Risky business: influence of eye flukes on use of risky microhabitats and conspicuousness of a fish host

Abstract

A prerequisite for a parasitic manipulation to be considered adaptive is that it confers a fitness benefit to the parasite, such as increased transmission to another host. These manipulations can involve alterations to a wide range of host phenotypic traits, including microhabitat choice. Eye flukes of the trematode family Diplostomidae use fish as intermediate hosts and must be transmitted by predation to a piscivorous bird. In New Zealand, the diplostomid Tylodelphys darbyi infects the eyes of a widespread endemic freshwater fish, the common bully Gobiomorphus cotidianus. Within the eye, T. darbyi metacercariae achieve large sizes and move freely about the aqueous and vitreous humors of the eye. We hypothesized that higher intensities of T. darbyi would (i) cause bullies to show increased activity and spend more time moving about in open space (i.e., more conspicuous, risky microhabitat) and (ii) reduce their ability to compete for shelter with fish harboring lower infection levels. Our experiments showed that heavily infected fish were more active and spent more time in the open, although the effect was age-dependent, with immature fish displaying decreases in activity and time spent in the open with increasing intensities of infection. We also demonstrated that heavily infected female bullies have a lower probability of using shelter, but males show the opposite pattern. It is possible that using more risky microhabitats increases the likelihood of the fish being eaten by the parasite’s predatory avian definitive hosts. However, our findings indicate that age- and sex-dependent effects call for a more nuanced interpretation.