High-Speed Videography Reveals How Honeybees Can Turn a Spatial Concept Learning Task Into a Simple Discrimination Task by Stereotyped Flight Movements and Sequential Inspection of Pattern Elements

Abstract

Honey bees display remarkable visual learning abilities, providing insights regarding visual information processing in a miniature brain. It was discovered that bees can solve a task that is generally viewed as spatial concept learning in primates, specifically the concept of "above" and "below." In these works, two pairs of visual stimuli were shown in the two arms of a Y-maze. Each arm displayed a "referent" shape (e.g., a cross, or a horizontal line) and a second geometric shape that appeared either above or below the referent. Bees learning the "concept of aboveness" had to choose the arm of the Y-maze in which a shape-any shape-occurred above the referent, while those learning the "concept of belowness" had to pick the arm in which there was an arbitrary item beneath the referent. Here, we explore the sequential decision-making process that allows bees to solve this task by analyzing their flight trajectories inside the Y-maze. Over 368 h of high-speed video footage of the bees' choice strategies were analyzed in detail. In our experiments, many bees failed the task, and, with the possible exception of a single forager, bees as a group failed to reach significance in picking the correct arm from the decision chamber of the maze. Of those bees that succeeded in choosing correctly, most required a close-up inspection of the targets. These bees typically employed a close-up scan of only the bottom part of the pattern before taking the decision of landing on a feeder. When rejecting incorrect feeders, they repeatedly scanned the pattern features, but were still, on average, faster at completing the task than the non-leaners. This shows that solving a concept learning task could actually be mediated by turning it into a more manageable discrimination task by some animals, although one individual in this study appeared to have gained the ability (by the end of the training) to solve the task in a manner predicted by concept learning.

Keywords: Apis mellifera; active vision; cognition; feature detection; local features; video tracking; visual learning.

Figure 1

Y-maze setup and training procedure for honeybees in an “aboveness–belowness” spatial learning task. (A) Schematic representation of the experimental setup. The Y-maze presents, on one side, the “above stimulus” with one of the five geometrical shapes above the referent cross, and on the other side the “below stimulus” where the same geometrical shape is below the cross. The center of the sheet contains the feeder where the bee has to crawl into a tunnel to get the reward. A timer is present to synchronize both cameras installed above the setup. (B) View of the Y-maze setup, taking the “bee perspective” from the decision chamber; the cross is, again, the referent. The “above” configuration is shown on the left, and the “below” configuration on the right. (C) Example of the conditioning and testing procedure. From bottom to top: bees were exposed to 15 pre-training bouts where a cross on a white sheet was rewarded (50% sugar solution) while the plain white sheet was associated with saturated quinine solution. Training consisted of 50 trials with “above configuration” in one arm and “below configuration” in the other one. The transfer tests were not rewarded. Half of the bees were rewarded on the “target above referent” relation whereas the other half was rewarded on the “target below referent” relation.

Figure 2

Performance of bees during training and transfer tests. (A) Group A (above configuration, n = 4) and Group B (below configuration, n = 7) learner bees. (B) Group A (above configuration, n = 5) and Group B (below configuration, n = 3) non-learner bees. Five blocks of 10 trials are represented with the percentage of correct choices. Green squares: number of correct feeders, blue circles: selection of correct Y-maze arm first, red triangles: abandoned incorrect arm for a correct feeder (the higher the better), purple diamonds: abandoned correct arm for an incorrect feeder (the lower the better). Transfer test results, hatched bars: percentage of correct first touches, dotted bars: percentage of accumulative touches on correct feeder. Error bars show standard deviation.

Figure 3

Summary of first and second scanned locations for bees during training. (A) learners, (B) non-learners. Solid: average number of 1st scans at a stimulus location (error bars: standard deviation). Hatched: average number of 2nd scans at a location (error bars: standard deviation), bottom: lowest shape presented on a stimulus, top: upper most shape, feeder: either a scan in front of, or landing on the feeder.