Risk-taking behaviour in African killifish – a case of parasitic manipulation?

Abstract

Parasites commonly manipulate host behaviour to increase transmission success between hosts. While most behavioural changes comprise slight alterations to host activity patterns and habitat use, some represent impressive alterations to routine behaviour which, while having direct positive effects on parasite transmission, compromise host survival. Here, we report conspicuous risky behaviour in an African annual killifish, Nothobranchius furzeri, infected by metacercariae of a strigeid trematode, Apatemon sp., residing in their cranial cavity. We demonstrate a striking contrast in the spatial and temporal behavioural responses of fish from populations naturally infected with Apatemon sp. and fish from two control populations with either a similar baseline parasite fauna but lacking Apatemon, or an overall low-level of infection. During routine activity, fish from Apatemon-infected populations positioned themselves just below the water surface, while other fish spent most of their time near the bottom. During a simulated avian attack, killifish from Apatemon-infected populations jumped above the water surface, moved in an uncoordinated manner, and rotated in the upper water layer, while fish from the control populations rapidly escaped into deeper water and ceased moving. The same self-exposing behaviour (jumping out of the water and lying on floating lily pads for extended periods) was also observed under natural conditions. Such behaviour greatly facilitates location of Apatemon-infected host fish by avian definitive hosts, especially in turbid pools. Moreover, the nothobranchiid killifish host's own life history, i.e. an extremely short lifespan limited to several months, may represent an important driver in the evolution of behavioural manipulation.