Double trouble: host behaviour influences and is influenced by co-infection with parasites

Parasitism is increasingly seen as an ecological factor contributing to behavioural variation among individuals. Yet, the causal direction of the relationship between animal personality and parasites remains unclear. We measured behavioural traits (i.e. exploration, activity, boldness) in pumpkinseed sunfish, Lepomis gibbosus, before and after an experimental infection using cages in a lake where sunfish were naturally exposed to trematode and cestode infection for 1 month. Despite our initial assumptions (i.e. that all individuals would have the same risk of infection within a cage), we found that initial behavioural traits strongly influenced infection susceptibility: initially bolder and less active fish acquired a higher density of trematode and cestode parasites during the infection period. Following infection, fish body condition decreased with increasing cestode density, suggesting that infection is costly to hosts. Body condition was positively correlated with distance moved, a measure of activity, regardless of individual infection status. The repeatability of exploration and activity behaviour and the strength of the activity–exploration correlation (i.e. behavioural syndrome) were reduced following parasite exposure. Distance moved and trematode density were negatively correlated, suggesting that this infection decreases host activity levels. Since trematodes have a complex life cycle with piscivorous birds as a final host, a decrease in activity following infection may make infected fish more susceptible to bird predation, benefiting the parasite. Our results highlight the close links between behaviour and parasitism. We propose that two mechanisms may simultaneously operate: initial host behaviour influences their risk of infection, and infection introduces variation in the behavioural traits of infected hosts.