Introduction
Parasites are an integral but often neglected part of food webs (Lafferty et al. 2008, Sukhdeo 2012). Taking parasites into account increases biodiversity and food web complexity. Currently mechanistic insights into the role of parasites on energy flow and community response patterns to environmental change is limited by a lack of conceptual studies investigating host-parasite dynamics in a community context (Buck et al. 2015). Thereby, existing theoretical and experimental studies support the importance of investigating parasitic interactions in a community context to assess the direct and indirect effects of parasites on non-host species (Miki et al. 2011, Banerji et al. 2015, Prosnier et al. 2018). One direct link between host-parasite and predator-prey interactions is the consumption of parasites by higher order predators (Johnson et al. 2010). For multi-host parasites this forms an important transmission pathway, however, parasites with free-living life stages or ectoparasites can be prone to direct consumption resulting in death and digestion of the parasite (Johnson et al. 2010). Consumption of parasites can substantially contribute to energy flow in food webs (Michalska-Smith et al. 2018), especially if it creates a link from an otherwise inedible prey (host) to a predator (Johnson et al. 2010). Examples for such parasite-mediated trophic interactions are known for a wide range of animals from terrestrial as well as aquatic systems (see review by Johnson et al. 2010), such as ticks on mammal skin that are eaten by birds (Ndlovu and Combrink 2015), or earthworms feeding on parasitic flatworms on snail skin (Hobart et al. 2021), and zooplankton consumption of zoospores, the free living stage of parasitic chytrids which might emerge from, for example, infection of (inedible or toxic) cyanobacteria (Kagami et al. 2014) or infections on the skin of amphibians (Buck et al. 2011).
In this study we use an example from the aquatic environment to investigate the consequences of such parasite-mediated trophic interactions for energy flow and community response along a nutrient gradient. Parasitic chytrids, form a dominant group of parasites in aquatic systems (Grossart et al. 2019). The zoospores - the free living stage of parasitic chytrids infecting phytoplankton - can form a highly nutritional food source for zooplankton, even increasing the supply of polyunsaturated fatty acids (PUFAs) compared to phytoplankton, which is the primary food source for zooplankton (Kagami et al. 2007, Agha et al. 2016, Rasconi et al. 2020). Of special interest is the case where zooplankton consumption of zoospores creates an additional trophic pathway from otherwise inedible phytoplankton to zooplankton, the so called ‘mycoloop’ (Kagami et al. 2007, Miki et al. 2011). While dominance of inedible phytoplankton would typically be assumed to limit zooplankton growth and energy flow to higher trophic levels, the presence of the mycoloop can enhance zooplankton growth, thus increasing food availability for higher trophic levels (Rasconi et al. 2014). Specifically, in temperate regions, the mycoloop might regularly form an important energy source for zooplankton during the late summer season, when phytoplankton communities are typically dominated by less edible algae (Sommer et al. 2012). Furthermore, its importance may be on the rise with world-wide eutrophication and global warming leading to increasing dominance of - often inedible or even toxic - cyanobacteria (Huisman et al. 2018, Bogard et al. 2020).
Due to multiple feedbacks within the plankton community, the net effects of parasitic fungi on primary production, community composition and energy transfer are difficult to predict. While chytrid infection of inedible phytoplankton species could indirectly support edible-insusceptible phytoplankton species via decreasing resource competition, zooplankton consumption of zoospores may at the same time lead to increasing top-down pressure on edible phytoplankton (Miki et al. 2011, Kagami et al. 2014). The net effect of chytrid infections on community composition and energy transport in planktonic food webs may depend on the specific environmental context. Furthermore, the importance of the mycoloop for zooplankton (i.e., the relative contribution of fungi to net energy gain of zooplankton) will depend on the feeding strategy of the zooplankton and differs between non-adaptive (passive) filter feeders like cladocerans (Uszko et al. 2015) vs. adaptive (active) hunters like copepods (Meunier et al. 2016). Especially for copepods experimental results indicate that they might actively choose fungi over other (less nutritious) prey (Ray et al. 2016).
We theoretically investigated the importance of parasite mediated trophic interactions for community dynamics and its consequences for energy flow along a nutrient gradient, by using a simplified food web model. The food web consists of two groups of phytoplankton, edible vs. non-edible, competing for a shared resource, parasitic fungi specialized on inedible phytoplankton and zooplankton feeding on edible phytoplankton and parasitic fungi. Extending on previous work by Miki et al. (2011), we accounted for (more realistic) nonlinear food/nutrient uptake terms and different feeding strategies representative for dominant zooplankton groups, i.e. non-adaptive (passive) filter feeders like cladocerans (Uszko et al. 2015) vs. adaptive (active) hunters like copepods (Meunier et al. 2016). Our results show that, under the assumption of saturating food/nutrient uptake rates, the increasing importance of the mycoloop with nutrient enrichment is much more pronounced compared to assuming linear food uptake terms. While the importance of the mycoloop increases smoothly for a non-adaptive consumer, we observed an abrupt shift towards strong preference for parasitic fungi from low to high nutrient levels for zooplankton with adaptive prey preference. Our theoretical results emphasize the importance of parasite-mediated trophic interactions on community dynamics and trophic transfer efficiency and how this is modulated by consumer feeding strategies.