Human-induced fear in wildlife: A review

Humans, like natural predators, can induce fear in wildlife, which has the potential to alter species-level survival and fitness. Though anthropogenic impacts on wildlife have been studied in detail, how wildlife respond behaviorally to human presence has been less studied. Here, we provide a literature review on how humans interact with wildlife populations through the ecology of fear framework. Fear responses can be proactive or reactive, and can go beyond behavioral changes to alterations in physiology (such as increases in stress) or alterations in individual chromosome structure. Wildlife are more likely to flee from humans if they possess a larger body size, are female, or have fear-associated genotypes. Intelligence and individual differences lead to variations in wildlife’s fear responses to humans that can make studying fear difficult. Wildlife fear responses to humans depend on environmental factors, including context-specific human presentation and whether the animal was in urban or rural habitats. Human-induced fear in wildlife may have cascading impacts on broader wildlife communities and habitat structure caused by changes in how individual species interact with other species and the environment.     

Landscapes of Coexistence for terrestrial carnivores: the ecological consequences of being downgraded from ultimate to penultimate predator by humans

Fear of predation can have major impacts on the behaviour of prey species. Recently the concept of the ecology of fear has been defined and formalised; yet there has been relatively little focus on how these ideas apply to large carnivore species which, although not prey sensu stricto, also experience fear as a result of threats from humans. Large carnivores are likely also subject to a Landscape of Fear similar to that described for prey species. We argue that although fear is generic, ‘human‐caused mortality’ represents a distinct and very important cause of fear for large carnivores, particularly terrestrial large carnivores as their activities overlap with those of humans to a greater degree. We introduce the idea of a ‘Landscape of Coexistence’ for large carnivores to denote a subset of the Landscape of Fear where sufficient areas of low human‐caused mortality risk are present in the landscape for long term coexistence of large carnivores and humans. We then explore aspects of terrestrial large carnivore behavioural ecology that may be best explained by risk of human‐caused mortality, and how the nature of a Landscape of Coexistence for these large carnivores is likely to be shaped by specific factors such as habitat structure, wild and domestic prey base, and human distribution and behaviour. The human characteristics of this Landscape of Coexistence may be as important in determining large carnivore distribution and behavioural ecology as the distribution of resources. Understanding the Landscape of Coexistence for terrestrial large carnivores is therefore important for their biology and conservation throughout large parts of their remaining ranges. Synthesis The Landscape of Fear concept describing the relationship between predator and prey also applies to the relationship between humans and top carnivores. We synthesise current research to introduce the Landscape of Coexistence concept, arguing that top predators respond to the risks of human‐caused mortality through spatiotemporal partitioning of activities to reduce contact with people. The character of the Landscape of Coexistence may be more important than the distribution of resources in determining large carnivore distribution and behavioural ecology in human dominated landscapes. Understanding their behavioural responses to human threats is crucial to successful conservation of large carnivores.     

Minimizing animal welfare harms associated with predation management in agro‐ecosystems

The impacts of wild predators on livestock are a common source of human–wildlife conflict globally, and predators are subject to population control for this reason in many situations. Animal welfare is one of many important considerations affecting decisions about predation management. Recent studies discussing animal welfare in this context have presented arguments emphasizing the importance of avoiding intentional harm to predators, but they have not usually considered harms imposed by predators on livestock and other animals. Efforts to mitigate predation impacts (including ‘no control’ approaches) cause a variety of harms to predators, livestock and other wildlife. Successfully minimizing the overall frequency and magnitude of harms requires consideration of the direct, indirect, intentional and unintentional harms imposed on all animals inhabiting agricultural landscapes. We review the harms resulting from the management of dingoes and other wild dogs in the extensive beef cattle grazing systems of Australia to illustrate how these negative impacts can be minimized across both wild and domestic species present on a farm or in a free‐ranging livestock grazing context. Similar to many other predator–livestock conflicts, wild dogs impose intermittent harms on beef cattle (especially calves) including fatal predation, non‐fatal attack (mauling and biting), pathogen transmission, and fear‐ or stress‐related effects. Wild dog control tools and strategies impose harms on dingoes and other wildlife including stress, pain and death as a consequence of both lethal and non‐lethal control approaches. To balance these various sources of harm, we argue that the tactical use of lethal predator control approaches can result in harming the least number of individual animals, given certain conditions. This conclusion conflicts with both traditional (e.g. continuous or ongoing lethal control) and contemporary (e.g. predator‐friendly or no‐control) predation management approaches. The general and transferable issues, approaches and principles we describe have broad applicability to many other human–wildlife conflicts around the world.     

Trophic rewilding establishes a landscape of fear: Tasmanian devil introduction increases risk‐sensitive foraging in a key prey species

Global declines of large carnivores have reduced the ‘landscape of fear’ that constrains the behaviour of other species. In recent years, active and passive trophic rewilding have potentially begun restoring these lost top–down controls. The Tasmanian devil Sarcophilus harrisii has declined severely due to a novel transmissible cancer. In response to extinction fears, devils were introduced to the devil‐free Maria Island, where their abundance rapidly increased. We tested how this introduction influenced risk‐sensitive foraging in the common brushtail possum Trichosurus vulpecula, a major prey species for devils, using giving‐up densities (GUDs). Before the introduction of devils, possum GUDs on Maria Island were indistinguishable from the long‐diseased region of Tasmania, where devils have been rare since ~2000. Three years after devil introduction, GUDs were 64% higher on Maria Island than the control region, demonstrating that after an initial period of high mortality, possums quickly adopted risk‐sensitive foraging behaviours. Devil activity across Maria Island was variable, leading to a heterogeneous landscape of fear and highlighting that top predators must be at functional densities to elicit behavioural responses from prey. Our study provides strong evidence that top predators modify the behaviour of prey by instilling fear, causing rapid ecological change following recoveries.     

Fear of feces? Tradeoffs between disease risk and foraging drive animal activity around raccoon latrines

Fear of predation alters prey behavior, which can indirectly alter entire landscapes. A parasite‐induced ecology of fear might also exist if animals avoid parasite‐contaminated resources when infection costs outweigh foraging benefits. To investigate whether animals avoid parasite contaminated sites, and if such avoidance balances disease costs and foraging gains, we monitored animal behavior at raccoon latrines – sites that concentrate both seeds and pathogenic parasite eggs. Using wildlife cameras, we documented over 40 potentially susceptible vertebrate species in latrines and adjacent habitat. Latrine contact rates reflected background activity, diet preferences and disease risk. Disease‐tolerant raccoons and rats displayed significant site attraction, while susceptible birds and small mammals avoided these high‐risk sites. This suggests that parasites, like predators, might create a landscape of fear for vulnerable hosts. Such non‐consumptive parasite effects could alter disease transmission, population dynamics, and even ecosystem structure.     

The landscape of fear as an emergent property of heterogeneity: Contrasting patterns of predation risk in grassland ecosystems

The likelihood of encountering a predator influences prey behavior and spatial distribution such that non‐consumptive effects can outweigh the influence of direct predation. Prey species are thought to filter information on perceived predator encounter rates in physical landscapes into a landscape of fear defined by spatially explicit heterogeneity in predation risk. The presence of multiple predators using different hunting strategies further complicates navigation through a landscape of fear and potentially exposes prey to greater risk of predation. The juxtaposition of land cover types likely influences overlap in occurrence of different predators, suggesting that attributes of a landscape of fear result from complexity in the physical landscape. Woody encroachment in grasslands furnishes an example of increasing complexity with the potential to influence predator distributions. We examined the role of vegetation structure on the distribution of two avian predators, Red‐tailed Hawk (Buteo jamaicensis) and Northern Harrier (Circus cyaneus), and the vulnerability of a frequent prey species of those predators, Northern Bobwhite (Colinus virginianus). We mapped occurrences of the raptors and kill locations of Northern Bobwhite to examine spatial vulnerability patterns in relation to landscape complexity. We use an offset model to examine spatially explicit habitat use patterns of these predators in the Southern Great Plains of the United States, and monitored vulnerability patterns of their prey species based on kill locations collected during radio telemetry monitoring. Both predator density and predation‐specific mortality of Northern Bobwhite increased with vegetation complexity generated by fine‐scale interspersion of grassland and woodland. Predation pressure was lower in more homogeneous landscapes where overlap of the two predators was less frequent. Predator overlap created areas of high risk for Northern Bobwhite amounting to 32% of the land area where landscape complexity was high and 7% where complexity was lower. Our study emphasizes the need to evaluate the role of landscape structure on predation dynamics and reveals another threat from woody encroachment in grasslands.     

Predators and the public trust

Many democratic governments recognize a duty to conserve environmental resources, including wild animals, as a public trust for current and future citizens. These public trust principles have informed two centuries of U.S.A. Supreme Court decisions and environmental laws worldwide. Nevertheless numerous populations of large‐bodied, mammalian carnivores (predators) were eradicated in the 20th century. Environmental movements and strict legal protections have fostered predator recoveries across the U.S.A. and Europe since the 1970s. Now subnational jurisdictions are regaining management authority from central governments for their predator subpopulations. Will the history of local eradication repeat or will these jurisdictions adopt public trust thinking and their obligation to broad public interests over narrower ones? We review the role of public trust principles in the restoration and preservation of controversial species. In so doing we argue for the essential roles of scientists from many disciplines concerned with biological diversity and its conservation. We look beyond species endangerment to future generations' interests in sustainability, particularly non‐consumptive uses. Although our conclusions apply to all wild organisms, we focus on predators because of the particular challenges they pose for government trustees, trust managers, and society. Gray wolves Canis lupus L. deserve particular attention, because detailed information and abundant policy debates across regions have exposed four important challenges for preserving predators in the face of interest group hostility. One challenge is uncertainty and varied interpretations about public trustees' responsibilities for wildlife, which have created a mosaic of policies across jurisdictions. We explore how such mosaics have merits and drawbacks for biodiversity. The other three challenges to conserving wildlife as public trust assets are illuminated by the biology of predators and the interacting behavioural ecologies of humans and predators. The scientific community has not reached consensus on sustainable levels of human‐caused mortality for many predator populations. This challenge includes both genuine conceptual uncertainty and exploitation of scientific debate for political gain. Second, human intolerance for predators exposes value conflicts about preferences for some wildlife over others and balancing majority rule with the protection of minorities in a democracy. We examine how differences between traditional assumptions and scientific studies of interactions between people and predators impede evidence‐based policy. Even if the prior challenges can be overcome, well‐reasoned policy on wild animals faces a greater challenge than other environmental assets because animals and humans change behaviour in response to each other in the short term. These coupled, dynamic responses exacerbate clashes between uses that deplete wildlife and uses that enhance or preserve wildlife. Viewed in this way, environmental assets demand sophisticated, careful accounting by disinterested trustees who can both understand the multidisciplinary scientific measurements of relative costs and benefits among competing uses, and justly balance the needs of all beneficiaries including future generations. Without public trust principles, future trustees will seldom prevail against narrow, powerful, and undemocratic interests. Without conservation informed by public trust thinking predator populations will face repeated cycles of eradication and recovery. Our conclusions have implications for the many subfields of the biological sciences that address environmental trust assets from the atmosphere to aquifers.     

Phantoms of the forest: legacy risk effects of a regionally extinct large carnivore

The increased abundance of large carnivores in Europe is a conservation success, but the impact on the behavior and population dynamics of prey species is generally unknown. In Europe, the recolonization of large carnivores often occurs in areas where humans have greatly modified the landscape through forestry or agriculture. Currently, we poorly understand the effects of recolonizing large carnivores on extant prey species in anthropogenic landscapes. Here, we investigated if ungulate prey species showed innate responses to the scent of a regionally exterminated but native large carnivore, and whether the responses were affected by human‐induced habitat openness. We experimentally introduced brown bear Ursus arctos scent to artificial feeding sites and used camera traps to document the responses of three sympatric ungulate species. In addition to controls without scent, reindeer scent Rangifer tarandus was used as a noncarnivore, novel control scent. Fallow deer Dama dama strongly avoided areas with bear scent. In the presence of bear scent, all ungulate species generally used open sites more than closed sites, whereas the opposite was observed at sites with reindeer scent or without scent. The opening of forest habitat by human practices, such as forestry and agriculture, creates a larger gradient in habitat openness than available in relatively unaffected closed forest systems, which may create opportunities for prey to alter their habitat selection and reduce predation risk in human‐modified systems that do not exist in more natural forest systems. Increased knowledge about antipredator responses in areas subjected to anthropogenic change is important because these responses may affect prey population dynamics, lower trophic levels, and attitudes toward large carnivores. These aspects may be of particular relevance in the light of the increasing wildlife populations across much of Europe.     

Lethal interactions among forest‐grouse predators are numerous,motivated by hunger and carcasses,and their impacts determined by the demographic value of the victims

New vertebrate communities are emerging in Europe following the recovery of multiple native predators to highly anthropized landscapes where predator control is still prevalent. While the lack of reference points for these communities creates novel challenges for conservationists and wildlife managers, they also provide opportunities to further our understanding of species interactions. Despite a growing body of evidence, many aspects of interactions among predators remain poorly understood, impairing our ability to anticipate the effects of such changes in predator communities. Through a systematic literature review, we gathered all the available evidence concerning the existence, strength, and demographic impacts of lethal predator interactions among forest‐grouse predators in Europe. We found a highly interconnected predator community, with 44 pairwise lethal interactions among 12 taxa. Three of these resulted in some degree of population suppression of the victim, while another three did not. However, most interactions (38) have not been evaluated for population suppression. Additionally, we highlight how predators interact simultaneously with a large range of other predators and identified at least two further taxa possibly suppressed through the combined impacts of multiple predators. We propose that interactions causing demographic suppression are characterized by impacts on individuals with high survival elasticity and that they are motivated by food limitation and additionally, in mammals, by competition for carcasses. Predator interactions, and our still poor understanding of them, introduce large uncertainties to conservation actions based on the management of predator abundances, which should be carefully evaluated.     

Do the antipredator strategies of shared prey mediate intraguild predation and mesopredator suppression?

Understanding the conditions that facilitate top predator effects upon mesopredators and prey is critical for predicting where these effects will be significant. Intraguild predation (IGP) and the ecology of fear are hypotheses used to describe the effects of top predators upon mesopredators and prey species, but make different assumptions about organismal space use. The IGP hypothesis predicts that mesopredator resource acquisition and risk are positively correlated, creating a fitness deficit. But if shared prey also avoid a top predator, then mesopredators may not have to choose between risk and reward. Prey life history may be a critical predictor of how shared prey respond to predation and may mediate mesopredator suppression. We used hierarchical models of species distribution and abundance to test expectations of IGP using two separate triangular relationships between a large carnivore, smaller intraguild carnivore, and shared mammalian prey with different life histories. Following IGP, we expected that a larger carnivore would suppress a smaller carnivore if the shared prey species did not spatially avoid the large carnivore at broad scales. If prey were fearful over broad scales, we expected less evidence of mesopredator suppression. We tested these theoretical hypotheses using remote camera detections across a large spatial extent. Lagomorphs did not appear to avoid coyotes, and fox detection probability was lower as coyote abundance increased. In contrast, white‐tailed deer appeared to avoid areas of increased wolf use, and coyote detection probability was not reduced at sites where wolves occurred. These findings suggest that mesopredator suppression by larger carnivores may depend upon the behavior of shared prey, specifically the spatial scale at which they perceive risk. We further discuss how extrinsic environmental factors may contribute to mesopredator suppression.     

Predator interactions, mesopredator release and biodiversity conservation

There is growing recognition of the important roles played by predators in regulating ecosystems and sustaining biodiversity. Much attention has focused on the consequences of predator-regulation of herbivore populations, and associated trophic cascades. However apex predators may also control smaller 'mesopredators' through intraguild interactions. Removal of apex predators can result in changes to intraguild interactions and outbreaks of mesopredators ('mesopredator release'), leading in turn to increased predation on smaller prey. Here we provide a review and synthesis of studies of predator interactions, mesopredator release and their impacts on biodiversity. Mesopredator suppression by apex predators is widespread geographically and taxonomically. Apex predators suppress mesopredators both by killing them, or instilling fear, which motivates changes in behaviour and habitat use that limit mesopredator distribution and abundance. Changes in the abundance of apex predators may have disproportionate (up to fourfold) effects on mesopredator abundance. Outcomes of interactions between predators may however vary with resource availability, habitat complexity and the complexity of predator communities. There is potential for the restoration of apex predators to have benefits for biodiversity conservation through moderation of the impacts of mesopredators on their prey, but this requires a whole-ecosystem view to avoid unforeseen negative effects.

'Nothing has changed since I began.
My eye has permitted no change.
I am going to keep things like this.'
From 'Hawk Roosting', by Ted Hughes.

     

Human activity helps prey win the predator-prey space race

Predator-prey interactions, including between large mammalian wildlife species, can be represented as a "space race", where prey try to minimize and predators maximize spatial overlap. Human activity can also influence the distribution of wildlife species. In particular, high-human disturbance can displace large carnivore predators, a trait-mediated direct effect. Predator displacement by humans could then indirectly benefit prey species by reducing predation risk, a trait-mediated indirect effect of humans that spatially decouples predators from prey. The purpose of this research was to test the hypothesis that high-human activity was displacing predators and thus indirectly creating spatial refuge for prey species, helping prey win the "space race". We measured the occurrence of eleven large mammal species (including humans and cattle) at 43 camera traps deployed on roads and trails in southwest Alberta, Canada. We tested species co-occurrence at camera sites using hierarchical cluster and nonmetric multidimensional scaling (NMS) analyses; and tested whether human activity, food and/or habitat influenced predator and prey species counts at camera sites using regression tree analysis. Cluster and NMS analysis indicated that at camera sites humans co-occurred with prey species more than predator species and predator species had relatively low co-occurrence with prey species. Regression tree analysis indicated that prey species were three times more abundant on roads and trails with >32 humans/day. However, predators were less abundant on roads and trails that exceeded 18 humans/day. Our results support the hypothesis that high-human activity displaced predators but not prey species, creating spatial refuge from predation. High-human activity on roads and trails (i.e., >18 humans/day) has the potential to interfere with predator-prey interactions via trait-mediated direct and indirect effects. We urge scientist and managers to carefully consider and quantify the trait-mediated indirect effects of humans, in addition to direct effects, when assessing human impacts on wildlife and ecosystems.     

The ecology of fear and inverted biomass pyramids

In inverted biomass pyramids (IBPs) prey are outnumbered by their predators when measured by biomass. We investigate how prey should behave in the face of danger from higher predator biomass, and how anti-predator behavior (in the form of vigilance) can, in turn, affect the predator–prey system. In this study, we incorporate anti-predator behaviors into a Lotka–Volterra predator–prey model in the form of fixed and facultative vigilance. Facultative vigilance models behavior as a dynamic foraging game, allowing us to assess optimal behavioral responses in the context of IBPs using a dynamical fitness optimization approach. We model vigilance as a tradeoff between safety and either the prey's maximum growth rate or its carrying capacity. We assess the population dynamics of predators and prey with fear responses, and investigate the role fear plays on trophic structure. We found that the ecology of fear plays an important role in predator–prey systems, impacting trophic structure and the occurrence of IBPs. Fixed vigilance works against IBP structure by always reducing the predator–prey biomass ratio at equilibrium with increasing levels of vigilance. Facultative vigilance can actually promote IBPs, as prey can now adjust their vigilance levels to cope with increased predation and the costs associated with vigilance. This is especially true when the effectiveness of vigilance is low and predators are very lethal. In general, these trends are true whether the costs of vigilance are felt on the prey's maximum growth rate or its carrying capacity. Just as the ecology of fear, when first introduced, was used to explain why top carnivores are rare in terrestrial systems, it can also be used to understand how big fierce predators can be common in IBPs.     

Hazardous duty pay and the foraging cost of predation

We review the concepts and research associated with measuring fear and its consequences for foraging. When foraging, animals should and do demand hazardous duty pay. They assess a foraging cost of predation to compensate for the risk of predation or the risk of catastrophic injury. Similarly, in weighing foraging options, animals tradeoff food and safety. The foraging cost of predation can be modelled, and it can be quantitatively and qualitatively measured using risk titrations. Giving‐up densities (GUDs) in depletable food patches and the distribution of foragers across safe and risky feeding opportunities are two frequent experimental tools for titrating food and safety. A growing body of literature shows that: (i) the cost of predation can be big and comprise the forager's largest foraging cost, (ii) seemingly small changes in habitat or microhabitat characteristics can lead to large changes in the cost of predation, and (iii) a forager's cost of predation rises with risk of mortality, the forager's energy state and a decrease in its marginal value of energy. In titrating for the cost of predation, researchers have investigated spatial and temporal variation in risk, scale‐dependent variation in risk, and the role of predation risk in a forager's ecology. A risk titration from a feeding animal often provides a more accurate behavioural indicator of predation risk than direct observations of predator‐inflicted mortality. Titrating for fear responses in foragers has some well‐established applications and holds promise for novel methodologies, concepts and applications. Future directions for expanding conceptual and empirical tools include: what are the consequences of foraging costs arising from interference behaviours and other sources of catastrophic loss? Are there alternative routes by which organisms can respond to tradeoffs of food and safety? What does an animal's landscape of fear look like as a spatially explicit map, and how do various environmental factors affect it? Behavioural titrations will help to illuminate these issues and more.     

Complex interactions among mammalian carnivores in Australia, and their implications for wildlife management

Mammalian carnivore populations are often intensively managed, either because the carnivore in question is endangered, or because it is viewed as a pest and is subjected to control measures, or both. Most management programmes treat carnivore species in isolation. However, there is a large and emerging body of evidence to demonstrate that populations of different carnivores interact with each other in a variety of complex ways. Thus, the removal or introduction of predators to or from a system can often affect other species in ways that are difficult to predict. Wildlife managers must consider such interactions when planning predator control programmes. Integrated predator control will require a greater understanding of the complex relationships between species. In many parts of the world, sympatric species of carnivores have coexisted over an evolutionary time scale so that niche differentiation has occurred, and competition is difficult to observe. Australia has experienced numerous introductions during the past 200 years, including those of the red fox (Vulpes vulpes) and the feral cat (Felis catus). These species now exist in sympatry with native mammalian predators, providing ecologists with the opportunity to study their interactions without the confounding effects of coevolution. Despite an increasing body of observational evidence for complex interactions among native and introduced predators in Australia, few studies have attempted to clarify these relationships experimentally, and the interactions remain largely unacknowledged. A greater understanding of these interactions would provide ecologists and wildlife managers world-wide with the ability to construct robust predictive models of carnivore communities, and to identify their broader effects on ecosystem functioning. We suggest that future research should focus on controlled and replicated predator removal or addition experiments. The dingo (Canis lupus dingo), as a likely keystone species, should be a particular focus of attention.     

Top carnivores increase their kill rates on prey as a response to human-induced fear

The fear induced by predators on their prey is well known to cause behavioural adjustments by prey that can ripple through food webs. Little is known, however, about the analogous impacts of humans as perceived top predators on the foraging behaviour of carnivores. Here, we investigate the influence of human-induced fear on puma foraging behaviour using location and prey consumption data from 30 tagged individuals living along a gradient of human development. We observed strong behavioural responses by female pumas to human development, whereby their fidelity to kill sites and overall consumption time of prey declined with increasing housing density by 36 and 42%, respectively. Females responded to this decline in prey consumption time by increasing the number of deer they killed in high housing density areas by 36% over what they killed in areas with little residential development. The loss of food from declines in prey consumption time paired with increases in energetic costs associated with killing more prey may have consequences for puma populations, particularly with regard to reproductive success. In addition, greater carcass availability is likely to alter community dynamics by augmenting food resources for scavengers. In light of the extensive and growing impact of habitat modification, our study emphasizes that knowledge of the indirect effects of human activity on animal behaviour is a necessary component in understanding anthropogenic impacts on community dynamics and food web function.     

Non‐consumptive effects of a top‐predator decrease the strength of the trophic cascade in a four‐level terrestrial food web

The fear of predators can strongly impact food web dynamics and ecosystem functioning through effects on herbivores morphology, physiology or behaviour. While non‐consumptive predator effects have been mostly studied in three‐level food chains, we lack evidence for the propagation of non‐consumptive indirect effects of apex predators in four level food‐webs, notably in terrestrial ecosystems. In experimental mesocosms, we manipulated a four‐level food chain including top‐predator cues (snakes), mesopredators (lizards), herbivores (crickets), and primary producers (plants). The strength of the trophic cascade induced by mesopredators through the consumption of herbivores decreased in the presence of top‐predator cues. Specifically, primary production was higher in mesocosms where mesopredators were present relative to mesocosms with herbivores only, and this difference was reduced in presence of top‐predator cues, probably through a trait‐mediated effect on lizard foraging. Our study demonstrates that non‐consumptive effects of predation risk can cascade down to affect both herbivores and plants in a four‐level terrestrial food chain and emphasises the need to quantify the importance of such indirect effects in natural communities.     

Living and dying in a multi‐predator landscape of fear: roe deer are squeezed by contrasting pattern of predation risk imposed by lynx and humans

The theory of predation risk effects predicts behavioral responses in prey when risk of predation is not homogenous in space and time. Prey species are often faced with a tradeoff between food and safety in situations where food availability and predation risk peak in the same habitat type. Determining the optimal strategy becomes more complex if predators with different hunting mode create contrasting landscapes of risk, but this has rarely been documented in vertebrates. Roe deer in southeastern Norway face predation risk from lynx, as well as hunting by humans. These two predators differ greatly in their hunting methods. The predation risk from lynx, an efficient stalk‐and‐ambush predator is expected to be higher in areas with dense understory vegetation, while predation risk from human hunters is expected to be higher where visual sight lines are longer. Based on field observations and airborne LiDAR data from 71 lynx predation sites, 53 human hunting sites, 132 locations from 15 GPS‐marked roe deer, and 36 roe deer pellet locations from a regional survey, we investigated how predation risk was related to terrain attributes and vegetation classes/structure. As predicted, we found that increasing cover resulted in a contrasting lower predation risk from humans and higher predation risk from lynx. Greater terrain ruggedness increased the predation risk from both predators. Hence, multiple predators may create areas of contrasting risk as well as double risk in the same landscape. Our study highlights the complexity of predator–prey relationship in a multiple predator setting. Synthesis In this study of risk effects in a multi‐predator context, LiDAR data were used to quantify cover in the habitat and relate it to vulnerability to predation in a boreal forest. We found that lynx and human hunters superimpose generally contrasting landscapes of fear on a common prey species, but also identified double‐risk zones. Since the benefit of anti‐predator responses depends on the combined risk from all predators, it is necessary to consider complete predator assemblages to understand the potential for and occurrence of risk effects across study systems.     

A landscape of coexistence for a large predator in a human dominated landscape

Human related mortality is a major threat for large carnivores all over the world and there is increasing evidence that large predators respond to human related risks in a similar way as prey respond to predation risk. This insight recently led to the conceptual development of a landscape of coexistence that can be used to identify areas which can sustain large predator populations in human dominated landscapes. In this study we applied the landscape of coexistence concept to a large predator in Europe. We investigated to what extent Eurasian lynx Lynx lynx habitat selection is affected by human disturbance in a human dominated landscape. More specifically, we were interested in the existence of a tradeoff between the availability of roe deer, one of their main prey and avoidance of human disturbance and how this affects the spatio‐temporal space use patterns of lynx. We found that lynx face a tradeoff between high prey availability and avoidance of human disturbance and that they respond to this by using areas of high prey availability (but also high human disturbance) during the night when human activity is low. Furthermore our analysis showed that lynx increase their travelling speed and remain more in cover when they are close to areas of high human disturbance. Despite clear behavioral adjustments in response to human presence, prey availability still proved to be the most important predictor of lynx occurrence at small spatial scale, whereas human disturbance was considerably less important. The results of our study demonstrate how spatio‐temporal adaptations in habitat selection enable large carnivores to persist in human dominated landscapes and demonstrate the usefulness of the concept of a landscape of coexistence to develop adaptive management plans for endangered populations of large carnivores.     

Reintroduced wolves and hunting limit the abundance of a subordinate apex predator in a multi-use landscape

Top-down effects of apex predators are modulated by human impacts on community composition and species abundances. Consequently, research supporting top-down effects of apex predators occurs almost entirely within protected areas rather than the multi-use landscapes dominating modern ecosystems. Here, we developed an integrated population model to disentangle the concurrent contributions of a reintroduced apex predator, the grey wolf, human hunting and prey abundances on vital rates and abundance of a subordinate apex predator, the puma. Increasing wolf numbers had strong negative effects on puma fecundity, and subadult and adult survival. Puma survival was also influenced by density dependence. Overall, puma dynamics in our multi-use landscape were more strongly influenced by top-down forces exhibited by a reintroduced apex predator, than by human hunting or bottom-up forces (prey abundance) subsidized by humans. Quantitatively, the average annual impact of human hunting on equilibrium puma abundance was equivalent to the effects of 20 wolves. Historically, wolves may have limited pumas across North America and dictated puma scarcity in systems lacking sufficient refugia to mitigate the effects of competition.