Discussion

Our model results highlight the critical role of parasite-mediated trophic interactions for community response and the importance of energy flow through the mycoloop pathway along a nutrient gradient, and how this is modulated by zooplankton feeding strategies. Our analysis extends on existing theory (Miki et al. 2011) by taking non-linear feeding interactions and different zooplankton feeding strategies into account, representative for major feeding guilds, i.e. non-adaptive filter feeders like cladocerans vs. adaptive active hunters like raptorial copepods. While we observe a smooth increase in energy flow through the mycoloop pathway with nutrient enrichment for a non-adaptive zooplankton, for an adaptive zooplankton, our results suggest an abrupt shift from dominance of energy flow through the direct phytoplankton-zooplankton pathway at low nutrient levels (Regime I) to equal dominance of both pathways at high nutrient levels (Regime II). Our study specifically indicates that parasitic fungi can contribute 50% or more to the diet of zooplankton in nutrient rich environments with the dominance of inedible phytoplankton. This clearly exceeds predictions under the assumption of linear feeding interactions (Miki et al. 2011) and is supported by empirical observations showing that fungal zoospores can contribute 50-60% to the zooplankton diet during phytoplankton blooms dominated by inedible species (Rasconi et al. 2014).
A notable result is that the reachability of an optimal prey preference might be limited by the food web response, due to a trade-off between total prey biomass and relative contribution of the more profitable prey (fungi) to total prey. In contrast to indications from previous studies on optimal foraging on multiple prey (Visser and Fiksen 2013), our results show that optimality might not be reached before a critical threshold of relative and total prey availability is reached, which itself is constrained by the community response along the nutrient gradient. Furthermore, the comparison of biomass patterns for the fixed and the adaptive preference case shows that the optimization of net-energy gain does not necessarily maximize consumer biomass. Our results suggest that the co-dependence of relative and total prey availability and the negative correlation between alternative prey species effectively keeps the adaptive preference function from maximizing consumer biomass. It would be interesting to look at the general relevance of this finding for adaptive predation in natural, complex communities.
This study also adds new aspects to the importance of food web structure for food web dynamics (Drossel et al. 2001, O’Gorman et al. 2010) and how this is modulated by species specific rates (Gibert and DeLong 2017) and trait adaptation (Cattin et al. 2004). The community response pattern with an increase of all species along the mycoloop but a decrease of edible phytoplankton with increasing nutrient availability (non-adaptive case and Regime I) follows the dynamics predicted for food webs consisting of one chain of even and one chain of odd length, which are connected via a shared resource and a shared predator (Wollrab et al. 2012). Similar to predictions from classic food web theory on predator-mediated coexistence between competing prey species (Holt et al. 1994, Leibold 1996), we also observe a shift from dominance of exploitative to apparent competition for the mycoloop web, reflected by the initial dominance and successive decrease (increase) of the superior (inferior) resource competitor with nutrient enrichment. While inedible phytoplankton would profit from enrichment even in the absence of the mycoloop, in its presence, zooplankton gains additional energy which results in an increased predation pressure on edible phytoplankton. This highlights the relevance of general topological features also in the context of parasitic interactions.
Furthermore, a comparison between dynamic properties of the structurally equivalent plankton food web (Thingstad and Sakshaug 1990, Stibor et al. 2004, Wollrab and Diehl 2015), where ciliates are structurally at the same position as parasitic fungi in the mycoloop food web, provides new insight into the occurrence of abrupt shifts in community response along a nutrient gradient. For both webs, the occurrence of a regime shift in community response is critically related to the assumption of an adaptive feeding strategy of the consumer. The topologically constrained community response where ciliates/fungi increase with nutrient enrichment while the alternative prey decreases, leads to a disproportional (abrupt) shift in prey preference for ciliates/fungi along the nutrient gradient (Wollrab and Diehl 2015, Wollrab et al. 2020). Notably, in both cases this abrupt shift in prey preference creates a bottleneck in energy flow and leads to a drastic shift in community responses to further enrichment, which is absent if assuming a non-adaptive consumer (for further details see Appendix S5). This finding reveals the critical interplay of structural features, functional response type and production rates for occurrence of abrupt shifts in community composition along a nutrient gradient (see details in Appendix S5).
Our analysis of the mycoloop food web also supports the potentially stabilizing role of parasites for system dynamics (Lafferty et al. 2006, Rogawa et al. 2018), constituting weak links in comparison to classic predator-prey interactions due to differences in productivity (Johnson et al. 2010). The growth/infection rate of phytoplankton vs. parasite prey determines the amount of energy (biomass) that can be produced per unit of time. Given the large difference in phytoplankton growth vs. fungal infectivity rate in our study system, the path from edible phytoplankton to zooplankton can be characterized as a fast energy pathway, while the path from fungi to zooplankton can be considered as a slow energy pathway. Hence, with increasing preference for parasitic fungi, the slow energy channel stabilizes the oscillatory dynamics of the fast energy channel (Rooney et al. 2006, Blanchard et al. 2011, Gellner and McCann 2016, see also Appendix S3, Fig. S3.3). We have to caution that the observed stabilizing role of the mycoloop might partly be due to the simplified representation of the host-parasite interaction, which ignores the time lag between parasite infection and zoospore emergence. A more detailed description of the parasite-host interactions, separating infected from susceptible host, might to some extent counteract the stabilizing features.
Given the empirical counter part of our modeled system, our results are of high relevance with global warming not only increasing the risk of cyanobacterial blooms (Davis et al. 2009), but also the prevalence of parasitic infections (Harvell et al. 2002, Ibelings et al. 2011, Gsell et al. 2013). Based on direct phyto-zooplankton interactions, a decline in zooplankton would be expected with increasing dominance of inedible phytoplankton (Lampert 1987). However, our results suggest that this might be counteracted if parasites form an alternative food source for zooplankton (Kagami et al. 2007, Frenken 2018, Agha et al. 2018). Extending on existing theory (Miki et al. 2011) by taking non-linear feeding interactions and different zooplankton feeding strategies into account, our model analysis provides a more realistic prediction on the importance of energy flow along the mycoloop for major feeding guilds, i.e. non-adaptive filter feeders like cladocerans vs. adaptive active hunters like raptorial copepods. Our study highlights that the dominant feeding guild might play a crucial role in the community response to environmental change. More generally our study suggests that taking parasitic interactions into account in a community context might be crucial to assess how environmental change will impact community response and trophic transfer efficiency. Additionally, the obtained limitations on optimal prey choice in the context of food web topology and corresponding community feedbacks have implications far beyond the investigated study system.