Parasite-associated phenotype modifications in threespine stickleback

The threespine stickleback fish, Gasterosteus aculeatus, is parasitized by the tapeworm Schistocephulus solidus in freshwater habitats. The competency of the parasite to infect a definitive host, one of many piscivorous birds, is associated with behavioral changes in parasitized stickleback that are likely to increase the chance of transmission to a definitive host. Over a limited geographical range, large tapeworm size is also associated with demelanization, a phenotypic change in the stickleback host that involves a dramatic loss of melanin in the skin and, simultaneously, a darkening of the eve. We demonstrate that stickleback harboring a worm large enough to be infective to a definitive host exhibit behavioral shifts likely to enhance transmission, but that these changes are substantially magnified in demelanized individuals, all of which were infected by large tapeworms. The results were similar whether we used a model of a bird flown over an aquarium, or a preserved trout moved to simulate attack under field conditions. Because changes in the levels of response to both kinds of predators were similar, we infer that behavioral modifications that enhance susceptiblity to visually hunting predators that are definitive hosts also enhance susceptibility to visually hunting predators (e.g. trout) that are not. In lakes where predatory fishes are common, the impact on S. solidus transmission could be substantial. Although other studies have suggested that positive buoyancy, forcing infected fish to remain near the surface, is one cause of these behavioral shifts, we detected no differences in water column position among unparasitized and parasitized classes of stickleback. Instead, infected stickleback appeared to move sluggishly and were less likely to respond to simulated attacks than were uninfected fish, and the behavioral shift was most dramatic in demelanized stickleback.