Fear of the human 'super predator' in native marsupials and introduced deer in Australia.

Recent experiments have demonstrated that carnivores and ungulates in Africa, Asia, Europe and North America fear the human 'super predator' far more than other predators. Australian mammals have been a focus of research on predator naiveté because it is suspected they show atypical antipredator responses. To experimentally test if mammals in Australia also most fear humans, we quantified the responses of four native marsupials (eastern grey kangaroo, Bennett's wallaby, Tasmanian pademelon, common brushtail possum) and introduced fallow deer to playbacks of predator (human, dog, Tasmanian devil, wolf) or non-predator control (sheep) vocalizations. Native marsupials most feared the human 'super predator', fleeing humans 2.4 times more often than the next most frightening predator (dogs), and being most, and significantly, vigilant to humans. These results demonstrate that native marsupials are not naïve to the peril humans pose, substantially expanding the taxonomic and geographic scope of the growing experimental evidence that wildlife worldwide generally perceive humans as the planet's most frightening predator. Introduced fallow deer fled humans, but not more than other predators, which we suggest may result from their being introduced. Our results point to both challenges concerning marsupial conservation and opportunities for exploiting fear of humans as a wildlife management tool.

Fear of the human "super predator" pervades the South African savanna.

Lions have long been perceived as Africa's, if not the world's, most fearsome terrestrial predator,1,2,3,4,5,6,7,8,9 the "king of beasts". Wildlife's fear of humans may, however, be far more powerful and all-prevailing1,10 as recent global surveys show that humans kill prey at much higher rates than other predators,10,11,12 due partly to technologies such as hunting with dogs or guns.11,13,14,15 We comprehensively experimentally tested whether wildlife's fear of humans exceeds even that of lions, by quantifying fear responses1 in the majority of carnivore and ungulate species (n = 19) inhabiting South Africa`s Greater Kruger National Park (GKNP),9,15,16,17 using automated camera-speaker systems9,18 at waterholes during the dry season that broadcast playbacks of humans, lions, hunting sounds (dogs, gunshots) or non-predator controls (birds).9,19,20,21,22 Fear of humans significantly exceeded that of lions throughout the savanna mammal community. As a whole (n = 4,238 independent trials), wildlife were twice as likely to run (p < 0.001) and abandoned waterholes in 40% faster time (p < 0.001) in response to humans than to lions (or hunting sounds). Fully 95% of species ran more from humans than lions (significantly in giraffes, leopards, hyenas, zebras, kudu, warthog, and impala) or abandoned waterholes faster (significantly in rhinoceroses and elephants). Our results greatly strengthen the growing experimental evidence that wildlife worldwide fear the human "super predator" far more than other predators,1,19,20,21,22,23,24,25,26,27,28 and the very substantial fear of humans demonstrated can be expected to cause considerable ecological impacts,1,6,22,23,24,29,30,31,32,33,34,35 presenting challenges for tourism-dependent conservation,1,36,37 particularly in Africa,38,39 while providing new opportunities to protect some species.1,22,40.

Prey species increase activity in refugia free of terrestrial predators.

The decline of terrestrial predator populations across the globe is altering top-down pressures that drive predator-prey interactions. However, a knowledge gap remains in understanding how removing terrestrial predators affects prey behavior. Using a bifactorial playback experiment, we exposed fox squirrels to predator (red-tailed hawks, coyotes, dogs) and non-predator control (Carolina wren) calls inside terrestrial predator exclosures, accessible to avian predators, and in control areas subject to ambient predation risk. Fox squirrels increased their use of terrestrial predator exclosures, a pattern that corresponded with 3 years of camera trapping. Our findings suggest fox squirrels recognized that exclosures had predictably lower predation risk. However, exclosures had no effect on their immediate behavioral response towards any call, and fox squirrels responded most severely to hawk predator calls. This study shows that anthropogenically driven predator loss creates predictably safer areas (refugia) that prey respond to proactively with increased use. However, the persistence of a lethal avian predator is sufficient to retain a reactive antipredator response towards an immediate predation threat. Some prey may benefit from shifting predator-prey interactions by gaining refugia without sacrificing a sufficient response towards potential predators.

Fear of predators in free-living wildlife reduces population growth over generations.

Correctly assessing the total impact of predators on prey population growth rates (lambda, λ) is critical to comprehending the importance of predators in species conservation and wildlife management. Experiments over the past decade have demonstrated that the fear (antipredator responses) predators inspire can affect prey fecundity and early offspring survival in free-living wildlife, but recent reviews have highlighted the absence of evidence experimentally linking such effects to significant impacts on prey population growth. We experimentally manipulated fear in free-living wild songbird populations over three annual breeding seasons by intermittently broadcasting playbacks of either predator or nonpredator vocalizations and comprehensively quantified the effects on all the components of population growth, together with evidence of a transgenerational impact on offspring survival as adults. Fear itself significantly reduced the population growth rate (predator playback mean λ = 0.91, 95% CI = 0.80 to 1.04; nonpredator mean λ = 1.06, 95% CI = 0.96 to 1.16) by causing cumulative, compounding adverse effects on fecundity and every component of offspring survival, resulting in predator playback parents producing 53% fewer recruits to the adult breeding population. Fear itself was consequently projected to halve the population size in just 5 years, or just 4 years when the evidence of a transgenerational impact was additionally considered (λ = 0.85). Our results not only demonstrate that fear itself can significantly impact prey population growth rates in free-living wildlife, comparing them with those from hundreds of predator manipulation experiments indicates that fear may constitute a very considerable part of the total impact of predators.

Prey tells, large herbivores fear the human 'super predator'.

Fear of the human 'super predator' has been demonstrated to so alter the feeding behavior of large carnivores as to cause trophic cascades. It has yet to be experimentally tested if fear of humans has comparably large effects on the feeding behavior of large herbivores. We conducted a predator playback experiment exposing white-tailed deer to the vocalizations of humans, extant or locally extirpated non-human predators (coyotes, cougars, dogs, wolves), or non-predator controls (birds), at supplemental food patches to measure the relative impacts on deer feeding behavior. Deer were more than twice as likely to flee upon hearing humans than other predators, and hearing humans was matched only by hearing wolves in reducing overall feeding time gaged by visits to the food patch in the following hour. Combined with previous, site-specific research linking deer fecundity to predator abundance, this study reveals that fear of humans has the potential to induce a larger effect on ungulate reproduction than has ever been reported. By demonstrating that deer most fear the human 'super predator', our results point to the fear humans induce in large ungulates having population- and community-level impacts comparable to those caused by the fear humans induce in large carnivores.

Fear of large carnivores is tied to ungulate habitat use: evidence from a bifactorial experiment.

The fear large carnivores inspire in large ungulates has been argued to have cascading effects down food webs. However, a direct link between ungulate habitat use and their fear of large carnivores has not been experimentally tested. To fill this critical gap, we conducted a bi-factorial experiment in an African savanna. We removed shrub cover and broadcast large carnivore vocalizations (leopard, hyena, dog) or non-threatening control vocalizations in both experimentally cleared and shrubby control sites. We recorded the proactive (frequency of visitation) and reactive (fleeing or vigilance) responses of multiple prey (impala, warthog, nyala and bushbuck). Critically, we found a significant proactive-reactive interaction. Ungulates were 47% more likely to run after hearing a predator vocalization in shrubby control sites than experimental clearings, demonstrating that ungulates perceived less fear from large carnivores in open habitat (clearings). Consistent with this finding, ungulates visited clearings 2.4 times more often than shrubby control sites and visited shrubby control sites less often at night, when large carnivores are most active. Combined with results from previous experiments demonstrating that the disproportionate use of available habitats by large ungulates can alter ecosystem properties, our experiment provides critical evidence that the fear large carnivores inspire in large ungulates can cause trophic cascades.

Humans, but not their dogs, displace pumas from their kills: An experimental approach.

Domestic dogs are the most abundant large carnivore on the planet, and their ubiquity has led to concern regarding the impacts of dogs as predators of and competitors with native wildlife. If native large carnivores perceive dogs as threatening, impacts could extend to the community level by altering interactions between large carnivores and their prey. Dog impacts may be further exacerbated if these human-associated predators are also perceived as indicators of risk from humans. However, observational approaches used to date have led to ambiguity regarding the effects of dog presence on wildlife. We experimentally quantified dog impacts on the behavior of a native large carnivore, presenting playbacks of dog vocalizations to pumas in central California. We show that the perceived presence of dogs has minimal impacts on puma behavior at their kill sites, and is no more likely to affect total feeding time at kills than non-threatening controls. We previously demonstrated that pumas exhibit strong responses to human cues, and here show that perceived risk from human presence far exceeds that from dogs. Our results suggest that protected areas management policies that restrict dogs but permit human access may in some cases be of limited value for large carnivores.

Predator-induced fear causes PTSD-like changes in the brains and behaviour of wild animals.

Predator-induced fear is both, one of the most common stressors employed in animal model studies of post-traumatic stress disorder (PTSD), and a major focus of research in ecology. There has been a growing discourse between these disciplines but no direct empirical linkage. We endeavoured to provide this empirical linkage by conducting experiments drawing upon the strengths of both disciplines. Exposure to a natural cue of predator danger (predator vocalizations), had enduring effects of at least 7 days duration involving both, a heightened sensitivity to predator danger (indicative of an enduring memory of fear), and elevated neuronal activation in both the amygdala and hippocampus - in wild birds (black-capped chickadees, Poecile atricapillus), exposed to natural environmental and social experiences in the 7 days following predator exposure. Our results demonstrate enduring effects on the brain and behaviour, meeting the criteria to be considered an animal model of PTSD - in a wild animal, which are of a nature and degree which can be anticipated could affect fecundity and survival in free-living wildlife. We suggest our findings support both the proposition that PTSD is not unnatural, and that long-lasting effects of predator-induced fear, with likely effects on fecundity and survival, are the norm in nature.

Fear of humans as apex predators has landscape-scale impacts from mountain lions to mice.

Apex predators such as large carnivores can have cascading, landscape-scale impacts across wildlife communities, which could result largely from the fear they inspire, although this has yet to be experimentally demonstrated. Humans have supplanted large carnivores as apex predators in many systems, and similarly pervasive impacts may now result from fear of the human 'super predator'. We conducted a landscape-scale playback experiment demonstrating that the sound of humans speaking generates a landscape of fear with pervasive effects across wildlife communities. Large carnivores avoided human voices and moved more cautiously when hearing humans, while medium-sized carnivores became more elusive and reduced foraging. Small mammals evidently benefited, increasing habitat use and foraging. Thus, just the sound of a predator can have landscape-scale effects at multiple trophic levels. Our results indicate that many of the globally observed impacts on wildlife attributed to anthropogenic activity may be explained by fear of humans.

Ecology of fear.

The 'ecology of fear' refers to the total impact of predators on prey populations and communities. The traditional view in ecology is that predators directly kill prey, thereby reducing prey survival and prey numbers - and that this is the limit of their ecological role. The ecology of fear posits that the behavioural, physiological and neurobiological costs of avoiding predation ('fear' for short) may additionally reduce prey fecundity and survival, and the total reduction in prey numbers resulting from exposure to predators may thus far exceed that due to direct killing alone. If this is the case, then failing to consider fear as a factor risks profoundly underestimating the ecological role predators play.

Fear affects parental care, which predicts juvenile survival and exacerbates the total cost of fear on demography.

Fear itself (perceived predation risk) can affect wildlife demography, but the cumulative impact of fear on population dynamics is not well understood. Parental care is arguably what most distinguishes birds and mammals from other taxa, yet only one experiment on wildlife has tested fear effects on parental food provisioning and the repercussions this has for the survival of dependent offspring, and only during early-stage care. We tested the effect of fear on late-stage parental care of mobile dependent offspring, by locating radio-tagged Song Sparrow fledglings and broadcasting predator or non-predator playbacks in their vicinity, measuring their parent's behavior and their own, and tracking the offspring's survival to independence. Fear significantly reduced late-stage parental care, and parental fearfulness (as indexed by their reduction in provisioning when hearing predators) significantly predicted their offspring's condition and survival. Combining results from this experiment with that on early-stage care, we project that fear itself is powerful enough to reduce late-stage survival by 24%, and cumulatively reduce the number of young reaching independence by more than half, 53%. Experiments in invertebrate and aquatic systems demonstrate that fear is commonly as important as direct killing in affecting prey demography, and we suggest focusing more on fear effects and on offspring survival will reveal the same for wildlife.

Fear of the human 'super predator' reduces feeding time in large carnivores.

Large carnivores' fear of the human 'super predator' has the potential to alter their feeding behaviour and result in human-induced trophic cascades. However, it has yet to be experimentally tested if large carnivores perceive humans as predators and react strongly enough to have cascading effects on their prey. We conducted a predator playback experiment exposing pumas to predator (human) and non-predator control (frog) sounds at puma feeding sites to measure immediate fear responses to humans and the subsequent impacts on feeding. We found that pumas fled more frequently, took longer to return, and reduced their overall feeding time by more than half in response to hearing the human 'super predator'. Combined with our previous work showing higher kill rates of deer in more urbanized landscapes, this study reveals that fear is the mechanism driving an ecological cascade from humans to increased puma predation on deer. By demonstrating that the fear of humans can cause a strong reduction in feeding by pumas, our results support that non-consumptive forms of human disturbance may alter the ecological role of large carnivores.

Do Large Carnivores and Mesocarnivores Have Redundant Impacts on Intertidal Prey?

The presence of large carnivores can affect lower trophic levels by suppressing mesocarnivores and reducing their impacts on prey. The mesopredator release hypothesis therefore predicts prey abundance will be higher where large carnivores are present, but this prediction assumes limited dietary overlap between large and mesocarnivores. Where dietary overlap is high, e.g., among omnivorous carnivore species, or where prey are relatively easily accessible, the potential exists for large and mesocarnivores to have redundant impacts on prey, though this possibility has not been explored. The intertidal community represents a potentially important but poorly studied resource for coastal carnivore populations, and one for which dietary overlap between carnivores may be high. To evaluate usage of the intertidal community by coastal carnivores and the potential for redundancy between large and mesocarnivores, we surveyed (i) intertidal prey abundance (crabs and fish) and (ii) the abundance and activity of large carnivores (predominantly black bears) and mesocarnivores (raccoons and mink) in an area with an intact carnivore community in coastal British Columbia, Canada. Overall carnivore activity was strongly related to intertidal prey availability. Notably, this relationship was not contingent on carnivore species identity, suggestive of redundancy-high intertidal prey availability was associated with either greater large carnivore activity or greater mesocarnivore activity. We then compared intertidal prey abundances in this intact system, in which bears dominate, with those in a nearby system where bears and other large carnivores have been extirpated, and raccoons are the primary intertidal predator. We found significant similarities in intertidal species abundances, providing additional evidence for redundancy between large (bear) and mesocarnivore (raccoon) impacts on intertidal prey. Taken together, our results indicate that intertidal prey shape habitat use and competition among coastal carnivores, and raise the interesting possibility of redundancy between mesocarnivores and large carnivores in their role as intertidal top predators.

Fear of large carnivores causes a trophic cascade.

The fear large carnivores inspire, independent of their direct killing of prey, may itself cause cascading effects down food webs potentially critical for conserving ecosystem function, particularly by affecting large herbivores and mesocarnivores. However, the evidence of this has been repeatedly challenged because it remains experimentally untested. Here we show that experimentally manipulating fear itself in free-living mesocarnivore (raccoon) populations using month-long playbacks of large carnivore vocalizations caused just such cascading effects, reducing mesocarnivore foraging to the benefit of the mesocarnivore's prey, which in turn affected a competitor and prey of the mesocarnivore's prey. We further report that by experimentally restoring the fear of large carnivores in our study system, where most large carnivores have been extirpated, we succeeded in reversing this mesocarnivore's impacts. We suggest that our results reinforce the need to conserve large carnivores given the significant "ecosystem service" the fear of them provides.

Diagnosing predation risk effects on demography: can measuring physiology provide the means?

Predators kill prey thereby affecting prey survival and, in the traditional top-down view of predator limitation, that is their sole effect. Bottom-up food limitation alters the physiological condition of individuals affecting both fecundity and survival. Predators of course also scare prey inducing anti-predator defences that may carry physiological costs powerful enough to reduce prey fecundity and survival. Here, we consider whether measuring physiology can be used as a tool to unambiguously diagnose predation risk effects. We begin by providing a review of recent papers reporting physiological effects of predation risk. We then present a conceptual framework describing the pathways by which predators and food can affect prey populations and give an overview of predation risk effects on demography in various taxa. Because scared prey typically eat less the principal challenge we see will be to identify measures that permit us to avoid mistaking predator-induced reductions in food intake for absolute food shortage. To construct an effective diagnostic toolkit we advocate collecting multiple physiological measures and utilizing multivariate statistical procedures. We recommend conducting two-factor predation risk × food manipulations to identify those physiological effects least likely to be mistaken for responses to bottom-up food limitation. We suggest there is a critical need to develop a diagnostic tool that can be used when it is infeasible to experimentally test for predation risk effects on demography, as may often be the case in wildlife conservation, since failing to consider predation risk effects may cause the total impact of predators to be dramatically underestimated.

Mammalian mesopredators on islands directly impact both terrestrial and marine communities.

Medium-sized mammalian predators (i.e. mesopredators) on islands are known to have devastating effects on the abundance and diversity of terrestrial vertebrates. Mesopredators are often highly omnivorous, and on islands, may have access not only to terrestrial prey, but to marine prey as well, though impacts of mammalian mesopredators on marine communities have rarely been considered. Large apex predators are likely to be extirpated or absent on islands, implying a lack of top-down control of mesopredators that, in combination with high food availability from terrestrial and marine sources, likely exacerbates their impacts on island prey. We exploited a natural experiment--the presence or absence of raccoons (Procyon lotor) on islands in the Gulf Islands, British Columbia, Canada--to investigate the impacts that this key mesopredator has on both terrestrial and marine prey in an island system from which all native apex predators have been extirpated. Long-term monitoring of song sparrow (Melospiza melodia) nests showed raccoons to be the predominant nest predator in the Gulf Islands. To identify their community-level impacts, we surveyed the distribution of raccoons across 44 Gulf Islands, and then compared terrestrial and marine prey abundances on six raccoon-present and six raccoon-absent islands. Our results demonstrate significant negative effects of raccoons on terrestrial, intertidal, and shallow subtidal prey abundance, and point to additional community-level effects through indirect interactions. Our findings show that mammalian mesopredators not only affect terrestrial prey, but that, on islands, their direct impacts extend to the surrounding marine community.

Food use is affected by the experience of nest predation: implications for indirect predator effects on clutch size.

Indirect predator effects on prey demography include any effect not attributable to direct killing and can be mediated by perceived predation risk. Though perceived predation risk clearly affects foraging, few studies have yet demonstrated that it can chronically alter food intake to an extent that affects demography. Recent studies have used stable isotopes to gauge such chronic effects. We previously reported an indirect predator effect on the size of subsequent clutches laid by song sparrows (Melospiza melodia). Females that experienced frequent experimental nest predation laid smaller clutches and were in poorer physiological condition compared to females not subject to nest predation. Every female was provided with unlimited supplemental food that had a distinctive (13)C signature. Here, we report that frequent nest predation females had lower blood δ(13)C values, suggesting that the experience of nest predation caused them to eat less supplemental food. Females that ate less food gained less fat and were in poorer physiological condition, consistent with the effect on food use contributing to the indirect predator effect on clutch size. Tissue δ(15)N values corroborated that clutch size was not likely constrained by endogenous resources. Finally, we report that the process of egg production evidently affects egg δ(13)C values, and this may mask the source of nutrients to eggs. Our results indicate that perceived predation risk may impose food limitation on prey even where food is unlimited and such predator-induced food limitation ought to be added to direct killing when considering the total effect of predators on prey numbers.

Perceived predation risk reduces the number of offspring songbirds produce per year.

Predator effects on prey demography have traditionally been ascribed solely to direct killing in studies of population ecology and wildlife management. Predators also affect the prey's perception of predation risk, but this has not been thought to meaningfully affect prey demography. We isolated the effects of perceived predation risk in a free-living population of song sparrows by actively eliminating direct predation and used playbacks of predator calls and sounds to manipulate perceived risk. We found that the perception of predation risk alone reduced the number of offspring produced per year by 40%. Our results suggest that the perception of predation risk is itself powerful enough to affect wildlife population dynamics, and should thus be given greater consideration in vertebrate conservation and management.

The Neurological Ecology of Fear: Insights Neuroscientists and Ecologists Have to Offer one Another.

That the fear and stress of life-threatening experiences can leave an indelible trace on the brain is most clearly exemplified by post-traumatic stress disorder (PTSD). Many researchers studying the animal model of PTSD have adopted utilizing exposure to a predator as a life-threatening psychological stressor, to emulate the experience in humans, and the resulting body of literature has demonstrated numerous long-lasting neurological effects paralleling those in PTSD patients. Even though much more extreme, predator-induced fear and stress in animals in the wild was, until the 1990s, not thought to have any lasting effects, whereas recent experiments have demonstrated that the effects on free-living animals are sufficiently long-lasting to even affect reproduction, though the lasting neurological effects remain unexplored. We suggest neuroscientists and ecologists both have much to gain from collaborating in studying the neurological effects of predator-induced fear and stress in animals in the wild. We outline the approaches taken in the lab that appear most readily translatable to the field, and detail the advantages that studying animals in the wild can offer researchers investigating the "predator model of PTSD."