Since its foundation from the Lotka-Volterra model in the early twentieth century, predator–prey theory has increasingly recognized the role of behavior and bioenergetics as drivers of trophic interactions and the dynamics of populations and ecosystems ( Holling, 1966 Abrams, 1984, 2010 Yodzis and Innes, 1992 Lima, 1998 Kondoh, 2003 Schmitz et al., 2004 Rooney et al., 2006 Loeuille, 2010 Valdovinos et al., 2010). Predation is one of the most important ecological interactions, determining the flow of energy and matter in nature, and imposing selective pressures that shape the evolution of organism traits and their distribution in ecological communities ( Elton, 1927 Lindeman, 1942 Paine, 1966 Sih et al., 1985 Vermeij, 1994 Abrams, 2000 Estes et al., 2011 Rossberg, 2013). Finally, besides having their own individual effects, metabolic responses have the potential to greatly alter, or even invert, functional response-stability relationships, and therefore can be critical to an integral understanding of predation and its influence on population dynamics and persistence. These results have implications for any resource management approach that relies on models of food web dynamics, which is the case of many applications of ecosystem-based fisheries management. They can also buffer the effects of press perturbations, such as harvesting, on target populations and on their prey through top-down trophic cascades, but are expected to magnify bottom-up cascades, including the effects of nutrient enrichment or the effects of altering lower trophic levels that can be caused by environmental forcing and climate change. Negative metabolic responses – those resulting from decreases in foraging activity when more prey is available, and arguably the most common – lead to lower local stability of food webs and a faster pace of change in population sizes, including higher excitability, higher frequency of oscillations, and quicker return times to equilibrium when stable. Using analytical and numerical approaches, I show that missing this component of interaction has broad consequences for dynamical stability and for the robustness of ecosystems to persistent environmental or anthropogenic stressors. By ignoring the associated metabolic responses, these models violate the principle of energy conservation and likely underestimate the strength of predator–prey interactions. These adjustments are adaptive, ubiquitous in nature, and are implicitly assumed by models of predator–prey dynamics that impose consumption saturation in functional responses. It is analogous and intrinsically linked to the functional response, which is the change in consumption rate with prey density, as they are both shaped by adjustments in foraging activity. Here I define the metabolic response as the change in energy expenditure of predators in response to changes in prey density. It is much harder to observe and to measure than its beneficial counterpart, prey consumption, yet it is not inconsequential for the dynamics of prey and predator populations. The metabolic cost of foraging is the dark energy of ecological systems.
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