Specific manipulation or systemic impairment? Behavioural changes of three-spined sticklebacks (Gasterosteus aculeatus) infected with the tapeworm Schistocephalus solidus

Talarico M., Seifert F., Lange J., Sachser N., Kurtz J., Scharsack J.

Abstract

Abstract: Manipulation of host behaviour by parasites to enhance transmission to the next host is a fascinating yet controversial phenomenon. This is because it is often hard to discriminate specific manipulation from unspecific side effects of the infection, i.e. a systemic impairment that could be due to a weakened general body condition. When infected with the tapeworm Schistocephalus solidus, stickleback fish swim closer to the water surface and exhibit reduced predation avoidance behaviour, which facilitates transmission of the tapeworm to the final host, most often a fish-eating bird. We here tested whether the behavioural changes of infected sticklebacks are specific to contexts where they would indeed enhance transmission, or rather more general. Therefore, we compared the behaviour of sticklebacks that were experimentally infected with S. solidus or left uninfected, in settings where the behaviour would influence parasite transmission to a high degree (response to a bird predator stimulus) or to a lesser extent (exploration of a new environment, activity while foraging). As expected, infected sticklebacks returned much faster to foraging after the bird predator stimulus and spent more time close to the water surface, compared to non-infected sticklebacks. By contrast, exploration of a new environment and activity while foraging did not differ between infected and non-infected sticklebacks. This suggests that alteration of the sticklebacks’ behaviour when infected with S. solidus is indeed due to specific manipulation of the predator avoidance behaviour and not a general, systemic impairment of infected sticklebacks. Significance statement: Manipulation of host behaviour by parasites is a fascinating but controversial phenomenon, since it is often difficult to disentangle if they are specifically induced or just a side effect of the infection. Stickleback fish, when infected with a tapeworm, change their behaviour dramatically; they swim closer to the water surface and reduce their escape behaviour, which exposes them to predation by birds, the final hosts of the parasite. We observed that sticklebacks infected with the tapeworm perform equally well as non-infected conspecifics in contexts with low relevance for parasite transmission, such as exploration of a new environment and foraging activity. However, the same infected sticklebacks exhibited the expected reduced escape behaviour when tested with a simulated bird attack. Our study suggests that the parasite specifically induces the sticklebacks’ behavioural changes and does not simply cause a systemic impairment.