The control of risk hypothesis: reactive vs. proactive antipredator responses and stress‐mediated vs. food‐mediated costs of response

Abstract

Inducible defences against predators evolve because they reduce the rate of direct predation, but this benefit is offset by the cost (if any) of defence. If antipredator responses carry costs, the effect of predators on their prey is partitioned into two components, direct killing and risk effects. There is considerable uncertainty about the strength of risk effects, the factors that affect their strength, and the mechanisms that underlie them. In some cases, antipredator responses are associated with a glucocorticoid stress response, and in other cases they are associated with trade-offs between food and safety, but there is no general theory to explain this variation. Here, I develop the control of risk (COR) hypothesis, predicting that proactive responses to predictable and controllable aspects of risk will generally have food-mediated costs, while reactive responses to unpredictable or uncontrollable aspects of predation risk will generally have stress-mediated costs. The hypothesis is grounded in laboratory studies of neuroendocrine stressors and field studies of food-safety trade-offs. Strong tests of the COR hypothesis will require more studies of responses to natural variation in predation risk and the physiological consequences of these responses, but its explanatory power can be illustrated with existing case studies.

Evaluating the effects of large marine predators on mobile prey behavior across subtropical reef ecosystems

“…On average, grunts and snappers arrived on coral reefs and in sea fans long before any predators. Whether predation risk is "predictable" or chronic on coral reefs remains unknown, but our findings offer an interesting potential link to the predicted foodrisk effects as described in the "control of risk" hypothesis (Creel, 2018).…”

“…Thus, the interaction between habitat features and the probability of predator detection and successful escape can result in altered prey risk‐associated behaviors and vigilance (Heithaus et al, ). It has been recently argued that predators may exact greater influences on prey behavior where predation risk is predictable (Creel, ). While we did not measure predictability of predation risk in our study, abundance of predators in certain habitats, a potential proxy for exposure, may have resulted in a pro‐active response of apprehensiveness toward the bait, although this remains speculative.…”

“…Animals often express their antipredator‐behaviors in high risk situations that are brief and infrequent (Lima & Bednekoff, ). These acute “reactive” responses are linked to areas of unpredictable predation risk (Creel, ). We hypothesized that potential behavioral risk effects might be highest in open areas.…”

Complex tactics in a dynamic large herbivore–carnivore spatiotemporal game

“…Bison could be constantly on the move in response to the ghost of predation past (Brown and Vincent , Le Saout et al 2015), regardless of current wolf presence in the landscape. In addition, other mechanisms, such as memory‐based foraging (Merkle et al 2014) or harassment by biting insects (Raponi et al ), could be implicated in bison's decision to leave a food patch. Nevertheless, for at least one season, our results demonstrate the role of predator distribution in triggering patch abandonment by prey as predicted by the shell game hypothesis (Mitchell and Lima ).…”

“…Experimental and empirical studies have shown that animals do commonly spend less time foraging in risky than in safer areas (Brown and Kotler ). Prey can also assess the local risk of predation and adjust the time spent in different areas of their home range to avoid periods when predators are most active (Valeix et al , Kohl et al ), or exhibit reactive responses, such as fleeing, following an encounter with predators (Courbin et al 2016). The risky places hypothesis predicts that prey will either avoid or spend less time in areas where predation risk is predictability high over the long term, while the risky times hypothesis predicts that anti‐predator behaviours will be triggered specifically when predators are in real‐time proximity of prey (Creel et al , Moll et al 2017).…”