Species diversity reduces parasite infection through cross-generational effects on host abundance

With growing interest in the effects of biodiversity on disease, there is a critical need for studies that empirically identify the mechanisms underlying the diversity-disease relationship. Here, we combined wetland surveys of host community structure with mechanistic experiments involving a multi-host parasite to evaluate competing explanations for the dilution effect. Sampling of 320 wetlands in California indicated that snail host communities were strongly nested, with competent hosts for the trematode Ribeiroia ondatrae predominating in low-richness assemblages and unsuitable hosts increasingly present in more diverse communities. Moreover, competent host density was negatively associated with increases in snail species richness. These patterns in host community assembly support a key prerequisite underlying the dilution effect. Results of multigenerational mesocosm experiments designed to mimic field-observed community assemblages allowed us to evaluate the relative importance of host density and diversity in influencing parasite infection success. Increases in snail species richness (from one to four species) had sharply negative effects on the density of infected hosts (-90% reduction). However, this effect was indirect; competition associated with non-host species led to a 95% reduction in host density (susceptible host regulation), owing primarily to a reduction in host reproduction. Among susceptible hosts, there were no differences in infection prevalence as a function of community structure, indicating a lack of support for a direct effect of diversity on infection (encounter reduction). In monospecific conditions, higher initial host densities increased infection among adult hosts; however, compensatory reproduction in the low-density treatments equalized the final number of infected hosts by the next generation, underscoring the relevance of multigenerational studies in understanding the dilution effect. These findings highlight the role of interspecific competition in mediating the relationship between species richness and parasite infection and emphasize the importance of field-informed experimental research in understanding mechanisms underlying the diversity-disease relationship.     

How flexible is phenotypic plasticity? Developmental windows for trait induction and reversal

Inducible defenses allow prey to modulate their phenotypic responses to the level of predation risk in the environment and reduce the cost of constitutive defenses. Inherent in this statement is that prey must alter their phenotypes during development in order to form these defenses. This has lead many ecologists and evolutionary biologists to call for studies that examine developmental plasticity to provide insights into the importance of development in controlling the trajectories of trait formation, the integration of phenotypes over ontogeny, and the establishment of developmental windows for trait formation and reversal. By moving away from studies that focus on a single point in development, we can obtain a more complete understanding of the phenotypic decisions and limitations of prey. We exposed freshwater snails (Helisoma trivolvis) to environments in which predatory water bugs (Belostoma flumineum) were always absent, always present, or added and removed at different points in development. We discovered that snails formed morphological defenses against water bugs. Importantly, after the initial induction of defenses, snails showed similar developmental trajectories as snails reared without predators. Further, the snails possessed wide developmental windows for inducible defenses that extended past sexual maturity. However, being induced later in development appeared to have an associated cost (i.e., decreased shell thickness) that was not found when water bugs were always present. This epiphenotype (i.e., new shell formation as an extension of the current shell) suggests that resource limitation plays an important role in responses to temporal variation in predation risk and may have critical ecological costs that limit the benefits of the inducible defense. Lastly, the ability of snails to completely reverse their defenses was limited to early in ontogeny due to the constraints associated with modular growth of shell material. In sum, we demonstrate that taking a developmental perspective is extremely valuable for understanding the ecology of inducible defenses.