How honeybees measure their distance from objects of unknown size

Abstract

Summary 1. To investigate whether bees use motion cues in the task of estimating distance, they were trained to collect a food reward on one of several ‘flowers’ of different sizes on an artificial meadow (Figs. 1, 4a, 6a). In each experiment, the height of the rewarded flower was kept constant during training. The bees were prevented from learning the sizes and positions of the flowers by varying these parameters continually during training as well as during the subsequent discrimination tests. Thus, the only reliable cue that could be used to recognize the rewarded flower was the speed at which its image moved across the retina as the bees flew over the meadow: The contours of a high flower would move faster than those of a lower one, irrespective of size. 2. Bees that are rewarded on a flower placed at a particular height discriminate it from flowers at other heights (Fig. 2a, b). This is independent of whether the bees have been trained to the highest flower (Fig. 4b), the lowest flower (Fig. 5b), or one at an intermediate height (Fig. 6b). In each case, they are able to select the correct flower according to the particular speed at which its image moves across the eye during the searching flight. 3. Under our experimental conditions, bees can discriminate height differences of 2 cm (Figs. 4c, 5c). 4. Introduction of a textured background enhances the accuracy of height discrimination (Fig. 2d). 5. Discrimination of flower height breaks down in the absence of green contrast (Fig. 2c), showing that the bees' performance in this task is mediated by signals from the green-sensitive receptors and is consequently colour-blind, as are all of the motion-induced behaviours so far examined in the bee. 6. We conclude that bees can estimate an object's distance by using its apparent motion across the retina when the background is featureless, and possibly, in addition, its motion relative to the background when the background is textured. When encountering a novel environment comprising unfamiliar objects of unknown size, the bees can evidently use these two types of motion cues to acquire a three-dimensional percept of the visual world.