Effects of parasites on fish behaviour: a review and evolutionary perspective

Fish serve as hosts to a range of parasites that are taxonomically diverse and that exhibit a wide variety of life cycle strategies. Whereas many of t hese parasites are passed directly between ultimate hosts, others need to n avigate through a series of intermediate hosts before reaching a host in (o r on) which they can attain sexual maturity. The realisation that parasites need not have evolved to minimise their impact on hosts to be successful, and in many cases may even have a requirement for their hosts to be eaten b y specific predators to ensure transmission, has renewed interest in the ev olutionary basis of infection-associated host behaviour. Fishes have proved popular models for the experimental examination of such hypotheses, and pa rasitic infections have been demonstrated to have consequences for almost e very aspect of fish behaviour. Despite a scarcity of knowledge regarding th e mechanistic basis of such behaviour changes in most cases, and an even lo wer understanding of their ecological consequences, there can be little dou bt that infection-associated behaviour changes have the potential to impact severely on the ecology of infected fishes. Changes in foraging efficiency , time budget, habitat selection, competitive ability, predator-prey relati onships, swimming performance and sexual behaviour and mate choice have all been associated with - and in some cases been shown to be a result of - pa rasite infections, and are reviewed here in some detail. Since the behaviou ral consequences of infections are exposed to evolutionary selection pressu res in the same way as are other phenotypic traits, few behavioural changes will be evolutionarily neutral and host behaviour changes that facilitate transmission should be expected. Despite this expectation, we have found li ttle conclusive evidence for the Parasite Increased Trophic Transmission (P ITT) hypothesis in fishes, though recent studies suggest it is likely to be an important mechanism. Additionally, since the fitness consequences of th e many behavioural changes described have rarely been quantified, their evo lutionary and ecological significance is effectively unknown. Potential hosts may also change their behaviour in the presence of infectiv e parasite stages, if they adopt tactics to reduce exposure risk. Such `beh avioural resistance', which may take the form of habitat avoidance, prey se lectivity or avoidance of infected individuals, can be viewed as behavioura l change associated with the threat of being parasitised, and so is include d here. Actually harbouring infections may also stimulate fishes to perform certain types of simple or complex behaviours aimed at removing parasites, such as substrate scraping or the visitation of cleaning stations, althoug h the efficacy of the latter as a parasite removal strategy is currently su bject to a good deal of debate. The effects parasites have on shoaling behaviour of host fish have attracte d a good deal of attention from researchers, and we have provided a case st udy to summarise the current state of knowledge. Parasites have been shown to affect most of the antipredator effects of shoaling (such as vigilance, co-ordinated evasion and predator confusion) and can also impair an individ ual's foraging ability. It therefore seems unsurprising that, in a number o f species avoidance of parasitised individuals has evolved which may explai n the occurrence of parasite-assorted shoals in the field. Parasitised fish are found more often in peripheral shoal positions and show a reduced tend ency for shoaling in some fish species. Given the array of host behaviours that may be changed, the fitness consequences of shoal membership for paras itised hosts and their parasites are not always easy to predict, yet an und erstanding of these is important before we can make predictions regarding t he ecological impact of infections on host fish populations. Clearly, there remain many gaps in our knowledge regarding the effects of p arasites on the behaviour of host fish. We believe that a much greater unde rstanding of the importance of infection-associated behaviour changes in fi sh could be gained from high quality research in comparatively few areas. W e have completed our review by highlighting the key research topics that we believe should attract new research in this field.