Abstract: How is parasite species diversity maintained? If different species are competing for shared host resources, then why is there not just one parasite that dominates every host niche? Maintenance of parasite diversity has historically taken a host-centric view. Yet, most parasites spend at least some portion of their life outside the host in a free-living stage, exposing them to the environment. Typically, competing parasite species adapt to different environments; such niche differentiation might allow coexistence across patches. However, what happens when environmental conditions get more extreme and less predictable? How do species that are unfavored by the environment sustain one bad patch after another and not go extinct? Storage effect (sensu Modern Coexistence Theory) predicts that fluctuation-dependent mechanisms like variation in local environment can be a major driver of coexistence. Fluctuations in local conditions can lead to temporary periods that are favorable to the rare species allowing their population to increase. Rare species then maintain viability until the average environment turns favorable. Here we translate classic ideas of species coexistence from storage effect theory into a parasitic realm. Using a combination of field-survey, field-mesocosms and modeling, we test the role of environmental fluctuations in maintaining the diversity of parasitic nematodes.
Our findings from a yearlong field survey and companion field-mesocosm experiment support that storage effect contributes to maintaining parasite diversity. Here we focus on two species of entomopathogenic nematode: Steinernema costaricense and kraussei. First, a year-long field survey, demonstrates the three conditions required for storage effect to operate (i) nematodes use their developmentally dormant phase to persist during environmentally unfavorable conditions (ii) species respond differently to environmental factors –S. costaricense is more strongly affected by temperature and moisture than S. kraussei (iii) species exhibit strong negative frequency dependence, promoting stabilization. Second, a field-mesocosm with minimal response surface design described the competition between the nematode species. Estimates of mean intra- and inter-specific competition coefficients establish low niche overlap between species indicating stable coexistence. Finally, partitioning the competition coefficients revealed covariance between competition and the environment. Specifically, competition limited growth more in environmentally favorable than unfavorable patches. The positive environment- competition covariance ensured that intra- specific competition will be stronger than the interspecific competition, a basic requirement for stabilized coexistence. Together, our results provide field-based evidence that environmental fluctuations via storage effect stabilize parasite community dynamics and contribute to the maintenance of parasite diversity in nature.
