The Dominant Role of Visual Motion Cues in Bumblebee Flight Control Revealed Through Virtual Reality

Abstract

Flying bees make extensive use of optic flow: the apparent motion in the visual scene generated by their own movement. Much of what is known about bees' visually-guided flight comes from experiments employing real physical objects, which constrains the types of cues that can be presented. Here we implement a virtual reality system allowing us to create the visual illusion of objects in 3D space. We trained bumblebees, Bombus ignitus, to feed from a static target displayed on the floor of a flight arena, and then observed their responses to various interposing virtual objects. When a virtual floor was presented above the physical floor, bees were reluctant to descend through it, indicating that they perceived the virtual floor as a real surface. To reach a target at ground level, they flew through a hole in a virtual surface above the ground, and around an elevated virtual platform, despite receiving no reward for avoiding the virtual obstacles. These behaviors persisted even when the target was made (unrealistically) visible through the obstructing object. Finally, we challenged the bees with physically impossible ambiguous stimuli, which give conflicting motion and occlusion cues. In such cases, they behaved in accordance with the motion information, seemingly ignoring occlusion.

Motion cues from the background influence associative color learning of honey bees in a virtual-reality scenario

“…These and other findings 59 , 61 – 63 clearly show the importance of ventral motion cues for the translational displacements of flying insects. Although less information is available for walking insects, experiments performed on desert ants Cataglyphis fortis walking in narrow tunnels showed that both the lateral and the ventral optic flow were dispensable for distance estimation 64 .…”

“…Whether Red 100 affected negatively chromatic discrimination, interfering with the L-receptor type involved in this discrimination is unknown. VR experiments with freely flying bumblebees trained to land on a virtual horizontal blue target located on a projected achromatic checkerboard made of random pink (RGB: 255, 127, 127) and white (RGB: 255, 255, 255) squares showed that the background had no incidence on the bees’ performance 61 . In this case, the pink light used could potentially stimulate all receptor types and thus truly affect the color vision system, contrarily to our red light (RGB: 255, 0, 0).…”

Characterizing long-range search behavior in Diptera using complex 3D virtual environments

“…This also indicates that static elements in the insect's field of view such as bezels, capillaries, and the camera did not evoke any gaze fixation as evidenced by the lack of any specific direction in this landscape and as observed in previous VRs (10,(23)(24)(25)(26). However, when provided a tree, flies fixated on and approached the tree, and exhibited stereotypical object avoidance/landing responses with rapid saccades (rapid body turns within the tree canopy) and foreleg extension when within <10 cm of elements in the canopy (35,36) This indicates that flying insects can distinguish, navigate, and respond to virtual 3D objects from the surrounding visual scenery. In a world with two identical trees, flies oriented and approached both trees equally, as described previously for field behavior ( 22 Along with a pest (apple fly), we also measured localization of virtual tree-like objects in a crane fly (P. laeta; S3) and for a disease vector (male mosquito, A. aegypti; Fig.…”

Putting the ecology back into insect cognition research

“…make objects appear, disappear, or even be at apparent distances) in freely walking and flying insects. For instance, flying bumblebees (Bombus terrestris) can be trained to search for virtual feeding platform or avoid virtual obstacles displayed on a screen on the ground of a flight arena (Frasnelli et al, 2018).…”