Eyes and vision in Arion rufus and Deroceras agreste (Mollusca; Gastropoda; Pulmonata): What role does photoreception play in the orientation of these terrestrial slugs?

Abstract

Zieger, M.V., Vakoliuk, I.A., Tuchina, O.P., Zhukov, V.V. and Meyer-Rochow, V.B. 2009. Eyes and vision in Arion rufus and Deroceras agreste (Mollusca; Gastropoda; Pulmonata): What role does photoreception play in the orientation of these terrestrial slugs? -Acta Zoologica (Stockholm) 90 : 189-204This paper deals with the orientational behaviour in the two terrestrial slugs Arion rufus and Deroceras agreste . It presents anatomical details of their eyes and provides an appraisal of the eyes' optical system. In both species the retinae contain two principal types of cell: photoreceptive and pigmented supportive cells. While only the eye of A. rufus apparently contains neurosecretory neurones, that of D. agreste is the only one equipped with a small additional retina with its own separate lens. Lens shapes vary between ovoid ( A. rufus ) and spherical ( D. agreste ). Our results demonstrate that the camera-type eyes in A. rufus and D. agreste have optical systems that do not allow the production of a sharp image on the retina. The slugs demonstrate negative visually mediated phototactic behaviour, but no polarization sensitivity. Only one aspect of the visual environment, namely the overall distribution of light and dark, seems to be important for these slugs. As the main role of the slugs' photoreceptors is to monitor environmental brightness and to assist the animal in orientating towards dark places, we conclude that these slugs do not need to perceive sharp images.

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

“…We first confirmed the negative phototactic nature of the slugs (Crozier and Cole, 1929;Zieger et al, 2009;Matsuo et al, 2014;Fujisaki and Matsuo, 2017) in the light-dark choice group test (Fig. 1A).…”

“…However, spatial comparison of light intensity is expected to be difficult in the case of brain photoreception because of its small size and the blurring of images during light penetration through the body wall. Indeed, Zieger et al (2009) failed to detect negative phototaxis behaviour when blinded slugs (Arion rufus or Deroceras agreste) were made to choose the direction of movement to either side wall (covered with black or white paper) in the arena. This result supports the idea that the brain is not optimized for spatial analysis of the light intensity in the environment.…”

“…The terrestrial gastropod slug Limax valentianus is nocturnal, and avoids light places in order not to lose water from its body. To do this, the slugs have a well-developed lens eye on the tip of their superior tentacles (STs), which can detect light with high sensitivity (Kataoka, 1975;Suzuki et al, 1979;Zieger et al, 2009;Land and Nilsson, 2012;Matsuo et al, 2017). Therefore, the slugs exhibit negative phototaxis behaviour, which is driven by comparing the intensities of incident light coming into the bilateral eyes (Crozier and Cole, 1929;Matsuo et al, 2014).…”

Slugs (Arionidae) benefit from nocturnal artificial illumination

“…A positive phototaxis of slugs from surrounding areas to the light sources would have resulted in an increase in nocturnal catches at the illuminated site. Given the light avoiding behavior of slugs (Zieger et al., ) and the long period over which the increases in slug abundance are recorded (3 years), we believe that the contribution of this effect is likely small. Slugs are notorious for moving slowly, crossing 10.8 m per day on average (Grimm & Schaumberger, ).…”

“…ALAN can have direct and indirect effect on slugs. Slugs are known to be negatively phototactic (Zieger, Vakoliuk, Tuchina, Zhukov, & Meyer‐Rochow, ) and therefore might avoid the use of illuminated habitats at night. Some predators of slugs are also light avoiding (such as hedgehogs and slow worms), while others (e.g., carabid beetles) are visual hunters and might benefit from the increased visibility of slugs under ALAN.…”