Integrating predator energetic balance, risk-taking behavior and microhabitat in functional response to untangle indirect interactions in a multispecies vertebrate community

Predator-prey interactions in natural communities are complex, with
predators often exploiting multiple prey types and generating indirect
interactions among them. Ecological theory has traditionally modeled these
interactions using functional responses models which are based on foraging
rates, not energy transfers. This approach overlooks how the energy
acquisition rate of a predator can alter its behavior and, in turn, the
strength of species interactions. Here, we integrate predator energetics
into a functional response model to represent trade-offs predators face
when foraging on prey that vary in risk and abundance across heterogeneous
landscapes. We compared model predictions to 20 years of prey species
density and reproductive success data. The mechanistic model was
parameterized for an Arctic tundra vertebrate community, where the Arctic
fox feeds on cyclic lemmings and eggs of sandpipers (non-risky prey) and
gulls (risky prey that often nest in partial refuge like islands). In this
system, predator-mediated interactions generate apparent mutualism between
lemmings and birds, but its strength varies between species, and the
mechanisms underlying this interaction remain unclear. We found that fox
energetic balance was highly related to lemming density, with a threshold
of 89 lemmings per km2 required for a positive energetic balance.
Model-predicted gull nest acquisition rates were lowest on islands when
the energetic balance of foxes was positive, and highest for nests on the
shore when foxes were in deficit. The model that incorporated predator
risk-taking behavior and energetic balance produced variation in gull
hatching success that most closely matched empirical observations. We
documented for the first time that a shift in predator energetic balance,
triggering changes in attack and capture probabilities on a risky prey,
can be a key mechanism underlying the apparent mutualism between lemmings
and gulls. In contrast, for non-risky prey, the indirect effect can be
essentially driven by changes in predator movement. These findings
highlight how prey characteristics can lead to different mechanisms behind
similar indirect interactions. Taken together, our results indicate that
mechanistic models integrating species traits, landscape features, and
energy-dependent behavioral adjustments can improve our ability to
quantify interaction strengths in natural communities.