Land snails can trap trematode cercariae in their shell: Encapsulation as a general response against parasites?

Abstract

Terrestrial gastropods are hosts of a wide variety of metazoan parasites and can respond to parasite exposure in various ways. One of these defence mechanisms, the ability to trap parasites in the host shell, was previously thought to apply only against nematodes. During a field survey along an urbanisation gradient, we found that the shell of Cornu aspersum and Cepaea nemoralis can contain encapsulated trematode cercariae, with prevalences of 7% and 1%, respectively over the entire sample, and up to 47% at the local population level. To our knowledge, this is the first case study unambiguously showing that land snails can trap non-nematode parasites in their shell at non-negligible prevalences. Shell-encapsulation could be a more general defence mechanism than previously described, and more studies are needed to understand its importance and variability.

UrbanCepaea nemoralissnails are less likely to have nematodes trapped within their shells

“…We then broke each shell into fragments using forceps, examined fragments under a binocular microscope, and recorded all animals found encapsulated within the shell as in e.g. Gérard et al (2023). A total of 606 nematodes were found in 104 shells; no other metazoan parasites were recorded.…”

“…This ability seems phylogenetically widespread, even present in slugs with vestigial shells (Rae et al, 2008; Rae, 2017), and could therefore provide a relatively easy to access record of ecological interactions. Following anecdotal records of mites and trematodes encapsulated in shells, it has further been suggested that this shell encapsulation might extend to other metazoan parasites (Dahirel et al, 2022; Gérard et al, 2023). However, given how rare these non-nematode records are, they may be merely by-products of a defence mechanism targeted towards nematodes, rather than evidence of a more generalized defence response (Gérard et al, 2023).…”

“…Following anecdotal records of mites and trematodes encapsulated in shells, it has further been suggested that this shell encapsulation might extend to other metazoan parasites (Dahirel et al, 2022; Gérard et al, 2023). However, given how rare these non-nematode records are, they may be merely by-products of a defence mechanism targeted towards nematodes, rather than evidence of a more generalized defence response (Gérard et al, 2023). The few snail species in which this phenomenon has been studied across multiple populations show that the prevalence of individuals trapping nematodes can vary widely between sites (Rae, 2017; Rae, 2018; Cowlishaw et al, 2019), but there has been no attempt, to our knowledge, to assess whether this variation could be non-random with respect to environmental context.…”

“…To that end, we combine here publicly available and standardized urbanization metrics with observations of field-collected snails across three cities in Belgium, using the grove snail Cepaea nemoralis (Gastropoda, family Helicidae) as a model. Like other helicids, C. nemoralis can encapsulate and trap parasitic nematodes in its shell (Williams & Rae, 2016; Rae, 2017; Dahirel et al, 2022; Gérard et al, 2023). This snail is also common both outside and within cities (Kerstes et al, 2019), and therefore a very suitable model to study variation in encapsulation rates, whether it is due to urbanization or to spatial (between-cities) differences.…”