Critical role of parasite-mediated energy pathway on community response to nutrient enrichment

Abstract

Parasites form an integral part of food webs, however, they are often ignored in classic food web theory or limited to the investigation of trophic transmission pathways. Specifically, direct consumption of parasites by nonhost predators is rarely considered, while it can contribute substantially to energy flow in food webs. In aquatic systems, chytrids constitute a major group of fungal parasites whose free-living infective stages (zoospores) form a highly nutritional food source to zooplankton. Thereby, the consumption of zoospores can create an energy pathway from otherwise inedible phytoplankton to zooplankton ("mycoloop"). This parasite-mediated energy pathway might be of special importance during phytoplankton blooms dominated by inedible or toxic primary producers like cyanobacteria, which are on the rise with eutrophication and global warming. We theoretically investigated community dynamics and energy transfer in a food web consisting of an edible nonhost and an inedible host phytoplankton species, a parasitic fungus, and a zooplankton species grazing on edible phytoplankton and fungi. Food web dynamics were investigated along a nutrient gradient contrasting nonadaptive zooplankton species representative for filter feeders like cladocerans and zooplankton with the ability to actively adapt their feeding preferences like many copepod species. Overall, the importance of the mycoloop for zooplankton increases with nutrient availability. This increase is smooth for nonadaptive consumers. For adaptive consumers, we observe an abrupt shift from an almost exclusive preference for edible phytoplankton at low nutrient levels to a strong preference for parasitic fungi at high nutrient levels. The model predicts that parasitic fungi could contribute up to 50% of the zooplankton diet in nutrient-rich environments, which agrees with empirical observations on zooplankton gut content from eutrophic systems during blooms of inedible diatoms or cyanobacteria. Our findings highlight the role of parasite-mediated energy pathways for predictions of energy flow and community composition under current and future environmental change.

Keywords: adaptive preference; energy flow; food web; mycoloop; parasites; parasite‐mediated energy pathway; parasitic fungi.