The visual ecology of bees - Tales of diverse eyes and behaviours

Abstract: The buzzing flight of bees is a popular summer hit. Yet, outside of a few familiar species of honeybees and bumblebees, these fantastic little creatures are still mostly unknown. With about twenty-five thousand species, bees are a very diverse group. They can be found in drastically different habitats. For example, some kinds of bumblebees endure the freezing temperatures and windswept tundra of Greenland, while others only thrive in the heat and humidity of the Amazonian forest. Some bees live in huge colonies with tens of thousands of members, while others live solitary lives. Some are narrower than a sesame seed, while others can reach the size of a human thumb. Despite these differences, bees all have in common the urge to visit flowers where they find their food. This habit makes them very important for the pollination of plants across the world. To go about their laborious life, bees make extensive use of their vision. They possess two types of eyes – ocelli and compound eyes – that they use to control their flight, find their way through the world, discover flowers and spot possible mates. To understand how bees interact with the environment, we thus need to explore the diversity of their eyes and of how they use them.The first chapter of my thesis is about landing, which is a fundamental behaviour in flying insects. However, in bees it is poorly known whether different species land in different ways. During an expedition to Brazil, I came across a species of bee with the most peculiar landing style. Rather than slowing down to land, as most animals do, these bees accelerate just before touchdown on the entrance to their hive. Why do these bees speed up when they land? Using a computer simulation, I found that this weird strategy may help the bees to avoid mid-air collisions with nestmates and reduce bee ‘traffic jams’ in front of the hive. In turn, this would make food collection more efficient for the colony and it would be easier for hive members to defend against intruders. With this chapter, I showed that the lifestyle of bees – where they live, how many there are and if they are exposed to intruders – can strongly influence their behaviour.In chapter two, I then asked if and how the bees from chapter one use vision to control their peculiar landing. I found that they did indeed rely on vision to control their landing and that they did so in a simple manner. Essentially, when the image of the entrance of the hive reaches a given size on their eyes, these bees start to speed up. When the image of the entrance reaches a second set size on the eyes of landing bees, they extend their landing gear – which is, for bees, their legs – in preparation for touchdown. This chapter reveals that bees can use simple rules to achieve complex behaviours such as landing safely.To explore the diversity of eyes in a large number of bees, we use X-ray images taken from a sample as it rotates (an approach known as computed tomography or CT, commonly used in a medical setting) to produce 3D images of the eyes. However, powerful tools are needed to analyse the large amounts of data that this approach generates. As I want to better understand how bee eyes work, I needed an efficient method for analysing 3D eye images created by CT, so I developed an automatic tool for distinguishing essential optical structures in the eyes of insects and other arthropods. In chapter three, I describe this method, provide a guide to use it, and give examples of its application to a few insect eyes.In the last chapter, I used CT to look into the diversity of the eyes across a range of bumblebees from different habitats around the world. Even though different species are genetically close to each other, I found that their eyes were far from ‘all the same’. For example, bumblebees that live in forests have eyes that may enable them to see less sharp but better in dim light than bumblebees living in open landscapes. I also found that cuckoo bumblebees – bees that lay their eggs in another bumblebee hive like cuckoo birds do – had peculiar eyes in comparison to other bumblebees. This indicates that the eyes of each species of bumblebees may be specialised for a specific combination of lifestyle and habitat. These results are important for the conservation of bumblebees because they suggest that the eyes of some species may make them more sensitive than others to changes in the environment. For example, farming practices that create large open fields may particularly disadvantage bumblebees with eyes adapted to forests.These four chapters only scratch the surface of the tight links between the eyes of bees, the ways they behave, and the worlds they live in. I hope that efforts to look into their diverse eyes will continue and will help to protect these crucial but endangered animals.