Physiological stress responses to natural variation in predation risk: evidence from white sharks and seals

Abstract

Predators can impact ecosystems through consumptive or risk effects on prey. Physiologically, risk effects can be mediated by energetic mechanisms or stress responses. The predation-stress hypothesis predicts that risk induces stress in prey, which can affect survival and reproduction. However, empirical support for this hypothesis is both mixed and limited, and the conditions that cause predation risk to induce stress responses in some cases, but not others, remain unclear. Unusually clear-cut variation in exposure of Cape fur seals (Arctocephalus pusillus pusillus) to predation risk from white sharks (Carcharodon carcharias) in the waters of Southwestern Africa provides an opportunity to test the predation-stress hypothesis in the wild. Here, we measured fecal glucocorticoid concentrations (fGCM) from Cape fur seals at six discrete islands colonies exposed to spatiotemporal variation in predation risk from white sharks over a period of three years. We found highly elevated fGCM concentrations in seals at colonies exposed to high levels of unpredictable and relatively uncontrollable risk of shark attack, but not at colonies where seals were either not exposed to shark predation or could proactively mitigate their risk through antipredatory behavior. Differences in measured fGCM levels were consistent with patterns of risk at the site and seasonal level, for both seal adults and juveniles. Seal fGCM levels were not correlated with colony population size, density, and geographic location. Investigation at a high risk site (False Bay) also revealed strong correlations between fGCM levels and temporal variation in shark attack rates, but not with shark relative abundance. Our results suggest that predation risk will induce a stress response when risk cannot be predicted and/or proactively mitigated by behavioral responses.

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

“…Because white sharks attack from below in a rapid rush from dark waters, attacks are unpredictable during a seal's passage through the high-risk area (Hammerschlag et al 2006). In a comparison of six islands, glucocorticoid levels were elevated at high-risk seal colonies in the high-predation season but not in the lowpredation season, and weekly mean glucocorticoid levels correlated tightly with weekly mean rates of attack (Hammerschlag et al 2017). These results exemplify stress-mediated effects associated with reactive antipredator responses to uncontrollable risks, as predicted by the COR hypothesis.…”

“…On the basis of such studies, it is reasonable to hypothesise that the costs of antipredator responses will be (at least in part) stress mediated when risk cannot be predicted or controlled by proactive responses. Examples that support this hypothesis include nesting songbirds (Clinchy et al 2004) and fur seals at rookeries (Hammerschlag et al 2017), both of which have limited control of their exposure to risk because they are tied to a breeding site with immobile offspring.…”

“…) and fur seals at rookeries (Hammerschlag et al . ), both of which have limited control of their exposure to risk because they are tied to a breeding site with immobile offspring.…”

Estimates of abundance and change in abundance of the Indo-Pacific bottlenose dolphins (Tursiops aduncus) along the south coast of South Africa

“…This impact of the sharks on the T. aduncus population may be direct (i.e. predation in itself) [49]; or indirect, whereby the predation risk brings about increased stress levels in the prey population that can reduce their performance and productivity, or changes in residency patterns reducing time spent in the area [50].…”

HPLC‐QTOF method for quantifying 11‐ketoetiocholanolone, a cortisol metabolite, in ruminants' feces: Optimization and validation

“…Detecting stress is an important aspect of physiological ecology and behavioral ecology, and it has been the focus of research on many taxa and scenarios. For instance, it was addressed in the study of the migratory disposition at different seasons for proactive and reactive birds (Pusch, Bentz, Becker, & Navara, 2018); as an indicator of natural variation in the predation of seals by white sharks (Hammerschlag et al, 2017); and even for evaluating the evolutionary adaptation of insects in a period of food scarcity (Wang et al, 2016).…”