Spatial Vision in Bees : Behavioural investigation of spatial resolution and contrast sensitivity

Abstract

Bees use multiple sensory modalities to perform day-to-day tasks. Light allows them to perceive objects and the general features of their surroundings, enabling them to find food and to navigate safely across the landscape. Although both these tasks involve vision, the requirements of the visual system differ depending upon what the bee wants to achieve; locate a flower to feed from or adjust its position in space to support a safe flight. This thesis addresses to what detail and contrast bees can perceive their surroundings under these two different behavioral contexts.

The thesis starts with a brief introduction to the fundamental aspects of spatial vision and a review of the methods used to study it in bees. In Paper I, I estimate the behavioral limits of spatial resolution and contrast sensitivity of the object discrimination system of the buff-tailed bumblebee Bombus terrestris. To do this, I trained the bees to discriminate between a rewarded and an unrewarded stimulus grating based on its orientation (horizontal or vertical). Once the bees had learnt this task, I changed grating frequency and contrast up until the point when the bees could no longer tell the differently oriented gratings apart. This defined the limits of spatial resolution and contrast sensitivity for this species for this visual task. The results suggest that buff-tailed bumblebees have a resolution threshold of about a quarter of a grating cycle per degree of visual angle. This is similar to the resolution threshold previously determined for honeybees. The contrast sensitivity of the bumblebees, however, was several times lower than that reported for honeybees. To determine if this difference in contrast sensitivity is species dependent, or possibly context dependent, I performed another three studies on two more bee species in a different behavioral context.

In Paper II, III, IV I estimated the spatial resolution and contrast sensitivity underlying the motion detection system in Asian honeybees, Apis cerana, buff-tailed bumblebees and European honeybees, Apis mellifera. To do this, I trained the bees to fly through a tunnel dressed with gratings of different spatial frequency and contrast and analyzed their flight trajectories as a function of the gratings: a bee that could resolve the grating shifted its lateral position away from it, while a bee that could not resolve it flew along the midline of the tunnel. From these results, it became obvious that the motion detection system of honeybees seems to have a twofold decrease in the spatial resolution compared to their object discrimination system. In addition, all three bee species tested have a very high contrast sensitivity underlying their motion detecting system.
In summary, the results presented in thesis indicate that the limits of spatial vision in bees depend largely on the behavioral context.

Abstract (Swedish)

Popular Science Abstract

How well bees can see the world?^a

Bees such as bumblebees and honeybees are some of the most important pollinators. They pollinate by using different sensory cues from the flowers, primarily vision and olfaction. In my PhD I was interested in understanding how well bees can see while they are inspecting flowers as well as while they are performing high-speed flight maneuvers.
Most of us have at least once visited an optician to get our vision checked. To quantify how well we can see, the optician asks us to read a chart (popularly known as Snellen’s chart) with letters of different orientations and sizes. Based on the patient’s ability to identify the letters, one can estimate how well a person can see visual details. This is known as estimating spatial resolution or visual acuity. It is not possible to use Snellen’s chart with the bees as they have not been taught how to read letters. Therefore, to determine the visual acuity of bees, I trained them to discriminate between vertically and horizontally oriented black and white stripe patterns by using a drop of sugar solution as the reward for a correct choice. Once they learned to discriminate horizontal the patterns, I then increased the number of stripes. If the bees could no longer discriminate the horizontal from the vertical pattern, then I assumed that the stripes were too fine for them to resolve. Since this was a dual choice experiment (between horizontal and vertical stripe patterns) when bees failed to see the orientation of the gratings they would make an equal number of visits to both patterns. By finding the point at which the bees could no longer discriminate the stripes, I could determine the limit of their spatial resolution. I also used a similar method to estimate the minimum amount of contrast (the difference between the brightness of the light and dark stripes) that is needed to resolve the stripes. 
In my PhD, I was also interested to see how much these estimates of visual acuity depend upon the context of the behavior being performed. For instance, we humans might see our immediate surroundings moving past us when travelling in a train as streaks or lines. The visual world would not appear like a streak if we were to inspect the scene from a static view point. One can imagine that, as we move in a train, we fail to see the finer details of the world past us. We know that bees can navigate through very visually-detailed environments. However, we do not know how well they can see the fine details of the world during their high-speed flight maneuvers. To investigate this, I conducted experiments where the bees were trained to fly along a tunnel to receive a food reward. I filmed their flights and analyzed them to see how well they responded to gratings of different sizes and contrasts.

The results indicate that honeybees have lower resolution vision when they are in motion. In addition, honeybees and bumblebees were able to see stripes with a lower contrast (that is, they had a higher contrast sensitivity) when flying along the tunnel (and they had to use their visual motion detection system) than when performing the dual choice experiment from a static position (when they were using their object discrimination system). These results suggest that they have different visual thresholds for each of these behavioral contexts, which are possibly mediated by different pathways in the brain. 
This means that bees see the world differently depending on whether they are standing still or flying!
^a Originally published popular science article in Navigation News (Chakravarthi et al. 2016a). Edited with permission from the editor.

• author: Chakravarthi, Aravin
• supervisor: Marie Dacke; Almut Kelber; Emily Baird
• opponent: Dr. Hempel de Ibarra, Natalie, University of Exeter, United Kingdom
• organization: Functional zoology; Lund Vision Group (research group)
• publishing date: 2017-05
• type: Thesis
• publication status: published
• subject: Natural Sciences
• keywords: Insect vision, Honeybees, Bumblebees, Spatial resolution, Contrast sensitivity, Motion detection, Object discrimination
• defense location: Lecture hall “Blå hallen”, Ecology building, Sölvegatan 37, Lund
• defense date: 2017-06-09 10:00:00
• ISBN: 978-91-7753-326-9
• ISBN: 978-91-7753-325-2
• language: English
• LU publication?: yes
• id: 5edcd192-f615-453d-8e7c-333b2bea6e2f
• date added to LUP: 2017-05-16 11:51:23
• date last changed: 2020-10-13 13:47:00