Loss of an apex predator in the wild induces physiological and behavioural changes in prey.

Predators can impact prey via predation or risk effects, which can initiate trophic cascades. Given widespread population declines of apex predators, understanding and predicting the associated ecological consequences is a priority. When predation risk is relatively unpredictable or uncontrollable by prey, the loss of predators is hypothesized to release prey from stress; however, there are few tests of this hypothesis in the wild. A well-studied predator-prey system between white sharks (Carcharodon carcharias) and Cape fur seals (Arctocephalus pusillus pusillus) in False Bay, South Africa, has previously demonstrated elevated faecal glucocorticoid metabolite concentrations (fGCMs) in seals exposed to high levels of predation risk from white sharks. A recent decline and disappearance of white sharks from the system has coincided with a pronounced decrease in seal fGCM concentrations. Seals have concurrently been rafting further from shore and over deeper water, a behaviour that would have previously rendered them vulnerable to attack. These results show rapid physiological and behavioural responses by seals to release from predation stress. To our knowledge, this represents the first demonstration in the wild of physiological changes in prey from predator decline, and such responses are likely to increase given the scale and pace of apex predator declines globally.

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

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.

Disappearance of white sharks leads to the novel emergence of an allopatric apex predator, the sevengill shark.

Despite global declines of apex predatory sharks, evidence for ecosystem consequences remains limited and debated. This is likely a result of both the logistical difficulties of measuring such processes in marine systems and also due to shifting baselines, whereby the ecosystem changes have occurred prior to monitoring. Between 2000-2018, we conducted standardized monitoring of white shark (Carcharodon carcharias) abundance patterns (N = 6,333 shark sightings) and predatory activity (N = 8,076 attacks on seals) at Seal Island, a Cape fur seal (Arctocephalus pusillus pusillus) colony in False Bay, South Africa. Over the 18-year study, declines in white shark abundance and attack rates were documented between 2015-2018, with anomalous lows occurring in 2017 and 2018. This included prolonged periods of complete white shark absence from Seal Island. The disappearance of white sharks from Seal Island coincided with the unprecedented appearance of sevengill sharks (Notorynchus cepedianus; N = 120 sightings), an otherwise allopatric kelp-associated apex predator in False Bay. We also recorded a sevengill shark attacking a live seal in the absence of white sharks. These data provide empirical evidence for behavioral shifts in an allopatric marine predator following the decline and disappearance of white sharks from a foraging site. This study demonstrates the importance of historical data and long-term monitoring for disentangling ecological consequences of apex predator declines.

White sharks (Carcharodon carcharias) scavenging on whales and its potential role in further shaping the ecology of an apex predator.

Scavenging, a result of a temporary pulse of resources, occurs in virtually all ecosystems containing carnivores, and is an important energy transfer pathway that can impact ecosystem structure and function, and this ecological significance has largely been considered from a terrestrial standpoint; however, little is known about the role of scavenging in shaping the behavioral ecology of marine species, specifically apex predators. Here we present findings from multiple opportunistic observations of white sharks scavenging on whale carcasses in False Bay, South Africa. Observations of white sharks scavenging over successive days provided evidence of strategic and selective scavenging by this species. Moreover, extended daily observations permitted recordings of unique social, aggregative, and feeding behaviors. We further compare these data against observations of natural predation by sharks on seals in the study area. We discuss these data in relation to environmental conditions, shark social interactions, migration patterns, whale biology, and behaviorally-mediated trophic cascades. While the appearance of a whale carcass is largely a stochastic event, we propose that white shark scavenging on whales may represent an underestimated, yet significant component to the overall foraging ecology of this species, especially as individuals attain sexual maturity.