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.