Discussion
Despite long-standing interest in food web energetics (after Lindeman
1942) and trophic cascades (after Hairston et al. 1960), research
on these two processes have been largely disconnected in the literature.
Energy transfer was considered mainly by ecosystem ecologists as a
diagram to understand ecosystem energetics and functioning (Chassotet al. 2010; Eddy et al. 2021), whereas trophic cascades
were widely adopted by community ecologists to understand population
dynamics (Layman et al. 2015; Jonsson 2017; Barbier & Loreau
2019). These two paradigms, however, address highly related processes of
the same ecosystem, so a unified framework has increasingly been
advocated by theoretical studies (DeBruyn et al. 2007; Barbier &
Loreau 2019). In line with these theoretical advances, our study
proposes to understand trophic cascades from an energetic perspective
and combines mesocosm experiments and food chain models to disentangle
two energetically relevant hypotheses. Our results showed strong
associations between trophic cascade strength and predator efficiency
but not with primary productivity (Fig. 5; Table S3, S4), supporting the
energy transfer hypothesis rather than the productivity hypothesis.
Thus, although primary productivity plays vital roles in food webs by
providing ultimate energy for all trophic species (Oksanen & Oksanen
2000; Post 2002), an impeded energy transfer could limit the biomass of
top predators and weaken their cascading effects (Mooney et al.2010; Kersch-Becker & Thaler 2015). These findings corroborate a recent
study on grassland experiments, where a decreased energy flow to
predatory beetles led to stronger suppressing effects of arthropod
herbivores on plants, i.e., weaker cascading effects (Barnes et
al. 2020).
In our experiment, the predator efficiency varies significantly among
mesocosms with different zooplankton community compositions. Mesocosms
dominated by D. magna (e.g., those initialized with D.
magna and D. brachyurum ) showed the highest predator efficiency
(Fig. 3c) and strongest trophic cascades. In comparison, mesocosms
dominated by other zooplankton species (e.g., those initialized withS. dorrii and D. brachyurum , or with all three zooplankton
species) showed lower predator efficiency and weaker trophic cascades in
spite of higher total zooplankton biomass (Fig. 2b). This may be
explained by the physical and chemical characteristics of D.
magna, making them better food sources for predators (Vincent et
al. 2020). Specifically, the lower motility of D. magna can
increase the attack rate of predators (Rall et al. 2012), and its
high body nutrient concentration can increase the assimilation
efficiency (DeMott et al. 1998). Therefore, the lower predator
efficiency may be attributed to the lack of high-quality resources in
mesocosms without D. magna , or low amount of high-quality
resources (i.e., lower biomass of D. magna ) in mesocosms with all
three zooplankton species (Fig. S3). These results highlight the
roles of species identity (O’Connor & Crowe 2005), rather than species
richness per se (Duffy 2002), in mediating the strength of trophic
cascades. Similar patterns have been reported for plant-herbivore
interactions, where a higher primary productivity driven by plant
diversity does not propagate to higher trophic levels due to the
presence of inedible or anti-herbivory plant species (Brett & Goldman
1997; Davis et al. 2010).
While nutrient supply had no significant impacts on trophic cascades, it
nevertheless imposed strong regulation on other processes of food webs.
In line with previous studies (Teurlincx et al. 2017; Zhou &
Declerck 2019), nutrient manipulations strongly shape the relative
abundance of zooplankton species (Fig. S3) as well as their biomass and
stoichiometry (Figs. 2a, S4). Moreover, the impaired performance of the
predator under LP treatments, e.g., low biomass, production, and body P
content, indicates a carryover effect of phytoplankton P limitation on
top trophic levels (Boersma et al. 2008). Interestingly, we found
that food chain efficiency (FCE) exhibited a unimodal pattern along the
gradient of nutrient supply (Fig. 3d). The lower FCE in LP than MP
treatments agrees with previous findings on the negative effects of
nutrient limitation (Dickman et al. 2008; Atkinson et al.2021). But with further P enrichment, FCE started to decline, due to the
relatively lower herbivore and predator efficiencies. This result may
suggest a disadvantages of high nutrients for food web efficiency
(Karpowicz et al. 2021), due to for example, differences in
responding magnitudes between primary producers and apex consumers to
nutrient enrichment (Fig. S2).
Our results may have useful
implications for natural resource management. In particular, the classic
biomanipulation approach for lake restoration is rooted in the theory of
trophic cascades, which assumed that addition of piscivorous fish
suppresses the biomass of planktivorous fish and releases the
herbivorous zooplankton, thus controlling algal biomass via grazing
(Carpenter et al. 1995). The importance of predator efficiency in
determining trophic cascades revealed in the present study suggests that
the biomanipulation approaches are most effective in systems with a
higher efficiency of energy flow into apex predators, whereas eutrophic
systems with low energy transfer efficiency may benefit weakly from the
manipulating practices of piscivores (Langeland 1990; Brett & Goldman
1996). In addition, our results also highlight the importance of trophic
interactions as drivers of ecosystem energy budgets, e.g., carbon
related functions (Strickland et al. 2013; Schmitz et al.2018; Wyatt et al. 2021). For example, elevated efficiencies of energy
transfer allowed increased biomass accumulation in apex consumers
(McCauley et al. 2018) and therefore stronger trophic cascades,
which may turn an ecosystem from carbon source into carbon sink (Schmitz
& Leroux 2020).