The effects of size, reproductive condition, and parasitism on foraging behaviour in a freshwater snail, Potamopyrgus antipodarum

Predation risk is expected to affect the foraging behaviour of individual prey according to their size, sex and reproductive condition. Parasites may also affect the foraging behaviour of their hosts, due to increased energetic demands imposed by the parasite, or due to a parasite strategy to increase the likelihood of its transmission to the next host. Field studies were conducted to determine the effects of size, reproductive condition and trematode infection on foraging behaviour in a freshwater snail, Potamopyrgus antipodarum. Among uninfected snails, small individuals (<3.8 mm in length) foraged more than large individuals during daylight hours when the risk of predation is greatest; non-brooding adult females foraged more during the day than females that were brooding embryos. These results suggest that juveniles and non-brooding females trade off the risk of predation with the energy required for growth and reproduction, respectively. Infection by a digenetic trematode (Microphallus sp.) also caused significant changes in snail behaviour. This trematode has a two-host life cycle. Snails are the intermediate host, and ducks are the final host. Encysted parasite larvae are transmitted to ducks when they ingest snails infected with mature larval cysts. Results showed that snails infected by encysted, transmissible larvae foraged in the early morning hours, and retreated under rocks during the late morning. In contrast, snails infected by unencysted non-transmissible larvae retreated to positions under rocks in the early morning, and mirrored the risk-averse strategy of brooding females. These results suggest that, when the parasite larvae encyst and become transmissible to the final host, they induce the snails to forage later into the morning. Because foraging by waterfowl is greatest in the early morning, encysted larvae may manipulate snail behaviour to increase the likelihood of their transmission to the final host. ? 1996 The Association for the Study of Animal Behaviour Increasing evidence shows that parasites can significantly influence an individual’s behaviour (for reviews see Holmes & Bethel 1972; Dobson 1988; Moore & Gotelli 1990; Combes 1991). The foraging habits of individuals may be especially prone to alteration by parasites because of the direct and indirect influences of parasitism (Moore & Gotelli 1990). Parasites decrease foraging efficiency in some species (Crowden & Broom 1980; Milinski 1985) and increase it in others (Williams & Gilbertson 1983). Parasites may impose large nutritive demands upon the host, causing an increase in foraging to compensate (Lester 1971; Milinski 1985; Holmes & Zohar 1990); or they may alter host behaviours by causing tissue damage (Baudoin 1975; Holmes & Zohar 1990; Hurd 1990; Thompson & Kavaliers 1994). Parasites may also manipulate the behaviour of their hosts in very specific ways (for reviews see Holmes & Bethel 1972; Dobson 1988; Moore & Gotelli 1990; Coombes 1991). Behavioural manipulation is expected to be most common in intermediate hosts of trophically transmitted parasites, because natural selection should favour any change in behaviour that increases the transmission of the parasite to the next host in the life cycle (Rothschild 1962; Holmes & Bethel 1972). Examples of what appear to be behavioural manipulation are common in the literature (e.g. Hindsbo 1972; Bethel & Holmes 1973; Muzzall & Rabalais 1975; Moore 1983; Curtis 1987; Poulin et al. 1992; Hechtel et al. 1993; Lowenberger & Rau Correspondence: E. P. Levri, Department of Biology, Indiana University, Bloomington, IN 47405, U.S.A. (email: [email protected]). 0003–3472/96/040891+11 $18.00/0 ? 1996 The Association for the Study of Animal Behaviour