Visual and movement memories steer foraging bumblebees along habitual routes

Abstract

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.

FlyDetector—Automated Monitoring Platform for the Visual–Motor Coordination of Honeybees in a Dynamic Obstacle Scene Using Digital Paradigm

“…In this study, we used a fisheye camera to simulate optic flow changes on insect foreheads and analyzed the collected images of the entire visual field to study the VMC of insects. In addition, we determined three parameters of honeybee behavior, including x - and y -axis differences and yaw orientation, which have been widely used to describe VMC behavior, such as collision avoidance [ 25 , 26 ] and visual memory behaviors [ 16 , 27 ]. In addition, real-time parameters of the gap were supported, enabling studies on the VMC mechanism in insects facing movement barriers.…”

“…Three classical visual parameters were used to analyze the behavior of compound-eyed insects [ 16 , 28 ], in order to verify our hypothesis that the flight stability of compound-eyed insects when facing dynamic scenes was due to them actively reducing the accuracy of the amplitude of the lateral visual motion recognition behavior. These included retinal size γ (γ, Equation (4)), rate of change of retinal size ( , Equation (5)), and relative retinal expansion velocity RREV (RREV, Equation (6)).…”

“…In addition, the vector velocity changes during the flight of the bumblebee were integrated to study the mechanism of identifying gaps and evaluating their passage during flight. For example, Bertrand et al [ 16 ] studied the interactions of visual memory, collision avoidance, and path integration of bumblebees using intra-channel heterochromatism to determine whether bumblebees use motor and visual memories to solve navigational conflict situations. Utilizing high-speed schlieren photography and particle-tracking-velocimetry, the wake flow of tethered houseflies was investigated [ 17 ], and Convolutional Neural Networks (CNNs) were also used to predict bee behaviors [ 18 ].…”

The potential underlying mechanisms during learning flights

“…In contrast to visual navigation, these local control mechanisms require little learning, and models often use hard-coded mechanisms to mimic such control [Bertrand et al. ( 2021 ), Lecoeur et al ( 2019 ), see for reviews Srinivasan et al. ( 1996 ), Serres and Ruffier ( 2017 )].…”

“… 2020 ), path integration (Webb 2019 ), local homing (Zeil 2022 ), and route-following (Bertrand et al. 2021 ; Buatois and Lihoreau 2016 ). We will see that these strategies have advantages and limitations (see Sect.…”