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.

A number of insects fly over long distances below the natural canopy, where the physical environment is highly cluttered consisting of obstacles of varying shape, size and texture. While navigating within such environments, animals need to perceive and disambiguate environmental features that might obstruct their flight. The most elemental aspect of aerial navigation through such environments is gap identification and 'passability' evaluation. We used bumblebees to seek insights into the mechanisms used for gap identification when confronted with an obstacle in their flight path and behavioral compensations employed to assess gap properties. Initially, bumblebee foragers were trained to fly though an unobstructed flight tunnel that led to a foraging chamber. After the bees were familiar with this situation, we placed a wall containing a gap that unexpectedly obstructed the flight path on a return trip to the hive. The flight trajectories of the bees as they approached the obstacle wall and traversed the gap were analyzed in order to evaluate their behavior as a function of the distance between the gap and a background wall that was placed behind the gap. Bumblebees initially decelerated when confronted with an unexpected obstacle. Deceleration was first noticed when the obstacle subtended around 35 deg on the retina but also depended on the properties of the gap. Subsequently, the bees gradually traded off their longitudinal velocity to lateral velocity and approached the gap with increasing lateral displacement and lateral velocity. Bumblebees shaped their flight trajectory depending on the salience of the gap, indicated in our case by the optic flow contrast between the region within the gap and on the obstacle, which decreased with decreasing distance between the gap and the background wall. As the optic flow contrast decreased, the bees spent an increasing amount of time moving laterally across the obstacles. During these repeated lateral maneuvers, the bees are probably assessing gap geometry and passability.

Returning home is a crucial task accomplished daily by many animals, including humans. Because of their tiny brains, insects, like bees or ants, are good study models for efficient navigation strategies. Bees and ants are known to rely mainly on learned visual information about the nest surroundings to pinpoint their barely visible nest-entrance. During the return, when the actual sight of the insect matches the learned information, the insect is easily guided home. Occasionally, modifications to the visual environment may take place while the insect is on a foraging trip. Here, we addressed the ecologically relevant question of how bumblebees' homing is affected by such a situation. In an artificial setting, we habituated bees to be guided to their nest by two constellations of visual cues. After habituation, these cues were displaced during foraging trips into a conflict situation. We recorded bumblebees' return flights in such circumstances and investigated where they search for their nest entrance following the degree of displacement between the two visually relevant cues. Bumblebees mostly searched at the fictive nest location as indicated by either cue constellation, but never at a compromise location between them. We compared these experimental results to the predictions of different types of homing models. We found that models guiding an agent by a single holistic view of the nest surroundings could not account for the bumblebees' search behaviour in cue-conflict situations. Instead, homing models relying on multiple views were sufficient. We could further show that homing models required fewer views and got more robust to height changes if optic flow-based spatial information was encoded and learned, rather than just brightness information.

Insects are remarkable flyers and capable of navigating through highly cluttered environments. We tracked the head and thorax of bumblebees freely flying in a tunnel containing vertically oriented obstacles to uncover the sensorimotor strategies used for obstacle detection and collision avoidance. Bumblebees presented all the characteristics of active vision during flight by stabilizing their head relative to the external environment and maintained close alignment between their gaze and flightpath. Head stabilization increased motion contrast of nearby features against the background to enable obstacle detection. As bees approached obstacles, they appeared to modulate avoidance responses based on the relative retinal expansion velocity (RREV) of obstacles and their maximum evasion acceleration was linearly related to RREVmax. Finally, bees prevented collisions through rapid roll manoeuvres implemented by their thorax. Overall, the combination of visuo-motor strategies of bumblebees highlights elegant solutions developed by insects for visually guided flight through cluttered environments.

13 14 A number of insects fly over long distances below the natural canopy where the physical 15 environment is highly cluttered consisting of obstacles of varying shape, size and 16 texture. While navigating within such environments animals need to perceive and 17 disambiguate environmental features that might obstruct their flight. The most 18 elemental aspect of aerial navigation through such environments is gap identification 19 and passability evaluation. We used bumblebees to seek insights into the mechanisms 20 used for gap identification when confronted with an obstacle in their flight path and 21 behavioral compensations employed to assess gap properties. Initially, bumblebee 22 33 the gap, in our case, indicated by the optic flow contrast between the region within the 34 gap and on the obstacle, which increases with decreasing distance between the gap and 35 the background wall. As the optic flow contrast decreased the bees spent increasing 36 time moving laterally across the obstacles. During these repeated lateral maneuvers the 37 bees are likely assessing gap geometry and passability. 38 39 40 65 and path planning. For long distance navigation, flying insects might use, apart from 66 vision, other sensory modalities such as odor and geomagnetic fields (Knaden and 67 Graham, 2016) In order for a flying animal to arrive at its intended destination or ensure 68 safe locomotion, at a basic level, the animal needs to process the obstacles that lie in its 69 path and identify gaps. Obstacle and gap detection may thus be considered the most 70