Behavioural impacts of trematodes on their snail host: Species‐specific effects or generalised response?

Abstract

Behavioural changes induced by parasites are extremely common, but their ultimate causes are often difficult to determine: they may represent adaptive manipulation by the parasite, adaptive responses by the host, or non‐adaptive side‐effects of infection. Contrasting the impacts of different parasites on the same host species offers an opportunity to test for species‐specific changes in host behaviour, which are less likely to be general side‐effects. Here, we tested the impacts of three trematode species (Apatemon sp. I, Plagiorchioid sp. I, and Maritrema poulini) on movement, microhabitat choice and responses to predator cues of their common intermediate host, the freshwater snail Potamopyrgus antipodarum. All three trematodes cause the castration of their host, and thus adaptive host responses to infection can be ruled out. In laboratory trials, snails infected with Apatemon sp. I moved a shorter total distance during the experimental period than uninfected control snails. However, all three trematode species similarly neutralised the attraction to lighted areas shown by uninfected snails, and none of the trematodes affected the time spent moving by their host or its responses to predator cues. Overall, there was little evidence for species‐specific effects on host behaviour by the three different trematode species in the same snail host. The single difference in induced behavioural change, involving one trematode species and one specific behavioural measure, is insufficient to reject the hypothesis that the behavioural impacts on the snail host are general and non‐adaptive by‐products of trematode infection.

The secretome of a parasite alters its host's behaviour but does not recapitulate the behavioural response to infection

“…Our results show that the secretome of S. solidus had significant effects on fish risky behaviour only in an allopatric (naive) population. This result is in accordance with the hypothesis that because allopatric sticklebacks did not evolve with S. solidus, they do not possess the adaptive 'generalized response' against S. solidus and its effects on fish physiology and behaviour, as proposed for this parasite and others [34,46]. Local adaptation and potential coevolution between the threespine stickleback and S. solidus was previously suggested with cross-infection studies [33,43,47].…”

The secretome of a parasite alters its host’s behaviour but does not recapitulate the behavioural response to infection

“…Our results show that the secretome of S. solidus had significant effects on fish risky behaviour only in an allopatric (naïve) population and that allopatric fish are therefore more sensitive to the secretome. These results are in accordance with the hypothesis that since allopatric sticklebacks did not co-evolve with S. solidus , they did not develop the adaptive “generalised response” against S. solidus and its effects on fish physiology and behaviour, as proposed for this parasite and others (43, 49, 62, 63). Local adaptation and potential co-evolution between the threespine stickleback and S. solidus was previously suggested with cross-infection studies (40, 43, 64).…”

Host preferences inhibit transmission from potential superspreader host species

“…All snails were collected in 2015 from the same 1 m 2 sites used to quantify focal host FOI in the field. We removed any snails that were shedding trematode cercariae on the day that they were brought into the laboratory, because trematodes may affect snail behaviour [34][35][36]. The remaining snails were randomly assigned to treatment groups and trials.…”