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 whether 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.

The bumblebee (Bombus terrestris) has become a common model animal in the study of various aspects of vision and visually guided behavior. Although the bumblebee visual system has been studied to some extent, little is known about the functional role of the first visual neuropil, the lamina. In this work, we provide an anatomical and electrophysiological description of the first-order visual interneurons, lamina monopolar cells (LMCs), of the bumblebee. Using intracellular recording coupled with dye injection, we found that bumblebee LMCs morphologically resemble those found in the honeybee, although only the LMC type L1 cells could be morphologically matched directly between the species. LMCs could also be classified on the basis of their light response properties as spiking or non-spiking. We also show that some bumblebee LMCs can produce spikes during responses to stimulation with naturalistic light contrasts, a property unusual for these neurons.

Filtering properties of the membrane form an integral part of the mechanisms producing the light-induced electrical signal in insect photoreceptors. Insect photoreceptors vary in response speed between different species, but recently it has also been shown that different spectral photoreceptor classes within a species possess diverse response characteristics. However, it has not been quantified what roles phototransduction and membrane properties play in such diversity. Here, we use electrophysiological methods in combination with system analysis to study whether the membrane properties could create the variation of the response speed found in the bumblebee (Bombus terrestris) photoreceptors. We recorded intracellular responses from each photoreceptor class to white noise-modulated current stimuli and defined their input resistance and linear filtering properties. We found that green sensitive cells exhibit smaller input resistance and membrane impedance than other cell classes. Since green sensitive cells are the fastest photoreceptor class in the bumblebee retina, our results suggest that the membrane filtering properties are correlated with the speed of light responses across the spectral classes. In general, our results provide a compelling example of filtering at the sensory cell level where the biophysical properties of the membrane are matched to the performance requirements set by visual ecology.

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