Snails and their trails: the multiple functions of trail‐following in gastropods

Abstract

Snails are highly unusual among multicellular animals in that they move on a layer of costly mucus, leaving behind a trail that can be followed and utilized for various purposes by themselves or by other animals. Here we review more than 40 years of experimental and theoretical research to try to understand the ecological and evolutionary rationales for trail-following in gastropods. Data from over 30 genera are currently available, representing a broad taxonomic range living in both aquatic and terrestrial environments. The emerging picture is that the production of mucus trails, which initially was an adaptation to facilitate locomotion and/or habitat extension, has evolved to facilitate a multitude of additional functions. Trail-following supports homing behaviours, and provides simple mechanisms for self-organisation in groups of snails, promoting aggregation and thus relieving desiccation and predation pressures. In gastropods that copulate, trail-following is an important component in mate-searching, either as an alternative, or in addition to the release of water- or air-borne pheromones. In some species, this includes a capacity of males not only to identify trails of conspecifics but also to discriminate between trails laid by females and males. Notably, trail discrimination seems important as a pre-zygotic barrier to mating in some snail species. As production of a mucus trail is the most costly component of snail locomotion, it is also tempting to speculate that evolution has given rise to various ways to compensate for energy losses. Some snails, for example, increase energy intake by eating particles attached to the mucus of trails that they follow, whereas others save energy through reducing the production of their own mucus by moving over previously laid mucus trails. Trail-following to locate a prey item or a mate is also a way to save energy. While the rationale for trail-following in many cases appears clear, the basic mechanisms of trail discrimination, including the mechanisms by which many snails determine the polarity of the trail, are yet to be experimentally determined. Given the multiple functions of trail-following we propose that future studies should adopt an integrated approach, taking into account the possibility of the simultaneous occurrence of many selectively advantageous roles of trail-following behaviour in gastropods. We also believe that future opportunities to link phenotypic and genotypic traits will make possible a new generation of research projects in which gastropod trail-following, its multitude of functions and evolutionary trade-offs can be further elucidated.

Predation on invasive land gastropods by a Neotropical land planarian

“…The ability to detect and follow chemical trails left by the prey is demonstrated for the first time in a species of Geoplaninae. Such a behaviour was already observed in species of other subfamilies of land planarians such as Bipaliinae and Rhynchodeminae, using similar experiments (Fiore et al 2004;Winsor et al 2004;Iwai et al 2010), as well as in other predators of land gastropods, such as the predatory snail Euglandina rosea (Férrussac) and carabid beetles (Parakinen 1994;Holland et al 2012;Ng et al 2013). The presence of sensorial pits in the anterior region of the body of land planarians (Dendy 1891;Carbayo 2010) may be related to this ability to detect chemical trails.…”

Response of gastropod grazers to food conditions, current velocity, and substratum roughness

“…There are some strategies of snails to find attractive food patches. B. tentaculata selects for food quality (Brendelberger, 1997) and studies by Moelzner and Fink (2014) indicated that odours of biofilm food organisms may aid Lymnaea stagnalis in finding attractive biofilms and Ng et al (2013) showed that snails follow the mucus trails of other snails, a behavioural strategy that also may help to find attractive food patches.…”

The worm has turned: Behavioural drivers of reproductive isolation between cryptic lineages

“…Attractin, Temptin, Enticin and Seductin are small molecules that act as water-borne sex pheromones promoting mate attraction (Painter et al, 1998(Painter et al, , 2004Cummins et al, 2004). These pheromones were first described in the marine mollusc Aplysia (sea slug/sea hare), and in terrestrial snails where they are implicated in trail-following (Ng et al, 2013). The expression of Attractin and Temptin has been detected in the transcriptomes of earthworm tissues, including epidermis and digestive tract (Novo et al, 2013), forming physical and functional interfaces with the environment, thus suggesting that the behaviour-modulating molecules could be released through the mucus or faeces ("casts") to create a trail (Ressler et al, 1968) analogous to those in snails for the attraction of potential mates.…”