Movements in the dark : flying, landing and walking in insects

Flying, as well as walking insects rely on vision to regulate locomotion, even in the dark when the visual system is much less reliable. To manage visual control of these behaviours at low light intensities, many insects have evolved optical adaptations, such as larger facet lenses and wider rhabdoms, and neural adaptations, such as spatial and temporal summation, to increase their visual sensitivity.To investigate the effect of light intensity on flight control in crepuscular insects, I filmed bumblebees flying through an experimental tunnel at different light intensities. I found that bumblebees control their flight well even in dim light but fly slower as light levels fall. We also measured the effect of light intensity on the response speed of bee photoreceptors and found that they respond more slowly at lower light intensities. These results indicate that bumblebees compensate both behaviourally and visually to be able to fly in dim light.Next, I examined the final moments of landing in bumblebees by training them to land on a flat platform that could be rotated to different orientations. I found that bumblebees adjust their body and head posture depending upon the orientation of the platform and that leg extension occurred at a constant distance from the surface (except at low platform tilts). I also investigated the effect of light intensity on the landing precision in bumblebees while landing at the same platform at two different orientations and at different light intensities. I found that bumblebees perform well-controlled landings in dim light, however, as light intensity decreased, the bees oriented their body more vertically and their head more horizontally relative to the horizontal plane and extended their legs further away from the platform. These results indicate that bumblebees rely on visual cues to perform smooth landings even in dim light.Finally, to investigate how walking insects adapt to dim light, we analysed the orientation performance of diurnal and nocturnal dung beetles while rolling their dung balls from the centre to the periphery of a circular arena in the lab as well as in the field. We found that both species oriented well to a point light source, such as the moon or an artificial light. When only wide-field cues were present, such as starlight or the polarization pattern around the moon, the nocturnal beetles were much better oriented. Moreover, we found no effect of light intensity on ball-rolling speed, suggesting that these beetles do not employ temporal summation strategies, but rather a spatial summation approach to adapt to dim light.To summarize, the data presented in this thesis has broadened our knowledge about insect flight, landing, walking and orientation performance in dim light and has given insights into which adaptations they might use to meet the challenges of unreliable visual signals

Night sky orientation with diurnal and nocturnal eyes: dim-light adaptations are critical when the moon is out of sight

The visual systems of many animals feature energetically costly specializations to enable them to function in dim light. It is often unclear, however, how large the behavioural benefit of these specializations is, because a direct comparison in a behaviourally relevant task between closely related day- and night-active species is not usually possible. Here we compared the orientation performance of diurnal and nocturnal species of dung beetles, Scarabaeus (Kheper) lamarcki and Scarabaeus satyrus, respectively, attempting to roll dung balls along straight paths both during the day and at night. Using video tracking, we quantified the straightness of paths and the repeatability of roll bearings as beetles exited a flat arena in their natural habitat or under controlled conditions indoors. Both species oriented equally well when either the moon or an artificial point light source was available, but when the view of the moon was blocked and only wide-field cues such as the lunar polarization pattern or the stars were available for orientation, nocturnal beetles were oriented substantially better. We found no evidence that ball-rolling speed changed with light level, which suggests little or no temporal summation in the visual system. Finally, we found that both diurnal and nocturnal beetles tended to choose bearings that led them towards a bright light source, but away from a dim one. Our results show that even diurnal insects, at least those with superposition eyes, could orient by the light of the moon, but that dim-light adaptations are needed for precise orientation when the moon is not visible

The final moments of landing in bumblebees, Bombus terrestris.

In comparison to other insects, like honeybees, bumblebees are very effective pollinators. Even though landing is a crucial part of pollination, little is known about how bumblebees orchestrate the final, critical moments of landing. Here, we use high-speed recordings to capture the fine details of the landing behaviour of free-flying bumblebees (Bombus terrestris), while landing on a flat platform with different orientations. We find that the bees have a fairly constant body and head orientation at the moment of leg extension, irrespective of platform tilt. At the same moment in time, the distance to the platform is held constant at around 8 mm (with the exception of low platform tilts). The orientation of the antennae and the first appendage that touches the platform vary between platform orientations, while the duration of the hover phase does not. Overall, the final moments of landing in bumblebees and their close relatives, the honeybees, are similar. However, the distance to the platform at the moment of leg extension and the duration of the hover phase are different in bumblebees and honeybees, suggesting that they are primarily adapted to land on surfaces with different orientations

Bumblebees perform well-controlled landings in dim light

To make a smooth touchdown when landing, an insect must be able to reliably control its approach speed as well as its body and leg position—behaviors that are thought to be regulated primarily by visual information. Bumblebees forage and land under a broad range of light intensities and while their behavior during the final moments of landing has been described in detail in bright light, little is known about how this is affected by decreasing light intensity. Here, we investigate this by characterizing the performance of bumblebees, B. terrestris, landing on a flat platform at two different orientations (horizontal and vertical) and at four different light intensities (ranging from 600 lx down to 19 lx). As light intensity decreased, the bees modified their body position and the distance at which they extended their legs, suggesting that the control of landing in these insects is visually mediated. Nevertheless, the effect of light intensity was small and the landings were still well controlled, even in the dimmest light. We suggest that the changes in landing behavior that occurred in dim light might represent adaptations that allow the bees to perform smooth landings across the broad range of light intensities at which they are active

Effect of light intensity on flight control and temporal properties of photoreceptors in bumblebees.

To control flight, insects rely on the pattern of visual motion generated on the retina as they move through the environment. When light levels fall, vision becomes less reliable and flight control thus becomes more challenging. Here, we investigated the effect of light intensity on flight control by filming the trajectories of free-flying bumblebees (Bombus terrestris, Linnaeus, 1758) in an experimental tunnel at different light levels. As light levels fell, flight speed decreased and the flight trajectories became more tortuous but the bees were still remarkably good at centring their flight about the tunnel's midline. To investigate if this robust flight performance can be explained by visual adaptations in the bumblebee retina, we also examined the response speed of the green sensitive photoreceptors at the same light intensities. We found that the response speed of the photoreceptors significantly decreased as light levels fell. This indicates that bumblebees have both behavioural (reduction in flight speed) and retinal (reduction in response speed of the photoreceptors) adaptations to allow them to fly in dim light. However, the more tortuous flight paths recorded in dim light suggest that these adaptations do not support flight with the same precision during the twilight hours of the day