Parasite infection disrupts escape behaviours in fish shoals.

Many prey species have evolved collective responses to avoid predation. They rapidly transfer information about potential predators to trigger and coordinate escape waves. Predation avoidance behaviour is often manipulated by trophically transmitted parasites, to facilitate their transmission to the next host. We hypothesized that the presence of infected, behaviourally altered individuals might disturb the spread of escape waves. We used the tapeworm Schistocephalus solidus, which increases risk-taking behaviour and decreases social responsiveness of its host, the three-spined stickleback, to test this hypothesis. Three subgroups of sticklebacks were placed next to one another in separate compartments with shelter. The middle subgroup contained either uninfected or infected sticklebacks. We confronted an outer subgroup with an artificial bird strike and studied how the escape response spread through the subgroups. With uninfected sticklebacks in the middle, escape waves spread rapidly through the entire shoal and fish remained in shelter thereafter. With infected sticklebacks in the middle, the escape wave was disrupted and uninfected fish rarely used the shelter. Infected individuals can disrupt the transmission of flight responses, thereby not only increasing their own predation risk but also that of their uninfected shoal members. Our study uncovers a potentially far-reaching fitness consequence of grouping with infected individuals.

Parasite-infected sticklebacks increase the risk-taking behaviour of uninfected group members.

Trophically transmitted parasites frequently increase their hosts' risk-taking behaviour, to facilitate transmission to the next host. Whether such elevated risk-taking can spill over to uninfected group members is, however, unknown. To investigate this, we confronted groups of 6 three-spined sticklebacks, Gasterosteus aculeatus, containing 0, 2, 4 or 6 experimentally infected individuals with a simulated bird attack and studied their risk-taking behaviour. As a parasite, we used the tapeworm Schistocephalus solidus, which increases the risk-taking of infected sticklebacks, to facilitate transmission to its final host, most often piscivorous birds. Before the attack, infected and uninfected individuals did not differ in their risk-taking. However, after the attack, individuals in groups with only infected members showed lower escape responses and higher risk-taking than individuals from groups with only uninfected members. Importantly, uninfected individuals adjusted their risk-taking behaviour to the number of infected group members, taking more risk with an increasing number of infected group members. Infected individuals, however, did not adjust their risk-taking to the number of uninfected group members. Our results show that behavioural manipulation by parasites does not only affect the infected host, but also uninfected group members, shedding new light on the social dynamics involved in host-parasite interactions.