HSS revisited: Bottom-up control in detritus food chains facilitates top-down control in grazing chains and greater omnivory across a productivity gradient

Background/Question/Methods

Ecologists have long sought to elucidate the effect of primary production on food web structure and function.  Classical theories hold that ecosystems are dominated by top-down trophic control (Green World Hypothesis) and that food chains are longer in more productive systems (Ecosystem Exploitation Hypothesis).  While the latter may be accurate when productivity is low, at high levels production may contribute to top-down suppression of intermediate consumers and omnivory may become prevalent, thus shortening food chains.  Moreover, these hypotheses are based largely on simple, linear representations of grazing pathways, and do not consider the existence of parallel and interconnected detritus-based pathways, nor that plant communities can become dominated by less edible species at high productivity.  In a simple extension of classical single-chain approaches, here we use empirical food web data from 23 marine systems to evaluate the effect of primary production on food web structure (the nature of trophic control, the edibility and fate of primary production, food chain length) in parallel grazing and detritus-based food chains linked by top predators.

Results/Conclusions

Across a productivity gradient we document bottom-up control in detritus-based food chains and top-down control in grazing chains, and an increasing reliance of top predators on detritus-based pathways.  These results support an Apparent Trophic Cascade hypothesis, in which donor-controlled bottom-up forcing in detritus pathways subsidizes top predator biomass, which in turn exerts top-down control in coupled grazing channels.  We find evidence of declining plant edibility with rising productivity, and document weakening herbivore control of plant biomass and a shift in the fate of primary production from grazing to detritus-based pathways across the productivity gradient.  Furthermore, and in agreement with recent theory, we document declining food chain length with increasing primary production; we show that this arises from greater omnivory, which manifests as a shift from carnivory to detritivory among consumers at intermediate trophic levels.  Our results testify to a fundamental role of detritus-based pathways in mediating food web responses to changing primary production, and suggest that a long-standing criticism of classical food web theories – the question of plant edibility – may in fact provide a mechanistic explanation for their prediction of top-down control.

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