Predation cues amplify the effects of parasites on the personality of a keystone grazer

Abstract

Abstract Parasites can alter species interactions either by modifying infected host behaviour or by influencing behavioural responses in uninfected individuals. Salt marsh ecosystems are characterized by a predator–prey interaction between the keystone grazer, Littoraria irrorata, and its main predator, Callinectes sapidus, both integral players in mediating the productivity of these habitats. Littoraria also acts as the first intermediate host for at least four species of digenetic trematode. Parasite infection has been shown to decrease grazing and climbing in populations of Littoraria, although effects on infected host response to predators have not been investigated. Moreover, how infection might increase or decrease among‐individual variation in behaviour (i.e. animal personality) is still unknown. Here we ask how trematode infection affects the expression of boldness in the anti‐predator responses of L. irrorata in both the absence and presence of a predator cue. We find that individual boldness varies substantially, and repeatability tends to increase as the number of stressors increases, with infected individuals exposed to a predator cue showing the strongest expression of behavioural types. Parasitism amplifies this effect, although the parasite itself does not appear to directly induce behavioural changes: infected snails show no evidence of decreased climbing or differences in refuge use as compared to their uninfected counterparts. Infection might therefore drive the expression of condition‐dependent personality differences evident only under high‐risk conditions. Group infection status strongly influenced behavioural reaction norms: uninfected individuals grouped with an infected snail were more responsive to predation risk, exhibiting increased climbing behaviour and spending less time in the water. Here parasites are influencing personality indirectly by inducing avoidance behaviours in healthy individuals, although only in high‐risk environments. The potential for exposure to parasites and predators fluctuates greatly across marsh ecosystems. Given the ecological importance of this predator–prey relationship, trematode infection can act as an important, although indirect, determinant of overall salt marsh community structure, health and function.