Monoxenous and heteroxenous parasites of fish manipulate behavior of their hosts in different ways

Adaptive host manipulation hypothesis is usually supported by case studies on trophically transmitted heteroxenous endoparasites. Trematodes and cestodes are among efficient manipulators of fish, their common intermediate hosts. In this review paper, new data on modifications of host fish behavior caused by monoxenous ectoparasitic crustaceans are provided together with a review of effects caused by heteroxenous parasites. Differences in modifications of host behavior caused by heteroxenous and monoxenous parasites are discussed. Manipulation by heteroxenous parasites enhances availability of infected fish to predators definitive hosts of the parasites. Fine-tuned synchronization of modified anti-predator behavior with a certain phase of the trematode Diplostomum spathaceum development in the eyes of fish, their second intermediate host, was shown. Modifications of behavior are habitat specific. When juvenile salmonids are in the open water, parasites impair their cooperative anti-predator behavior; in territorial bottom-dwelling salmonids, individual defense behavior such as sheltering is the main target of manipulation. It was shown that monoxenous ectoparasitic crustaceans Argulus spp. decreased motor activity, aggressiveness and increased shoal cohesiveness of infected fish. Such a behavior facilitates host and mate searching in these parasites, which often change their hosts, especially during reproduction. Reviewed experimental data suggest that heteroxenous parasites manipulate their host mainly through impaired defense behavior, e.g. impairing shoaling in fish. Alternatively, monoxenous parasites facilitate shoaling that is profitable for both parasites and hosts. Coordination of modified host behavior with the parasite life cycle, both temporal and spatial, is the most convincing criterion of the adaptive value of host manipulation.