Nest-associated scent marks help bumblebees localizing their nest in visually ambiguous situations.

Social insects such as ants and bees are excellent navigators. To manage their daily routines bumblebees, as an example, must learn multiple locations in their environment, like flower patches and their nest. While navigating from one location to another, they mainly rely on vision. Although the environment in which bumblebees live, be it a meadow or a garden, is visually stable overall, it may be prone to changes such as moving shadows or the displacement of an object in the scenery. Therefore, bees might not solely rely on visual cues, but use additional sources of information, forming a multimodal guidance system to ensure their return home to their nest. Here we show that the home-finding behavior of bumblebees, when confronted with a visually ambiguous scenario, is strongly influenced by natural scent marks they deposit at the inconspicuous nest hole when leaving their nest. Bumblebees search for a longer time and target their search with precision at potential nest locations that are visually familiar, if also marked with their natural scent. This finding sheds light on the crucial role of odor in helping bees find their way back to their inconspicuous nest.

Bumblebees display characteristics of active vision during robust obstacle avoidance flight.

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.

Visual and movement memories steer foraging bumblebees along habitual routes.

One persistent question in animal navigation is how animals follow habitual routes between their home and a food source. Our current understanding of insect navigation suggests an interplay between visual memories, collision avoidance and path integration, the continuous integration of distance and direction travelled. However, these behavioural modules have to be continuously updated with instantaneous visual information. In order to alleviate this need, the insect could learn and replicate habitual movements ('movement memories') around objects (e.g. a bent trajectory around an object) to reach its destination. We investigated whether bumblebees, Bombus terrestris, learn and use movement memories en route to their home. Using a novel experimental paradigm, we habituated bumblebees to establish a habitual route in a flight tunnel containing 'invisible' obstacles. We then confronted them with conflicting cues leading to different choice directions depending on whether they rely on movement or visual memories. The results suggest that they use movement memories to navigate, but also rely on visual memories to solve conflicting situations. We investigated whether the observed behaviour was due to other guidance systems, such as path integration or optic flow-based flight control, and found that neither of these systems was sufficient to explain the behaviour.

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

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.

Visually guided homing of bumblebees in ambiguous situations: A behavioural and modelling study.

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.

Analysing Head-Thorax Choreography During Free-Flights in Bumblebees.

Animals coordinate their various body parts, sometimes in elaborate manners to swim, walk, climb, fly, and navigate their environment. The coordination of body parts is essential to behaviors such as, chasing, escaping, landing, and the extraction of relevant information. For example, by shaping the movement of the head and body in an active and controlled manner, flying insects structure their flights to facilitate the acquisition of distance information. They condense their turns into a short period of time (the saccade) interspaced by a relatively long translation (the intersaccade). However, due to technological limitations, the precise coordination of the head and thorax during insects' free-flight remains unclear. Here, we propose methods to analyse the orientation of the head and thorax of bumblebees Bombus terrestris, to segregate the trajectories of flying insects into saccades and intersaccades by using supervised machine learning (ML) techniques, and finally to analyse the coordination between head and thorax by using artificial neural networks (ANN). The segregation of flights into saccades and intersaccades by ML, based on the thorax angular velocities, decreased the misclassification by 12% compared to classically used methods. Our results demonstrate how machine learning techniques can be used to improve the analyses of insect flight structures and to learn about the complexity of head-body coordination. We anticipate our assay to be a starting point for more sophisticated experiments and analysis on freely flying insects. For example, the coordination of head and body movements during collision avoidance, chasing behavior, or negotiation of gaps could be investigated by monitoring the head and thorax orientation of freely flying insects within and across behavioral tasks, and in different species.

The Critical Role of Head Movements for Spatial Representation During Bumblebees Learning Flight.

Bumblebees perform complex flight maneuvers around the barely visible entrance of their nest upon their first departures. During these flights bees learn visual information about the surroundings, possibly including its spatial layout. They rely on this information to return home. Depth information can be derived from the apparent motion of the scenery on the bees' retina. This motion is shaped by the animal's flight and orientation: Bees employ a saccadic flight and gaze strategy, where rapid turns of the head (saccades) alternate with flight segments of apparently constant gaze direction (intersaccades). When during intersaccades the gaze direction is kept relatively constant, the apparent motion contains information about the distance of the animal to environmental objects, and thus, in an egocentric reference frame. Alternatively, when the gaze direction rotates around a fixed point in space, the animal perceives the depth structure relative to this pivot point, i.e., in an allocentric reference frame. If the pivot point is at the nest-hole, the information is nest-centric. Here, we investigate in which reference frames bumblebees perceive depth information during their learning flights. By precisely tracking the head orientation, we found that half of the time, the head appears to pivot actively. However, only few of the corresponding pivot points are close to the nest entrance. Our results indicate that bumblebees perceive visual information in several reference frames when they learn about the surroundings of a behaviorally relevant location.

Gap perception in bumblebees.

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.