Parasitized snails take the heat: a case of host manipulation?

Abstract

Infection-induced changes in a host's thermal physiology can represent (1) a generalized host response to infection, (2) a pathological side-effect of infection, or (3), provided the parasite's development is temperature-dependent, a subtle case of host manipulation. This study investigates parasite-induced changes in the thermal biology of a first intermediate host infected by two castrating trematodes (genera Maritrema and Philophthalmus) using laboratory experiments and field surveys. The heat tolerance and temperatures selected by the snail, Zeacumantus subcarinatus, displayed alterations upon infection that differed between the two trematodes. Upon heating, snails infected by Maritrema sustained activity for longer durations than uninfected snails, followed by a more rapid recovery, and selected higher temperatures in a thermal gradient. These snails were also relatively abundant in high shore localities in the summer only, corresponding with seasonal elevated microhabitat temperatures. By contrast, Philophthalmus-infected snails fell rapidly into a coma upon heating and did not display altered thermal preferences. The respective heat tolerance of each trematode corresponded with the thermal responses induced in the snail: Maritrema survived exposure to 40°C, while Philophthalmus was less heat tolerant. Although both trematodes infect the same tissues, Philophthalmus leads to a reduction in the host's thermal tolerance, a response consistent with a pathological side effect. By contrast, Maritrema induces heat tolerance in the snail and withstood exposure to high heat. As the developmental rate and infectivity of Maritrema increase with temperature up to 25°C, one adaptive explanation for our findings is that Maritrema manipulates the snail's thermal responses to exploit warm microhabitats.

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

“…Although this parasite targets fish as its next host, whereas the other two species we investigated presumably target arthropods, it is difficult to imagine how reduced snail movement (by only about 20%) could benefit the parasite for either intra‐host multiplication or successful cercarial transmission to fish. Species‐specific effects of trematodes on the physiology or morphology of their common snail host have been reported before, that is influences on shell shape (Hay, Fredensborg, & Poulin, ; Lagrue & Poulin, ) or thermal tolerance (Bates, Leiterer, Wiedeback, & Poulin, ) associated with certain trematode species but not others. However, without clear a priori predictions linking the phenotypic changes with transmission success in some trematodes but not in others, the most parsimonious explanation is that the changes are not adaptive for either the parasites or (given that snails are castrated by trematode infection) the host.…”

Gimme shelter – the relative sensitivity of parasitic nematodes with direct and indirect life cycles to climate change

“…also Fig. ), as has been documented in some cestodes (Macnab & Barber, ), trematodes (Bates et al ., ), and even malarial parasites (Fialho & Schall, ). Finally, the idea of a shelter effect likely also applies to any limiting factor that influences both host and parasite, not just temperature.…”

Some (worms) like it hot: fish parasites grow faster in warmer water, and alter host thermal preferences

“…Our results add to a growing body of research suggesting that host thermal preferences may be frequent targets of manipulative parasites. Marine snails ( Zeacumantus subcarinatus ) infected with Maritrema novaezealandensis trematodes – which attain infectivity more quickly at higher temperatures (Studer et al ., ) – become more heat tolerant than non‐infected conspecifics following infection and actively seek out warmer temperatures (Bates et al ., ), as do trypanosome‐infected sandflies, the vectors of reptile malaria. In the latter example, preferred higher temperatures speed up parasite development and hence the probability of transmission during the flies’ next blood meal (Fialho and Schall, ).…”