Bumblebee flight performance in cluttered environments: effects of obstacle orientation, body size and acceleration

James D. Crall, Sridhar Ravi, Andrew M. Mountcastle, Stacey A. Combes

Locomotion through structurally complex environments is fundamental to the life history of most flying animals, and the costs associated with movement through clutter have important consequences for the ecology and evolution of volant taxa. However, few studies have directly investigated how flying animals navigate through cluttered environments, or examined which aspects of flight performance are most critical for this challenging task. Here, we examined how body size, acceleration and obstacle orientation affect the flight of bumblebees in an artificial, cluttered environment. Non-steady flight performance is often predicted to decrease with body size, as a result of a presumed reduction in acceleration capacity, but few empirical tests of this hypothesis have been performed in flying animals. We found that increased body size is associated with impaired flight performance (specifically transit time) in cluttered environments, but not with decreased peak accelerations. In addition, previous studies have shown that flying insects can produce higher accelerations along the lateral body axis, suggesting that if maneuvering is constrained by acceleration capacity, insects should perform better when maneuvering around objects laterally rather than vertically. Our data show that bumblebees do generate higher accelerations in the lateral direction, but we found no difference in their ability to pass through obstacle courses requiring lateral versus vertical maneuvering. In sum, our results suggest that acceleration capacity is not a primary determinant of flight performance in clutter, as is often assumed. Rather than being driven by the scaling of acceleration, we show that the reduced flight performance of larger bees in cluttered environments is driven by the allometry of both path sinuosity and mean flight speed. Specifically, differences in collision-avoidance behavior underlie much of the variation in flight performance across body size, with larger bees negotiating obstacles more cautiously. Thus, our results show that cluttered environments challenge the flight capacity of insects, but in surprising ways that emphasize the importance of behavioral and ecological context for understanding flight performance in complex environments.