Introduction
Trophic cascades characterize the top-down effects of predators
propagating down trophic levels, which represent one of the most classic
paradigms in community ecology and have stimulated tremendous amount of
experimental and theoretical studies (Carpenter & Kitchell 1988; Poliset al. 2000; Carpenter 2010; Ripple et al. 2016). Mounting
evidence have demonstrated the prevalence of trophic cascades in nature
(Pace et al. 1999; Shurin & Seabloom 2005)
and their far-reaching impacts on
ecosystem functioning and services (Estes et al. 2011; Stricklandet al. 2013; Walsh et al. 2016; Stock et al. 2017).
Despite many previous studies to reveal various biotic and abiotic
factors that potentially influence the strength of trophic cascades
(Schmitz et al. 2004; Borer et al. 2005; Bruno & O’Connor
2005; Otto et al. 2008), the inconsistent outcomes, for example
the idiosyncratic effects of predator diversity (Bruno & O’Connor 2005;
Otto et al. 2008), suggest a continued uncertainty of its
ultimate mechanisms.
One long recognized potential
explanation is the productivity hypothesis, which predicts that the
strength of trophic cascades increases with primary productivity (Fig.
1a). Primary productivity provides the essential energy and elements for
upper trophic levels within a food web. Such bottom-up processes
determine not only the trophic position of the apex predator, i.e., food
chain length (Post 2002), but also the accumulation of its biomass
(Moore & De Ruiter 2012; Barbier & Loreau 2019). By supporting higher
biomass of apex predators, a higher primary productivity can potentially
trigger a stronger trophic cascade. This hypothesis, historically
illustrated as the ecosystem exploitation hypothesis (EEH) (Oksanenet al. 1981), has been supported by positive relationships
between primary productivity and trophic cascade strength found across
various studies (Wootton & Power 1993; Su et al. 2021). However,
evidence that does not support the relationship between primary
productivity and the strength of trophic cascades was also reported in
other studies (Borer et al. 2005). These contrasting findings are
striking as they have been found even within the same realm, e.g.,
freshwaters (Borer et al. 2005; Su et al. 2021).
An implicit assumption underlying the productivity hypothesis is
unimpeded
vertical energy fluxes, where energy fixed by primary producers can
reach higher trophic levels efficiently. This assumption, nevertheless,
rarely holds in nature (Lindeman 1942; DeBruyn et al. 2007). In
natural ecosystems, only a small proportion of energy from low trophic
levels can be converted into biomass of high trophic levels, due to
inefficiencies in food ingestion, assimilation, and biomass production
(Barneche & Allen 2018; Eddy et al. 2021). For instance, food
webs often involve many less edible plants (Oksanen & Oksanen 2000) or
anti-predative herbivores (Degerman et al. 2018), which can
significantly hamper vertical energy flow to apex predators (Stiboret al. 2004). Inefficiency in energy transfer can significantly
influence the biomass distribution of food webs (de Ruiter et al.1995; McCauley et al. 2018; Barbier & Loreau 2019) and thereby
alter the strength of trophic cascades (Heath et al. 2014;
Galiana et al. 2021). In particular, too low energy transfer may
decouple biomass production at higher
trophic levels from primary production, violating assumptions underlying
the productivity hypothesis (Brett & Goldman 1997; Davis et al.2010). In such cases, the strength of trophic cascade depends mainly on
the efficiency of energy transfer (energy transfer hypothesis; Fig. 1b),
rather than the amount of energy supply characterized by the primary
productivity. While the transfer efficiency hypothesis has been
formulated in mathematical models (DeBruyn et al. 2007), it has
not been tested explicitly.
In this study, we conduct a field mesocosm experiment, combined with
mathematical models, to test the aforementioned two hypotheses
underlying trophic cascades (i.e., the productivity hypothesis and
energy transfer hypothesis; Figure 1). We constructed mesocosms hosting
a three-level food chain and quantified the strength of trophic cascade
by simulating loss of top predator. We simultaneously manipulated
nutrient supply and zooplankton community composition to generate
variation in primary productivity and energy transfer efficiencies,
respectively. Because both primary productivity and energy transfer
processes are necessary for maintaining higher biomass of apex
predators, we expected a weakened relationship between primary
productivity (resp. energy transfer efficiency) and trophic cascade
strength when energy transfer efficiency (resp. primary productivity) is
impeded (Fig. 1). We end our discussion with scientific and practical
implications of our results.