun to shed light on turbulence-mitigation strategies used by biological fliers [30], such as the mechanisms used by bumblebees to increase stability. One example found that bumblebees respond to turbulence with changes in wing kinematics that are both static (as in altered mean values) and dynamic (stroke by stroke) [31]. …”

Wind drives temporal variation in pollinator visitation in a fragmented tropical forest

“…Wind affects macroecological patterns of insect dispersal and migration [6,7]. Mean wind flow [8] and fluctuations (i.e., turbulence) pose biomechanical challenges [9][10][11][12][13] that push maneuverability limits in flying insects [14] and may impose energetic costs on flight [15]. The mechanical and physiological challenges posed by wind may have important effects on their interactions with plants, including herbivory [16,17], and pollinator visitation and landing [18].…”

“…While wind is thus known to have many effects on pollinator behavior and ecology, our understanding of its influence on bee abundance and plant visitation rates is limited. While extreme wind speeds restrict bee flight and foraging (reviewed in [29]), recent studies have found that wind can have either positive [30] or negligible [10,31] effects on bee abundance and activity. Some wind's variable effects could be explained by differences in pollinator sensory ecology, particularly the importance of olfactory cues for locating floral resources.…”