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

Abstract

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.

From Paths to Routes: A Method for Path Classification

“…However, we can extend it to trajectories that do not form routes. For example, animals may steer in a given direction to go away from a food source and hide its collected reward (e.g., dung beetle, Dacke et al, 2013 ), move in a convoluted manners to avoid a predator or chase prey (Boeddeker et al, 2003 ; Kane and Zamani, 2014 ; Wardill et al, 2017 ) or perform complex search behavior when searching for home (Doussot et al, 2020 ; Schultheiss et al, 2015 ). In these examples, the animals are not following a route.…”

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

“…Yet, several modeling analyses showed that to enable successful homing, there is no need to know the exact location in space where the bee memorizes environmental information, such as a panoramic-snapshot (Dewar et al, 2014 ; Doussot et al, 2020a ). These models solely require the memorized panoramic-snapshots to be oriented toward the nest-hole.…”

“…Therefore, insects also rely on view-matching in the final approach to their nest (Zeil, 2012 ; Webb, 2019 ; Sun et al, 2020 ). An insect is thought to compare its current retinotopic representation of the environment with one or several previously-stored views of its nest surroundings (Doussot et al, 2020a ). These views might be learned during its early trips out of the nest, when naïve to the visual surroundings.…”

“…However, insects like bees may use views containing depth information. Indeed brightness information alone cannot account for homing behavior under all observed environmental conditions (Zeil, 1993b ; Fry and Wehner, 2002 ; Vardy and Möller, 2005 ; Dittmar et al, 2010 , 2011 ; Riabinina et al, 2014 ; Boeddeker et al, 2015 ; Collett and Zeil, 2018 ; Lobecke et al, 2018 ; Doussot et al, 2020a ). Irrespective of the stored information about the environment, it is still unknown where exactly this information is gathered during the learning flights and in which frame of reference, be it allocentric or egocentric, it is represented in the insect brain.…”

Switching perspective: Comparing ground-level and bird’s-eye views for bees navigating clutter

“…Behavioural studies showed that views close to the goal are acquired during learning walks or flight [11,42] and modelling studies could emphasise the successful use during homing [12,14,13] for the memorised snapshots (eight positions taken either outside or inside the clutter and either above the clutter, bird's eye view, or close to the ground, frog's eye views). A&B: Examples of panoramic snapshots in A from the bird's eye view outside the clutter and in B frog's eye views inside the clutter.…”