Comparing cases of parasitism and predation that lead to victim death, parasites need more time to complete victim exploitation. This longer “interaction durability” delays energy transfer from host to parasite. During exploitation, parasite virulence differentiates the infected from the susceptible host dynamics. However, how this parasite characteristic influences the dynamics of their host and nonhost (insusceptible) species in the same community is largely unknown. Here, we use mathematical modelling to investigate the influence, exemplifying an experimental plankton community. In this community, nonhost zooplankton feeds on edible nonhost phytoplankton (resource competitor of the host) and parasite propagules released from infected inedible phytoplankton (“mycoloop” pathway). To assess the effects of parasite-host durability, we contrast parasite-host implementations as Lotka-Volterra predator-prey interaction (immediate energy transfer) with susceptible-infected (SI) host-parasite interactions. For the latter, parasite energy intake depends on infected host density but not susceptible hosts directly (delayed transfer). We further consider the difference between susceptible and infected host dynamics modulated by parasite virulence via its effect on host nutrient uptake. To assess the within-community effects, subcommunities are also investigated, excluding/including the parasite without/with the mycoloop. Our results show that, besides host elimination, longer interaction durability of the host-parasite interaction delays parasite attacks on susceptible hosts, allowing them to increase further (a hydra effect), independent of parasite virulence level. This effect observed in the isolated host-parasite systems is preserved in larger communities with negative consequences for the nonhost species, independent of the mycoloop. These theoretical results are supported by empirical observations within and beyond plankton realms. Our study reveals distinctive influences of parasites on community shot-term dynamics, which stem from the longer interaction durability.

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.