Eye fluke infection changes diet composition in juvenile European perch (Perca fluviatilis)

Intraspecific diet specialization, usually driven by resource availability, competition and predation, is common in natural populations. However, the role of parasites on diet specialization of their hosts has rarely been studied. Eye flukes can impair vision ability of their hosts and have been associated with alterations of fish feeding behavior. Here it was assessed whether European perch (Perca fluviatilis) alter their diet composition as a consequence of infection with eye flukes. Young-of-the-year (YOY) perch from temperate Lake Müggelsee (Berlin, Germany) were sampled in two years, eye flukes counted and fish diet was evaluated using both stomach content and stable isotope analyses. Perch diet was dominated by zooplankton and benthic macroinvertebrates. Both methods indicated that with increasing eye fluke infection intensity fish had a more selective diet, feeding mainly on the benthic macroinvertebrate Dikerogammarus villosus, while less intensively infected fish appeared to be generalist feeders showing no preference for any particular prey type. Our results show that infection with eye flukes can indirectly affect interaction of the host with lower trophic levels by altering the diet composition and highlight the underestimated role of parasites in food web studies.

Altered neuronal activity in the visual processing region of eye-fluke-infected fish

Fish, like most vertebrates, are dependent on vision to varying degrees for a variety of behaviours such as predator avoidance and foraging. Disruption of this key sensory system therefore should have some impact on the ability of fish to execute these tasks. Eye-flukes, such as Tylodelphys darbyi, often infect fish where they are known to inflict varying degrees of visual impairment. In New Zealand, T. darbyi infects the eyes of Gobiomorphus cotidianus, a freshwater fish, where it resides in the vitreous chamber between the lens and retina. Here, we investigate whether the presence of the parasite in the eye has an impact on neuronal information transfer using the c-Fos gene as a proxy for neuron activation. We hypothesized that the parasite would reduce visual information entering the eye and therefore result in lower c-Fos expression. Interestingly, however, c-Fos expression increased with T. darbyi intensity when fish were exposed to flashes of light. Our results suggest a mechanism for parasite-induced visual disruption when no obvious pathology is caused by infection. The more T. darbyi present the more visual stimuli the fish is presented with, and as such may experience difficulties in distinguishing various features of its external environment.

Negative associations between parasite avoidance, resistance and tolerance predict host health in salmonid fish populations

Genetic variation in defence against parasite infections is fundamental for host–parasite evolution. The overall level of defence of a host individual or population includes mechanisms that reduce parasite exposure (avoidance), establishment (resistance) or pathogenicity (tolerance). However, how these traits operate and evolve in concert is not well understood. Here, we investigated genetic variation in and associations between avoidance, resistance and tolerance in a natural host–parasite system. Replicated populations of Atlantic salmon ( Salmo salar ) and sea trout (an anadromous form of brown trout, Salmo trutta ) were raised under common garden conditions and infected with the eye fluke Diplostomum pseudospathaceum . We demonstrate significant genetic variation in the defence traits across host populations and negative associations between the traits, with the most resistant populations showing the weakest avoidance and the lowest infection tolerance. These results are suggestive of trade-offs between different components of defence and possibly underlie the genetic variation in defence traits observed in the wild. Because the three defence mechanisms affect host–parasite evolution in profoundly different ways, we emphasize the importance of studying these traits in concert.

Limited impacts of chronic eye fluke infection on the reproductive success of a fish host

Parasitic infections may affect the reproductive success of the host either directly, through behavioural modification, or indirectly, by altering their reproductive investment in response to infection. We determined the effects of infection with the eye fluke Diplostomum pseudospathaceum (Trematoda) on the reproductive traits of European bitterling (Rhodeus amarus, Cyprinidae), an intermediate fish host with a resource-based mating system. Male bitterling infected by Diplostomum exhibited a larger but less pronounced red eye spot (sexually selected signal) than control males, suggesting that infected males were less preferred by females. The frequency of female ovulation and number of offspring were comparable between the infected and the control group, although there was a 1–2 week delay in the peak of ovulation and offspring production in infected fish, which is known to coincide with higher juvenile mortality. Chronic eye fluke infection had minimal metabolic costs (measured as oxygen consumption) and, consistent with these results, reproductive activity did not differ between infected and control fish in an experimental test of intersexual selection. Overall, the impact of eye fluke infection on the reproduction of European bitterling was limited. We consider the potential effect of favourable conditions during experiments (abundant food, access to spawning substrate and lack of predators and co-infections) on experimental outcomes and recognize that the effects of chronic eye fluke infection in natural conditions might be more pronounced.

Innate antipredator behavior can promote infection in fish even in the absence of predators

Natural enemies—predators and parasites—largely shape the dynamics of ecosystems. It is known that antipredator and antiparasite defense can be mutually conflicting, however consequences of this trade-off for the regulation of infection burden in animals are still poorly understood. We hypothesize that even in the absence of cues from predators, innate antipredator behavior (“ghost of predation past”) interferes with defense against parasites and can enhance the infection risk. As a case study, we explore interactions between a commercial species, the rainbow trout Oncorhynchus mykiss, and its parasite, the trematode eye-fluke Diplostomum pseudospathaceum. Fish–parasite interactions were tested in compartmentalized tanks where shelters and parasites were presented in different combinations providing various conditions for microhabitat choice and territorial behavior. Shelters were attractive and contestable despite the absence of predators and presence of parasites. The individuals fighting for shelters acquired more than twice the number of cercariae as compared to those in infected shelter-free compartments. Most infected were subordinate fish with a higher ventilation rate. Fish possessing shelters were less vulnerable to parasites than fighting fish. Grouping reduced the infection load, although less efficiently than sheltering. Our data demonstrate that the innate antipredator behavior can undermine antiparasite tactics of the fish and result in higher infection rates. Using our empirical results, we construct a mathematical model which predicts that enriching the environment in fish farming will be beneficial only when a large number of shelters is provided. Using insufficient number of shelters will increase the parasite burden in the fish.