The hairworm (Nematomorpha) Paragordius tricuspidatus has the ability to alter the behaviour of its terrestrial insect host (the cricket Nemobius sylvestris), making it jump into the water to reach its reproductive habitat. Because water is a limited and critical resource in the ecosystem, we predicted that hairworms should adaptively manipulate host behaviour to maximize parasite reproductive success. Our results supported the hypothesis that the host manipulation strategy of hairworms consists of at least two distinct steps, first the induction of erratic behaviour and then suicidal behaviour per se. Hairworms secured mating by starting to manipulate their host before being fully mature. Once induced, the cricket's suicidal behaviour was maintained until the host found water but the fecundity of worms decreased over time. As expected, the fecundity of worms was better in crickets with suicidal rather than erratic behaviour. (C) 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved