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

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

Sex and age related changes in the locomotor activity and phototactic behaviors of two closely related species of Camponotus ants.

A virgin ant queen has only one opportunity in her lifetime to realize her reproductive fitness when she leaves her nest for a mating flight. After successful mating she sheds her wings, excavates a nest and starts laying eggs to initiate her own colony. Here we report the results of our study on two related species of Camponotus ants - day active Camponotus paria and night active Camponotus compressus - aimed at investigating (i) if there exist inter-species differences in the activity and phototactic behaviors of males and queens, (ii) whether these behaviors in the queen change after mating, and (iii) whether the activity rhythm of queens changes with age. We find that while activity profiles differ between C. paria and C. compressus virgin males and queens, such differences in queens disappear after mating. Once mated, the activity rhythm of queens shows little change with age; the rhythm in virgin queens, on the other hand, changes considerably. As virgins, C. paria queens are positively phototactic, while C. compressus queens are negatively phototactic. After mating, C. paria queens become less phototactic, particularly during the subjective night, while C. compressus queens remain negatively phototactic. These results indicate that there are considerable differences in the activity and phototactic behaviors of virgin queens of the two related species of Camponotus ants. Most of these differences disappear after mating, which suggests that these behaviors may have evolved primarily for the proper execution of pre-mating events

Spatial Vision in Bombus terrestris.

Bombus terrestris is one of the most commonly used insect models to investigate visually guided behavior and spatial vision in particular. Two fundamental measures of spatial vision are spatial resolution and contrast sensitivity. In this study, we report the threshold of spatial resolution in B. terrestris and characterize the contrast sensitivity function of the bumblebee visual system for a dual choice discrimination task. We trained bumblebees in a Y-maze experimental set-up to associate a vertical sinusoidal grating with a sucrose reward, and a horizontal grating with absence of a reward. Using a logistic psychometric function, we estimated a resolution threshold of 0.21 cycles deg(-1) of visual angle. This resolution is in the same range but slightly lower than that found in honeybees (Apis mellifera and A. cerana) and another bumblebee species (B. impatiens). We also found that the contrast sensitivity of B. terrestris was 1.57 for the spatial frequency 0.090 cycles deg(-1) and 1.26 for 0.18 cycles deg(-1)

Sex and age related changes in the locomotor activity and phototactic behaviors of two closely related species of Camponotus ants

A virgin ant queen has only one opportunity in her lifetime to realize her reproductive fitness when she leaves her nest for a mating flight. After successful mating she sheds her wings, excavates a nest and starts laying eggs to initiate her own colony. Here we report the results of our study on two related species of Camponotus ants - day active Camponotus paria and night active Camponotus compressus - aimed at investigating (i) if there exist inter-species differences in the activity and phototactic behaviors of males and queens, (ii) whether these behaviors in the queen change after mating, and (iii) whether the activity rhythm of queens changes with age. We find that while activity profiles differ between C. paria and C. compressus virgin males and queens, such differences in queens disappear after mating. Once mated, the activity rhythm of queens shows little change with age; the rhythm in virgin queens, on the other hand, changes considerably. As virgins, C. paria queens are positively phototactic, while C. compressus queens are negatively phototactic. After mating, C. paria queens become less phototactic, particularly during the subjective night, while C. compressus queens remain negatively phototactic. These results indicate that there are considerable differences in the activity and phototactic behaviors of virgin queens of the two related species of Camponotus ants. Most of these differences disappear after mating, which suggests that these behaviors may have evolved primarily for the proper execution of pre-mating events

High contrast sensitivity for visually guided flight control in bumblebees

Many insects rely on vision to find food, to return to their nest and to carefully control their flight between these two locations. The amount of information available to support these tasks is, in part, dictated by the spatial resolution and contrast sensitivity of their visual systems. Here, we investigate the absolute limits of these visual properties for visually guided position and speed control in Bombus terrestris. Our results indicate that the limit of spatial vision in the translational motion detection system of B. terrestris lies at 0.21 cycles deg−1 with a peak contrast sensitivity of at least 33. In the perspective of earlier findings, these results indicate that bumblebees have higher contrast sensitivity in the motion detection system underlying position control than in their object discrimination system. This suggests that bumblebees, and most likely also other insects, have different visual thresholds depending on the behavioral context

Mean Flight Data for Spatial Frequency and Contrast Experiments

This file contains the mean flight data (lateral position and 2D ground speed) for each flight in each of the experimental conditions presented in the paper. Please note that the Bombus terrestris data is taken from Chakravarti et al. 2017

Differences in spatial resolution and contrast sensitivity of flight control in the honeybees Apis cerana and Apis mellifera

Visually guided behaviour is constrained by the capacity of the visual system to resolve detail. This, in turn, is limited by the spatial resolution and contrast sensitivity of the underlying visual system. Because these properties are interdependent and vary nonuniformly, it is only possible to fully understand the limits of a specific visually guided behaviour when they are investigated in combination. To understand the visual limits of flight control in bees, which rely heavily on vision to control flight, and to explore whether they vary between species, we tested how changes in spatial resolution and contrast sensitivity affect the speed and position control of the Asian and European honeybees (Apis cerana and Apis mellifera). Despite the apparent similarity of these species, we found some interesting and surprising differences between their visual limits. While the effect of spatial frequency and contrast on position control is similar between the species, ground speed is differently affected by these variables. A comparison with published data from the bumblebee Bombus terrestris revealed further differences. The visual resolution that limits the detection and use of optic flow for flight control in both species of honeybee is lower than the previously anatomically determined resolution and differs from object detection limits of A. mellifera, providing evidence that the limits of spatial resolution and contrast sensitivity are highly tuned to the particular behavioural task of a species

Differences in spatial resolution and contrast sensitivity of flight control in the honeybees Apis cerana and Apis mellifera

Visually guided behaviour is constrained by the capacity of the visual system to resolve detail. This, in turn, is limited by the spatial resolution and contrast sensitivity of the underlying visual system. Because these properties are interdependent and vary nonuniformly, it is only possible to fully understand the limits of a specific visually guided behaviour when they are investigated in combination. To understand the visual limits of flight control in bees, which rely heavily on vision to control flight, and to explore whether they vary between species, we tested how changes in spatial resolution and contrast sensitivity affect the speed and position control of the Asian and European honeybees (Apis cerana and Apis mellifera). Despite the apparent similarity of these species, we found some interesting and surprising differences between their visual limits. While the effect of spatial frequency and contrast on position control is similar between the species, ground speed is differently affected by these variables. A comparison with published data from the bumblebee Bombus terrestris revealed further differences. The visual resolution that limits the detection and use of optic flow for flight control in both species of honeybee is lower than the previously anatomically determined resolution and differs from object detection limits of A. mellifera, providing evidence that the limits of spatial resolution and contrast sensitivity are highly tuned to the particular behavioural task of a species