OPEN Human disturbance thresholds determine the ecological role of an apex predator

OPEN Human disturbance thresholds determine the ecological role of an apex predator

The return of large carnivores to human-dominated landscapes complicates predator-prey dynamics. While predator and anthropogenic effects are well-documented in intact systems, their interplay in fragmented landscapes remains understudied. We examined whether apex predators still regulate prey and mesopredators in the large mammal community of the Golan Heights-a mosaic of nature reserves, farmland and military zones-where wolves, golden jackals and wild boar are culled to mitigate agricultural losses and human-wildlife conflict. Using sixty camera traps and high-resolution culling data, we quantified predator-prey and intraguild relationships, identifying land protection thresholds at which they shifted. We found that endangered mountain gazelles were most active in protected areas (top fifty percent of sites) with higher wolf activity and consistently avoided jackals. Species-specific culling increased jackal activity but decreased boar activity in nonprotected areas (lower sixty-five percent and sixty-two percent of sites, respectively), outweighing the suppressive effects of wolves. While jackal culling modestly benefited gazelles in protected areas, the positive association between wolves and gazelles was sevenfold stronger. These findings suggest that apex predators may maintain their ecological roles in fragmented landscapes up to a threshold of human disturbance, beyond which top-down regulation weakens and ecosystem function deteriorates.

Large carnivores have undergone widespread declines globally due to various human pressures, including habitat loss, hunting and conflict with humans. However, recent improvements in conservation policies and legislative protection have facilitated their recovery in some human-dominated landscapes. These landscapes- characterized by extensive land modification, habitat fragmentation and agriculture-now cover approximately seventy-five percent of global terrestrial areas. Large carnivores function as apex predators in food webs, exerting far-reaching ecological impacts through both direct predation and indirect effects on prey and competitor behavior. Two key mechanisms underpinning these effects are (one) "landscape of fear", in which prey and mesopredators alter their spatial and temporal activity patterns in response to perceived predation risk, and (two) "mesopredator release", where the loss or suppression of apex predators allows mid-sized carnivores to proliferate, often leading to increased predation on their smaller prey. Together, these processes form the foundation of apex predator theory (used hereafter), which describes how top predators structure ecosystems through both lethal and non-lethal effects. While these dynamics are well-documented in relatively undisturbed landscapes, their applicability to human-modified systems remains less explored. As large carnivores recolonize increasingly altered habitats, research is needed to determine whether they retain key ecological functions or if human pressures disrupt their regulatory roles in these complex environments. This study examines how an apex predator interacts with both prey and mesopredators in a human-dominated landscape, identifying the thresholds at which its functional role is maintained or diminished.

Apex predators are expected to regulate predator-prey dynamics by controlling populations of large herbivores such as elk, white-tailed deer or wild boar which can overexploit native vegetation. Additionally, by exerting top-down pressure on intermediate-sized carnivores, apex predators are expected to control mesopredator populations that would otherwise impose strong predation pressure on smaller prey species. However, humanized habitats often favor highly adaptable mesopredators,

particularly those capable of exploiting anthropogenic resources such as garbage, crop fields, or domestic animal waste. This resource plasticity enables mesopredators such as foxes, raccoons and feral cats to thrive and spread even in the presence of larger carnivores. A striking example is the current rapid expansion of the golden jackal across Europe, which coincides with continental gray wolf recovery; yet, the ecological consequences of this expansion and the extent to which wolf recovery may regulate it remain largely understudied. While some studies from human-dominated landscapes suggest apex predators suppress both herbivores and mesopredators, human disturbance can often confound these trophic dynamics and obscure efforts to quantify them. In ecosystems already strained by human pressures, understanding the capacity of apex predators to fulfill their ecological roles is essential to inform conservation and management strategies.

Even when apex predators successfully recolonize human-dominated areas, they face a wide range of novel anthropogenic pressures. Habitat fragmentation, human activity in wild areas, depletion of wild prey substituted by domestic animals and human-wildlife conflict can all affect predator distribution and behavior patterns, as well as the way they interact with species at lower trophic levels. Among these pressures, culling management is a widespread tool for reducing livestock depredation. While culling has shown some success with solitary carnivores such as American black bears and Eurasian lynx, social species often exhibit compensatory behaviors like increased reproduction or dispersal, making long-term control difficult. Furthermore, heavy culling can threaten population viability when thresholds are exceeded. Beyond direct interventions, extensive land-use changes such as agricultural expansion and urban development reduce habitat availability and disrupt the spatiotemporal patterns of interspecific interactions. Taken together, these overlapping pressures challenge the capacity of apex predators to maintain their ecological roles in human-modified landscapes.

As human-induced pressures intensify, natural trophic interactions within ecosystems can break down, disrupting or collapsing ecological balance. An ecosystem out of balance reveals a critical breaking point, i.e., a threshold beyond which ecosystems lose their capacity for natural regulation. Notably, this breaking point does not necessarily correspond to the extinction of apex predators but marks the boundary at which they cease to realize their ecological roles, even in seemingly suitable habitats. Where apex predators have become functionally extinct, humans may replace apex predators as the dominant regulatory force, directly and indirectly controlling prey and mesopredator populations. For example, overhunting of prey species can reduce predator numbers and weaken top-down control, while anthropogenic food subsidies, such as livestock carcasses, garbage dumps and crop surpluses, can eliminate natural bottom-up regulation such that mesopredator or prey populations inflate beyond the regulatory capacity of natural top-down control. In some cases, apex predators themselves may become reliant on these human-provided resources, further weakening their role in structuring ecological communities. While these dynamics highlight the complexity of predator-prey interactions in anthropogenic landscapes, the thresholds at which apex predators lose their regulatory function remain poorly understood, particularly in fragmented or actively managed landscapes. A key challenge is disentangling natural trophic interactions from anthropogenic influences affecting species' spatiotemporal patterns at the community level. As landscapes become increasingly fragmented and shared among humans and wildlife, quantifying breaking points of predator-prey interactions is crucial for understanding how factors such as land use, resource availability and human activity shape the capacity of apex predators to maintain ecological balance in diverse multi-use landscapes.

The Golan Heights in the Middle East provides an ideal system for testing apex predator function in a human-dominated mosaic landscape, as it hosts high biodiversity in a matrix of diverse land uses, including agriculture, recreation and military activity. Over the past half-century, wildlife protection laws and increased cattle and crop availability have allowed wildlife in this region to recover substantially, resulting in some of the highest global densities of grey wolves, golden jackals and wild boar; it is also a last stronghold of the endangered mountain gazelle. Although all wild species are legally protected, wolf, jackal and wild boar populations are actively managed through culling programs to mitigate livestock depredation and crop damage. This unique context-characterized by apex predator recovery, high mesopredator densities and human intervention-offers a rare opportunity to examine how predators retain their ecological roles in a fragmented landscape. By leveraging fine-scale culling data across multiple trophic levels, we can assess community-level responses to both natural and anthropogenic pressures, identifying the thresholds at which human activity disrupts apex predator function.

We asked whether apex predator theory holds in a mosaic landscape where predator-prey dynamics are influenced by both natural and human-mediated factors. We analyzed the population-level responses of gazelles, wild boar, jackals and wolves to the combined pressures of predation, culling and land management. We hypothesized that: Wolves and jackals, abundant sympatric predators of mountain gazelles, would suppress gazelle activity, reflecting additive top-down control; Consequently, areas with intense wolf and jackal culling would serve as conservation refuges for gazelles, given the known link between dense predator populations and increased fawn mortality; Increased wolf activity would suppress jackal and wild boar activity, in line with the mesopredator release and landscape of fear theories and wolves' known reliance on boar as prey in Mediterranean landscapes. This effect would demonstrate wolves' ecological role in regulating both mesopredators and prey; Lastly, anthropogenic pressures, such as culling and land use change, would either outweigh or interact with natural trophic interactions to shape the structure of the large mammal community, as observed in other fragmented landscapes where human activities often overwhelm natural ecological processes.

To test these hypotheses, we applied integrated N-mixture and structural equation models to systematic camera trap data, incorporating high-resolution culling records and land-use layers to quantify lethal risk and human disturbance gradients for apex predators, mesopredators and prey. We used a priori directed acyclic graphs to visualize hypothesized relationships among species, natural predator-prey dynamics and human-mediated pressures. Our findings reveal that even in a fragmented, human-dominated landscape, apex predators remain functionally important within remaining protected patches, amplifying the ecological benefits of these areas. We also found that the suppressive effect of mesopredator culling was amplified within refugia but reversed outside them, suggesting that apex predators' regulatory control begins to deteriorate with increasing anthropogenic pressure.

Results

We generated twenty-three thousand independent detections of our four study species, comprising one thousand forty-three independent detections of wolves, eleven thousand nine hundred fifty-nine of jackals, four thousand nine hundred thirty-seven of wild boar and five thousand sixty-one of mountain gazelles. Naive occupancy, or the proportion of sampling locations with detections, was high for all four species-ninety-five percent for wolves, one hundred percent for jackals, ninety-seven percent for wild boar and eighty-eight percent for gazelles. Jackals were the most abundant species, averaging one hundred forty-nine point four six plus or minus sixty-seven point five four standard deviation sightings per two-week period per sampling location, followed by wild boar one hundred twenty-nine point one three plus or minus sixty-seven point seven nine standard deviation, gazelle one hundred twelve point six one plus or minus forty-five point one zero standard deviation and lastly wolves twenty-six point zero eight plus or minus eight point zero three standard deviation.

Our top structural equation model linked three species-specific GLMs for jackal, wild boar, and gazelle, with wolf activity modeled exogenously. This structure ranked above alternative structural equation models that included a separate wolf GLM. Parallel N-mixture models produced consistent patterns but showed poorer fit and less stable P-values.