Bumblebees perceive the spatial layout of their environment in relation to their body size and form to minimize inflight collisions

Abstract

Animals that move through complex habitats must frequently contend with obstacles in their path. Humans and other highly cognitive vertebrates avoid collisions by perceiving the relationship between the layout of their surroundings and the properties of their own body profile and action capacity. It is unknown whether insects, which have much smaller brains, possess such abilities. We used bumblebees, which vary widely in body size and regularly forage in dense vegetation, to investigate whether flying insects consider their own size when interacting with their surroundings. Bumblebees trained to fly in a tunnel were sporadically presented with an obstructing wall containing a gap that varied in width. Bees successfully flew through narrow gaps, even those that were much smaller than their wingspans, by first performing lateral scanning (side-to-side flights) to visually assess the aperture. Bees then reoriented their in-flight posture (i.e., yaw or heading angle) while passing through, minimizing their projected frontal width and mitigating collisions; in extreme cases, bees flew entirely sideways through the gap. Both the time that bees spent scanning during their approach and the extent to which they reoriented themselves to pass through the gap were determined not by the absolute size of the gap, but by the size of the gap relative to each bee’s own wingspan. Our findings suggest that, similar to humans and other vertebrates, flying bumblebees perceive the affordance of their surroundings relative their body size and form to navigate safely through complex environments.

Information Is Where You Find It: Perception as an Ecologically Well-Posed Problem

“…hover in front of the gap and oscillate from side to side, keeping the edges in its field of view (see Figure 9). As the gap narrows from $2 to <1 wingspans, the mean number of passes increases from 2 to 10, and the mean peering time grows from <1 second to 4 seconds (Ravi et al, 2020a). This strongly suggests that the bees are scanning the edges of narrower gaps to determine their width from optic flow.…”

“…He said that his bees were behaving just like our humans: As gap width (G) decreases, the bee begins to pivot about a vertical axis and fly through the gap sideways (Figure 9), analogous to humans rotating their shoulders. Because the bee's body length is only half its wingspan (W), this yaw maneuver enables them to pass through much narrower gaps (Ravi et al, 2020a), as Sridhar's slow-motion videos illustrate (Ravi et al, 2020b).…”

Wind and route choice affect performance of bees flying above versus within a cluttered obstacle field

“…Wind increased the magnitude of lateral excursions, but this effect was likely limited to navigation rather than force production (e.g., air speed control) because, contrary to ground speeds, the effect occurred in both tailwinds and headwinds. Mechanical stimuli from wind can interfere with insect responses to visual stimuli [52], so the larger lateral excursions executed by honeybees in wind were possibly an intentional action to take in more visual information from the landscape to compensate for the mechanical challenge of wind [22,23]. To our knowledge, most studies on the effects of wind on bee flight have been conducted in headwinds [21,48], so additional studies that examine how steady winds from other directions interact with visual signals to affect flight performance are needed [54].…”

“…In addition, the difference in optic flow produced by nearby obstacles versus the background helps bees gauge the dimensions and distance of obstacles [22,23]. Bees can enhance the visual information they receive from obstacles in the environment by performing side-to-side casting maneuvers as they fly or by slowing down and visually inspecting obstacles before continuing their flights, a behavior often associated with learning the layout of a new environment [22][23][24]. Overall, visual information is crucial for flying bees, and obstacles (e.g., cluttered vegetation) help provide the signals necessary for bees to successfully transit these structures.…”

“…Thus, bees can use optic flow to gauge their distance from an obstacle [16,17], to reduce their flight speed as they approach an obstacle [20], to maintain their flight speed relative to an obstacle despite external wind [21], and to center themselves within a flight corridor, by moving laterally to balance optic flow across their left and right eyes [12,18,19]. In addition, the difference in optic flow produced by nearby obstacles versus the background helps bees gauge the dimensions and distance of obstacles [22,23]. Bees can enhance the visual information they receive from obstacles in the environment by performing side-to-side casting maneuvers as they fly or by slowing down and visually inspecting obstacles before continuing their flights, a behavior often associated with learning the layout of a new environment [22][23][24].…”