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.