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.

Keywords: bee; environmental complexity; insect flight; radio-frequency identification (RFID); stability; wind.

Figure 1.

Simultaneous sampling of environmental wind and bumblebee foraging behaviour. (a) Field experimental set-up, showing location of the experimental bumblebee colony and adjacent sonic anemometer for recording wind speed and turbulence. (b) RFID-tagged bumblebee forager (black arrow) approaching the nest entrance. (c) Sample data collected over 2 days, showing environmental wind (blue, top), temperature (red, middle), and foraging behaviour of individual bumblebee workers (black, bottom). For each worker, nest exits and entrances are indicated by filled and open triangles, respectively, arranged along a single row.

Figure 2.

Foraging bumblebees experience highly variable wind environments. (a) Heat map of instantaneous wind speeds and turbulence intensities observed over 10-s intervals during all bumblebee foraging bouts. Dashed grey lines and open black circles show combinations of wind speeds and turbulence intensity used in subsequent wind tunnel experiments. (b,c) Mean wind speed (b) and turbulence intensity (c) of observed (grey) versus simulated (white) foraging bouts. Boxes show the median and inter-quartile range (IQR), and whiskers indicate data range (75th and 25th ± 1.5 × IQR, respectively).

Figure 3.

Wind tunnel experiments to test the effect of turbulent flow on bumblebee flight. (a) Schematic diagram of wind tunnel design. (b) Turbulent power spectra for laminar (blue) and turbulent (red) flow conditions in the wind tunnel. Black line indicates the expected −5/3 decay characteristic of freestream turbulence in natural environments. (c) Schematic drawing of a bumblebee showing the three axes of body angular orientation. (d) Sample trace of pitch and roll over a single trial with turbulent flow at 1.5 m s⁻².

Figure 4.

Body stability and mean wing kinematics across flow conditions. (a) Standard deviation of roll orientation, (b) mean wingbeat frequency and (c) mean stroke amplitude by speed and flow condition, with laminar trials in blue and turbulent trials in red. Bars above show comparisons between laminar and turbulent flow trials, at 1.5 and 3.0 m s⁻¹, and bars below show comparisons between laminar flow trials across speeds. Asterisks indicate significant differences between groups at the α = 0.05 level, and daggers indicate marginal significance (0.05 < p < 0.10). Boxplots show the median and IQR, and whiskers depict the data range (75th and 25th ± 1.5 × IQR, respectively).

Figure 5.

Variability in wing kinematics during flight in turbulence. (a) Within-trial variance in left–right amplitude asymmetry and (b) maximum left–right amplitude asymmetry, with laminar trials in blue and turbulent trials in red. Bars above show comparisons between laminar and turbulent flow trials, at 1.5 and 3.0 m s⁻¹, and bars below show comparisons between laminar flow trials across speeds. (c,e) Correlations between absolute roll angle of the body and asymmetry in stroke amplitude between the left and right wings, shown (c) for each stroke during one trial and (e) stroke-averaged correlations across all trials. (d) Locations of wingtips at pronation (orange) and supination (blue) during a single trial, rotated into the body frame. (f) Variance of pronation angle (orange) and supination angle (blue) across trials. Boxplots show the median and IQR, while whiskers depict the data range (75th and 25th ± 1.5 × IQR, respectively). Asterisks indicate significant differences between groups at the α = 0.05 level, and daggers indicate marginal significance (0.05 < p < 0.10).