Light avoidance by non-ocular photosensing system in the terrestrial slugLimax valentianus

Abstract

Although the eye is the best-studied photoreceptive organ in animals, the presence of non-ocular photosensing systems has been reported in numerous animal species. However, most of the roles that nonocular photosensory systems play remain elusive. We found that the terrestrial slug Limax valentianus avoids light and escapes into dark areas even if it is blinded by the removal of the bilateral superior tentacle. The escape behaviour was more evident for short-wavelength light. Illumination to the head with blue but not red light elicited avoidance behaviour in the blinded slugs. Illumination to the tail was ineffective. The light-avoidance behaviour of the blinded slugs was not affected by the removal of the penis, which lies on the brain in the head, suggesting that the penis is dispensable for sensing light in the blinded slug. mRNA of Opn5A, xenopsin, retinochrome and, to a lesser extent, rhodopsin was expressed in the brain according to RT-PCR. Lightevoked neural responses were recorded from the left cerebro-pleural connective of the isolated suboesophageal ganglia of the brain, revealing that the brain is sensitive to short wavelengths of light (400-480 nm). This result is largely consistent with the wavelength dependency of the light-avoidance behaviour of the blinded slugs that we observed in the present study. Our results strongly support that the terrestrial slug L. valentianus detects and avoids light by using its brain as a light-sensing organ in the absence of eyes.

Visual afferents from an eye in the terrestrial slug Limax valentianus

“…Unexpectedly, we noticed that the immunoreactivity (IR) of Gqrhodopsin was detected in the terminal of optic nerves if the brain was fixed within 24 h after tracer incorporation (Figure 3), which is probably due to the high expression level of Gq-rhodopsin (Matsuo et al, 2019;Nishiyama et al, 2019). Gq-rhodopsin-IR was only found in the medial lobe of the optic neuropile (white arrow in the upper panels of Figure 3).…”

“…Slugs detect ambient light using not only their tentacular eyes but also their brain as a photosensor, although the possibility of dermal photosensing has also been proposed in the closely related pulmonate Lymnaea (Chono et al., 2002; Sunada et al., 2010). Thus, they can exhibit negative phototaxis behavior even if their bilateral eyes on the superior tentacle (ST) are removed (Nishiyama et al., 2019). We have previously demonstrated that the brain photoreceptors expressing Opsin5A (Opn5A), which constitutes a visual pigment, send projections to the contralateral optic neuropile through the cerebral commissure and form gap junctions between the terminals of retinal photoreceptors (Matsuo et al., 2020).…”

Beware glowing cadavers: bioluminescence of nematode symbiont Photorhabdus protects nematode-infected host cadavers from nocturnal scavengers

“…Most slugs are omnivorous, nocturnal scavengers that feed on dead vegetation, fungi, dead animals, and other detritus (Barnes and Weil, 1945;Jennings and Barkham, 1975;Keller and Snell, 2002). While they possess simple eyes (and certain light sensitive areas of the brain) that can detect light intensity, they do not form clear images (Zieger et al, 2009;Nishiyama et al, 2019) and seek food using olfactory cues (Gelperin, 1974;Gelperin, 1975;Kiss, 2017). Where organisms are protected in more than one modality, it can be difficult to disentangle the contribution of each modality to defence; artificial light sources are an important tool in demonstrating a defensive role of light where chemical defences are also effective (Underwood et al, 1997;Marek et al, 2011).…”

Plant volatiles mediated the orientation preference of slugs to different plant species

“…Field investigations revealed that slugs, including Arion lusitanicus , Deroceras reticulatum , and Arion distinctus , prefer to forage in dark conditions 16,17 . The light‐avoidance behavior of slugs makes their olfactory sense an indispensable sensory organ for locating food in dark conditions 16,18 . When slugs forage at night, volatiles released by plants can be perceived by slugs and help them discriminate host plants from non‐host plants, 19–22 therefore the volatiles from different plant species could be attractive or repellent.…”

“…16,17 The light-avoidance behavior of slugs makes their olfactory sense an indispensable sensory organ for locating food in dark conditions. 16,18 When slugs forage at night, volatiles released by plants can be perceived by slugs and help them discriminate host plants from non-host plants, [19][20][21][22] therefore the volatiles from different plant species could be attractive or repellent. Plant volatiles contain varied categories of chemicals, such as fatty acid derivatives, terpenes, phenylpropanoids, benzenoids, and so on.…”