Photobehaviours guided by simple photoreceptor systems

Abstract

Light provides a widely abundant energy source and valuable sensory cue in nature. Most animals exposed to light have photoreceptor cells and in addition to eyes, there are many extraocular strategies for light sensing. Here, we review how these simpler forms of detecting light can mediate rapid behavioural responses in animals. Examples of these behaviours include photophobic (light avoidance) or scotophobic (shadow) responses, photokinesis, phototaxis and wavelength discrimination. We review the cells and response mechanisms in these forms of elementary light detection, focusing on aquatic invertebrates with some protist and terrestrial examples to illustrate the general principles. Light cues can be used very efficiently by these simple photosensitive systems to effectively guide animal behaviours without investment in complex and energetically expensive visual structures.

Keywords: Non-visual photoreception; Photokinesis; Photophobia; Phototaxis; Scotophobia.

Fig. 1

a Photophobia in sea urchin larvae. Bright light induces reversal of swimming direction via Opsin2 activation in arm mesenchymal cells. This inhibits the cholinergic neural signalling that regulates forward ciliary beating (Yaguchi et al. 2022). Larvae entering above-threshold levels of strongly illuminated surface waters will switch to backward swimming into deeper water. White dotted arrows indicate flow direction of the cilia and large blue arrows show the larva’s direction of travel. b Xenopus frog tadpoles swim actively under bright light, but when entering a darkened region such as the shadow of a lily pad, the pineal eye elicits an upward swimming response in the tadpole (Jamieson and Roberts 2000). This allows it to locate shaded vegetation on the surface, on which it prefers to attach. c Acroporid coral larvae swim actively in bright light. Hypothetical trajectories travelled over a fixed time period are represented by the blue lines behind the larvae. On sudden experiencing a sudden dimming of light intensity, they show a scotophobic response by slowing forward movement (Sakai et al. 2020). The average speed change is proportional to the intensity change, suggesting a photokinetic response mechanism. d Mutants lacking eyespots in the unicellular alga Chlamydomonas reinhardtii show a reversed phototactic response to light stimulation, relative to wild types that possess eyespots (Ueki et al. 2016). They are able to achieve this because the convex shape of the cell itself focuses light onto the cell wall photoreceptors region opposite from the light source, creating a focused area of stimulation. e The planula larva of the hydrozoan Clava multicornis swings its aboral front end (“head”) as it crawls along macroalgae substrates away from its parent. The “head” has two loose aggregations of RF-amide-expressing neurons (pink), which appear to be involved in intensity signal comparisons as the head sways side to side (Piraino et al. 2011). The side closest to the light (blue arrows) will receive more activation than the other side. The larva turns to and direct its crawling along an increasing light gradient, using the vector in which the average stimulation on both sides becomes equal (color figure online)

Fig. 2

Simplified behavioural assays (left) are depicted as viewed from above a shallow rectangular dish of water containing small motile aquatic animals. The apparatuses are designed to be used in ambient darkness with specified light stimuli that allow discrimination between different photobehaviours. On the right, light-seeking animals in the dish are represented by black dots and show the hypothetical distributions that would result from time spent exposed to the light stimuli provided. These assays can help to assess whether an organism has directional light-sensing capability or not. a One suggested method to confirm photokinetic or intensity gradient-following photobehaviour. A LED array provides even diffuse illumination from below, which is passed through a 2D linear gradient filter (or stepped neutral density gradient). Light-seeking animals that moderate swimming speed to light intensity or compare intensity over time as they travel through space, will accumulate on one side, whereas, an animal that “sees” light direction or images will not. b A point light source on one side produces a weak light gradient in all directions from the source, which photokinetic animals without directional light sensors can potentially follow to show a phototaxis-like response. Positively phototactic animals with directional sensors will accumulate close to the brightest spot. This design is often used experimentally assess light-seeking behaviour, but is unsuitable to verify true phototaxis. c To confirm directional light sensing or spatial vision and true phototaxis, a light stimulus must be collimated into a parallel beam using an aspheric lens, to illuminate the entire chamber evenly. This will remove intensity gradients and prevent photokinetic or gradient followers from accumulating on one side (color figure online)