Abstract

Gaze direction is closely coupled with body movement in insects and other animals. If movement patterns interfere with the acquisition of visual information, insects can actively adjust them to seek relevant cues. Alternatively, where multiple visual cues are available, an insect’s movements may influence how it perceives a scene. We show that the way a foraging bumblebee approaches a floral pattern could determine what it learns about the pattern. When trained to vertical bicoloured patterns, bumblebees consistently approached from below centre in order to land in the centre of the target where the reward was located. In subsequent tests, the bees preferred the colour of the lower half of the pattern that they predominantly faced during the approach and landing sequence. A predicted change of learning outcomes occurred when the contrast line was moved up or down off-centre: learned preferences again reflected relative frontal exposure to each colour during the approach, independent of the overall ratio of colours. This mechanism may underpin learning strategies in both simple and complex visual discriminations, highlighting that morphology and action patterns determines how animals solve sensory learning tasks. The deterministic effect of movement on visual learning may have substantially influenced the evolution of floral signals, particularly where plants depend on fine-scaled movements of pollinators on flowers.

Highlights

  • Eyes and associated neural architectures have evolved in diverse ways to provide animals with adaptive views of the world

  • Other animals cannot shift their gaze independently from the body due to morphological constraints, meaning that the direction of gaze is more closely tied with their actions. This coupling is pronounced in many insects which are capable of very limited head movements and lack the ability to move their eyes and lenses within the head

  • We argue that, when visual cues are not limiting, efficient motor patterns define the viewing conditions and incidentally determine what visual information is acquired for solving various behavioural tasks, such as learning the colours and patterns of a food source, a task of particular importance for bees foraging on flowers

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Summary

INTRODUCTION

Eyes and associated neural architectures have evolved in diverse ways to provide animals with adaptive views of the world. Other animals cannot shift their gaze independently from the body due to morphological constraints, meaning that the direction of gaze is more closely tied with their actions This coupling is pronounced in many insects which are capable of very limited head movements and lack the ability to move their eyes and lenses within the head. Previous evidence suggests that bees might generally prefer to approach vertically presented stimuli from below (Anderson, 1977; Giger, 1996), which could significantly affect perception and learning processes This question is highly relevant for understanding the bee’s natural foraging behaviour, as many flowers are tilted or vertically oriented. We show that the outcome of a learning task with flower-like colour patterns is determined by the bees’ approach directions during training

MATERIALS AND METHODS
Training Procedures
RESULTS
DISCUSSION
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