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.

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.

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.

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 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.

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.

Modelling the fear effect in predator-prey interactions.

A recent field manipulation on a terrestrial vertebrate showed that the fear of predators alone altered anti-predator defences to such an extent that it greatly reduced the reproduction of prey. Because fear can evidently affect the populations of terrestrial vertebrates, we proposed a predator-prey model incorporating the cost of fear into prey reproduction. Our mathematical analyses show that high levels of fear (or equivalently strong anti-predator responses) can stabilize the predator-prey system by excluding the existence of periodic solutions. However, relatively low levels of fear can induce multiple limit cycles via subcritical Hopf bifurcations, leading to a bi-stability phenomenon. Compared to classic predator-prey models which ignore the cost of fear where Hopf bifurcations are typically supercritical, Hopf bifurcations in our model can be both supercritical and subcritical by choosing different sets of parameters. We conducted numerical simulations to explore the relationships between fear effects and other biologically related parameters (e.g. birth/death rate of adult prey), which further demonstrate the impact that fear can have in predator-prey interactions. For example, we found that under the conditions of a Hopf bifurcation, an increase in the level of fear may alter the direction of Hopf bifurcation from supercritical to subcritical when the birth rate of prey increases accordingly. Our simulations also show that the prey is less sensitive in perceiving predation risk with increasing birth rate of prey or increasing death rate of predators, but demonstrate that animals will mount stronger anti-predator defences as the attack rate of predators increases.

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.

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.

Multiple measures elucidate glucocorticoid responses to environmental variation in predation threat.

Predator-induced changes in the glucocorticoid responses of prey have been proposed to mediate indirect predator effects on prey demography. Ambiguities exist, however, as to whether differences in predation threat in the environment at large affect the mean glucocorticoid response in wild birds and mammals, and whether this is likely to affect reproduction. Most studies to date that have examined glucocorticoid responses to environmental variation in predation threat have evaluated just one of the several potential measures of the glucocorticoid response, and this may be the source of many ambiguities. We evaluated multiple measures of the glucocorticoid response [plasma total CORTicosterone, corticosteroid binding globulin (CBG) and free CORT] in male and female song sparrows (Melospiza melodia) sampled at locations differing in predation threat in the environment at large, where we have previously reported reproductive differences suggestive of indirect predator effects. Total CORT varied markedly with predation threat in males but not females whereas the opposite was true for CBG, and both sexes demonstrated the same moderately significant free CORT response. Considering all three indices, a glucocorticoid response to environmental variation in predation threat was evident in both sexes, whereas there were ambiguities considering each index singly. We conclude that collecting multiple physiological measures and conducting multivariate analyses may provide a preferable means of assessing glucocorticoid responses to environmental variation in predation threat, and so help clarify whether such glucocorticoid changes affect reproduction in wild birds and mammals.

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.

Indirect predator effects on clutch size and the cost of egg production.

Predator-induced changes in physiology and behaviour may negatively affect a prey's birth rate. Evidence of such indirect predator effects on prey demography remains scarce in birds and mammals despite invertebrate and aquatic studies that suggest ignoring such effects risks profoundly underestimating the total impact of predators. We report the first experimental demonstration of indirect predator effects on the annual 'birth' rate resulting from negative effects on the size of subsequent clutches laid by birds. We manipulated the probability of nest predation and measured the size of subsequent clutches and multiple indices of the mother's physiological condition, while controlling for food availability, date and stage of breeding. Females subject to frequent experimental nest predation laid smaller subsequent clutches and were in poorer physiological condition, particularly regarding non-resource-based indices (e.g. oxidative stress and glucocorticoid mobilization) consistent with both a response to the threat of predation and an increased cost of egg production.

Food supplementation leads to bottom-up and top-down food-host-parasite interactions.

1. Food-prey-predator interactions may involve both 'bottom-up' and 'top-down' processes. Conventionally, food-host-parasite interactions have been seen as governed solely from the 'bottom-up', i.e. well-fed hosts can better resist parasites and so suffer less parasitism. Recent studies on diverse endo- and ecto-parasites increasingly highlight that well-fed hosts provide parasites with a better resource base, and so may be more likely to be parasitized. 2. Brood parasites exploit host parental behaviour by laying their eggs in others' nests. The brown-headed cowbird (Molothrus ater) is a North American brood parasite that exploits over 100 host species. 3. We conducted a food addition experiment on song sparrows (Melospiza melodia), a frequently parasitized cowbird host, near Victoria, BC, Canada. We expected results consistent with conventional 'bottom-up' effects because we previously found that food supplemented sparrows better eluded nest predation, and we thus also expected them to be better at eluding cowbird parasitism. 4. Here, we report results to the contrary. Food supplemented sparrows were parasitized as often as non-food supplemented sparrows, were multiply parasitized significantly more often, and suffered significantly more parasitism-induced egg loss. Our results suggest cowbirds preferentially parasitized better fed hosts and cowbirds benefited from doing so as food supplemented sparrows fledged significantly more cowbird young per multiply parasitized nest. The pattern of egg loss also accorded with recent evidence indicating that cowbirds may remove just the right number of host eggs to maximize provisioning of the cowbird nestling. 5. Our work suggests that brood parasitism in vertebrates involves both 'top-down' and 'bottom-up' processes consistent with the growing number of studies showing that food-host-parasite interactions are more complex than previously thought. One of the conservation implications of our results is that greater food availability may not provide hosts a respite from brood parasitism, but is, nonetheless, beneficial overall.

Food-supplementing parents reduces their sons' song repertoire size.

Food-supplemented parents typically produce more offspring, as numerous experiments on vertebrate populations have shown. 'Propagule' (egg or neonate) size and parental care may also be affected, with implications concerning the adult quality of offspring, although few experiments have addressed whether food-supplementing one generation affects adult quality in the next. We conducted a food supplementation experiment on song sparrows (Melospiza melodia) and tested whether song repertoire size, a demonstrated indicator of male quality, differed between the adult sons of fed (food-supplemented) and unfed (non-food-supplemented) parents. Counterintuitively, fed parents produced sons with smaller adult song repertoires, who may thus be expected to contribute fewer offspring, and fewer grand-offspring, to the population. Fed and unfed parents invested equally in the total biomass of their clutches and broods, and average nestling condition was comparable, but because fed parents produced more offspring, average egg and nestling sizes were reduced. Fed and unfed parents apportioned care differently within their broods, and we suggest compensatory growth of offspring emerging from light eggs, or egg size itself, may have affected adult repertoire size. Conceivably, the conservation benefits of food-supplementing populations could attenuate over time if fed parents produce offspring of poorer quality than themselves.

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.

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.