Critical role of parasite-mediated trophic interactions for energy flow and community dynamics

Parasites form an integral part of food webs, however, mechanistic insights into the role of parasites for energy flow and community dynamics is currently limited by a lack of conceptual studies investigating host-parasite interactions in a community context. In aquatic systems, chytrids constitute a major group of fungal parasites and their free-living infective stage (zoospores) forms a highly nutritional food source to zooplankton. Consumption of zoospores can create an energy pathway from otherwise inedible phytoplankton to zooplankton (“mycoloop”). The impact of such parasite-mediated energy pathways on community dynamics and energy transfer to higher trophic levels is of high importance considering eutrophication and global warming induced shifts to dominance of unfavourable prey such as cyanobacteria. We theoretically investigated community dynamics and energy transfer in a food web consisting of an edible-nonhost and an inedible-host phytoplankton species, a fungal parasite, and a zooplankton species grazing on edible phytoplankton and fungi. Food web dynamics were investigated along a nutrient gradient for two cases: (1) non-adaptive zooplankton species representative for filter feeders like cladocerans and (2) zooplankton with the ability to actively adapt their feeding preferences like many copepod species. For both feeding strategies, the importance of the mycoloop for zooplankton increases with nutrient availability. This increase is smooth for non-adaptive consumers. For a consumer with an adaptive feeding preference, we observe an abrupt shift from almost exclusive preference for edible phytoplankton (dominant prey) at low nutrient levels to a strong preference for parasitic fungi at high nutrient levels. The model predicts that parasitic fungi can contribute up to 50% of the zooplankton diet in nutrient rich environments, agreeing with empirical observations on zooplankton gut content from eutrophic systems during cyanobacterial blooms. Our findings highlight the role of parasite-mediated energy pathway for predictions on energy flow and community composition under environmental change.