A mechanistic model of functional response provides new insights into indirect interactions among arctic tundra prey

Prey handling processes are considered a dominant mechanism leading to short-term positive indirect effects between prey that share a predator. However, a growing body of research indicates that predators are not necessarily limited by such processes in the wild. Density-dependent changes in predator foraging behavior can also generate positive indirect effects but they are rarely included as explicit functions of prey densities in functional response models. With the aim of untangling proximate mechanisms of species interactions in natural communities and improving our ability to quantify interaction strength, we extended the multi-prey version of the Holling disk equation by including density-dependent changes in predator foraging behavior. Our model, based on species traits and behavior, was inspired by the vertebrate community of the arctic tundra, where the main predator (the arctic fox) is an active forager feeding primarily on cyclic small rodent (lemming) and eggs of various tundra-nesting bird species. Short-term positive indirect effects of lemmings on birds have been documented over the circumpolar Arctic but the underlying mechanisms remain poorly understood. We used a unique data set, containing high-frequency GPS tracking, accelerometer, behavioral, and experimental data to parameterize the multi-prey model, and a 15-year time series of prey densities and bird nesting success to evaluate interaction strength between species. We found that (1) prey handling processes play a minor role in our system and (2) changes in arctic fox daily activity budget and distance traveled can partly explain the predation release on birds observed during lemming peaks. These adjustments in predator foraging behavior with respect to the main prey density thus appear as the dominant mechanism leading to positive indirect effects commonly reported among arctic tundra prey. Density-dependent changes in functional response components have been little studied in natural vertebrate communities and deserve more attention to improve our ability to quantify the strength of species interactions.