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.

Synergistic effects of predation and parasitism on competition between edible and inedible phytoplankton

“…Furthermore, corresponding to previous theoretical work [11], our experimental results indicate that insight from studies on single interaction types might be misleading for assessing effects of multiple interaction types on community dynamics and its ecological consequences. Our study experimentally demonstrated that the effects of parasitic fungi on community composition are different depending on community composition, nutrient availability and physiological parameters, as has been suggested verbally or theoretically [6][7][8]17], and we specified the additive and synergistic effects. Thus, our study illuminates the ecological role of "dark-matter" fungi on short-term food web dynamics beyond existing knowledge.…”

“…In addition, if inedible phytoplankton becomes infected, the produced fungal zoospores can provide an alternative food source for zooplankton as they couple primary and secondary production through the mycoloop [16]. Thus, the mycoloop potentially affects population dynamics and composition of plankton communities not only directly but also indirectly via changing the energy transfer pathway [17]. To our knowledge, no empirical study has directly demonstrated how the mycoloop affects plankton community composition and dynamics in an experimental community.…”

The chytrid insurance hypothesis: integrating parasitic chytrids into a biodiversity–ecosystem functioning framework for phytoplankton–zooplankton population dynamics

“…The mycoloop hypothesis has been subject to population modelling to evaluate scenarios and explore population dynamics (Grami et al 2011 ; Miki et al 2011 ; Kagami et al 2014 ; Frenken et al 2020a ; Frenken et al 2020b ; Thongthaisong et al 2022 ). In a pioneering paper, Miki et al ( 2011 ) found that although the mycoloop could have positive effects on zooplankton production, the overall impact could be negative if zooplankton growth efficiency was lower when feeding on chytrids than on small algae (Fig.…”

“…In more recent models, parasitism by chytrids was found to alleviate competition amongst edible phytoplankton, increasing zooplankton production (Kagami et al 2014 ). High zooplankton densities can also reduce chytrid transmission (through consuming free-living infective zoospores) and overgraze edible algae, favouring the growth of inedible phytoplankton that can then feedback to depress the zooplankton population (Kagami et al 2014 ; Thongthaisong et al 2022 ). Although modelling indicates that the mycoloop predominantly influences blooms (Thongthaisong et al 2022 ), this might relate to modelling assumptions that nutrients are not recycled in the system through zooplankton excretion and death.…”

“…High zooplankton densities can also reduce chytrid transmission (through consuming free-living infective zoospores) and overgraze edible algae, favouring the growth of inedible phytoplankton that can then feedback to depress the zooplankton population (Kagami et al 2014 ; Thongthaisong et al 2022 ). Although modelling indicates that the mycoloop predominantly influences blooms (Thongthaisong et al 2022 ), this might relate to modelling assumptions that nutrients are not recycled in the system through zooplankton excretion and death. Model outcomes, thus, may hinge on critical details about how the mycoloop system is defined mathematically.…”