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.

Effects of predator control on behaviour of an apex predator and indirect consequences for mesopredator suppression

1. Apex predators can benefit ecosystems through top–down control of mesopredators and herbivores. However, apex predators are often subject to lethal control aimed at minimizing attacks on livestock. Lethal control can affect both the abundance and behaviour of apex predators. These changes could in turn influence the abundance and behaviour of mesopredators.

2. We used remote camera surveys at nine pairs of large Australian rangeland properties, comparing properties that controlled dingoes Canis lupus dingo with properties that did not, to test the effects of predator control on dingo activity and to evaluate the responses of a mesopredator, the feral cat Felis catus.

3. Indices of dingo abundance were generally reduced on properties that practiced dingo control, in comparison with paired properties that did not, although the effect size of control was variable. Dingoes in uncontrolled populations were crepuscular, similar to major prey. In populations subject to control, dingoes became less active around dusk, and activity was concentrated in the period shortly before dawn.

4. Shifts in feral cat abundance indices between properties with and without dingo control were inversely related to corresponding shifts in indices of dingo abundance. There was also a negative relationship between predator visitation rates at individual camera stations, suggesting cats avoided areas where dingoes were locally common. Reduced activity by dingoes at dusk was associated with higher activity of cats at dusk.

5. Our results suggest that effective dingo control not only leads to higher abundance of feral cats, but allows them to optimize hunting behaviour when dingoes are less active. This double effect could amplify the impacts of dingo control on prey species selected by cats. In areas managed for conservation, stable dingo populations may thus contribute to management objectives by restricting feral cat access to prey populations.

6. Synthesis and applications. Predator control not only reduces indices of apex predator abundance but can also modify their behaviour. Hence, indicators other than abundance, such as behavioural patterns, should be considered when estimating a predator's capacity to effectively interact with lower trophic guilds. Changes to apex predator behaviour may relax limitations on the behaviour of mesopredators, providing enhanced access to resources and prey.

Does fire influence the landscape-scale distribution of an invasive mesopredator?

Predation and fire shape the structure and function of ecosystems globally. However, studies exploring interactions between these two processes are rare, especially at large spatial scales. This knowledge gap is significant not only for ecological theory, but also in an applied context, because it limits the ability of landscape managers to predict the outcomes of manipulating fire and predators. We examined the influence of fire on the occurrence of an introduced and widespread mesopredator, the red fox (Vulpes vulpes), in semi-arid Australia. We used two extensive and complimentary datasets collected at two spatial scales. At the landscape-scale, we surveyed red foxes using sand-plots within 28 study landscapes - which incorporated variation in the diversity and proportional extent of fire-age classes - located across a 104 000 km2 study area. At the site-scale, we surveyed red foxes using camera traps at 108 sites stratified along a century-long post-fire chronosequence (0-105 years) within a 6630 km2 study area. Red foxes were widespread both at the landscape and site-scale. Fire did not influence fox distribution at either spatial scale, nor did other environmental variables that we measured. Our results show that red foxes exploit a broad range of environmental conditions within semi-arid Australia. The presence of red foxes throughout much of the landscape is likely to have significant implications for native fauna, particularly in recently burnt habitats where reduced cover may increase prey species' predation risk.

Demonising the dingo : how much wild dogma is enough?

The roles that top predators play in regulating the structure and function of ecosystems have long been controversial. This is particularly the case when predators pose adverse risks for human life and/or economic interests. The critique of literature on dingoes and their ecological roles in Australia provided by Allen et al. (2011) shows that top predators remain a potentially polarising issue. In opposition to Allen et al. we argue that these widespread patterns of species’ abundances, attributed to the effects of dingoes and evident at scales ranging from the foraging behaviour of individuals through to continental scale patterns of species abundances, constitute strong support for the mesopredator release hypothesis and provide evidence that dingoes benefit biodiversity conservation by inducing community wide trophic cascades. Harnessing the positive ecological effects of dingoes while at the same time minimising their impacts on agriculture is a major socio-political challenge in Australia [Current Zoology 57 (5): 668-670].

Top predators as biodiversity regulators : the dingo Canis lupus dingo as a case study

Top-order predators often have positive effects on biological diversity owing to their key functional roles in regulating trophic cascades and other ecological processes. Their loss has been identified as a major factor contributing to the decline of biodiversity in both aquatic and terrestrial systems. Consequently, restoring and maintaining the ecological function of top predators is a critical global imperative. Here we review studies of the ecological effects of the dingo Canis lupus dingo, Australia's largest land predator, using this as a case study to explore the influence of a top predator on biodiversity at a continental scale. The dingo was introduced to Australia by people at least 3500 years ago and has an ambiguous status owing to its brief history on the continent, its adverse impacts on livestock production and its role as an ecosystem architect. A large body of research now indicates that dingoes regulate ecological cascades, particularly in arid Australia, and that the removal of dingoes results in an increase in the abundances and impacts of herbivores and invasive mesopredators, most notably the red fox Vulpes vulpes. The loss of dingoes has been linked to widespread losses of small and medium-sized native mammals, the depletion of plant biomass due to the effects of irrupting herbivore populations and increased predation rates by red foxes. We outline a suite of conceptual models to describe the effects of dingoes on vertebrate populations across different Australian environments. Finally, we discuss key issues that require consideration or warrant research before the ecological effects of dingoes can be incorporated formally into biodiversity conservation programs.

The dingo and biodiversity conservation : response to Fleming et al. (2012)

Several authors have recently argued that dingoes could be used to help conserve biodiversity in Australia. Fleming et al. (2012) [Australian Mammalogy 34, 119–131] offer the alternative view that restoration of dingo predation is unlikely to help native species, and is more likely to do harm. We think many of the arguments used by Fleming et al. to reach that conclusion are either unsound or beside the point, and we explain why.

Towards a cohesive, holistic view of top predation: a definition, synthesis and perspective

Research on the ecology of top predators - upper trophic level consumers that are relatively free from predation once they reach adult size - has provided regular contributions to general ecology and is a rapidly expanding and increasingly experimental, multidisciplinary and technological endeavour. Yet, an exponentially expanding literature coupled with rapid disintegration into specialized, disconnected subfields for study (e.g. vertebrate predators versus invertebrate predators, community ecology versus biological control etc.) increasingly means that we are losing a coherent, integrated understating of the role and importance of these species in ecosystems. This process of canalization is likely to hinder sharing of scientific discovery and continued progress, especially as there is a growing need to understand the generality of the top-down forcing, as demonstrated for some members of this group. Here, we propose ways to facilitate synthesis by promoting changes in mentality and awareness among specialists through increased debate and collaboration, conceptual reviews and a series of exemplary case studies. The strategy will rely on the collective contribution by all scientists in the field and will strive to consolidate and formalise top-order predation as a holistic, cohesive, cross-taxonomical field of research studying the ecology, evolution and behaviour of apex predators and their capability to exert top-down forcing on lower trophic levels. © 2014 The Authors.

Dingoes can help conserve wildlife and our methods can tell

Management of apex predators is among the most controversial wildlife management issues globally. In Australia, some ecologists have advocated using the dingo, Canis dingo, as a tool for conservation management, due to evidence that they suppress invasive mesopredators. Hayward & Marlow (Journal of Applied Ecology, 51, 2014 and 835) questioned the capacity of dingoes to provide benefits to native biodiversity due to their inability to eradicate foxes and cats. They also argued that indices of abundance commonly used in studies of mesopredator release by dingoes (namely, track-based indices) invalidate the conclusions of the studies. Hayward & Marlow caution conservation practitioners against incorporating dingoes into conservation programmes. Counter to their claims, we summarise research showing that the suppression of invasive mesopredators (cf. eradication) can enhance populations of native species and is therefore a meaningful conservation objective. We highlight literature supporting the hypothesis that dingoes suppress mesopredator abundance and activity, which in turn benefits native biodiversity. We show that Hayward & Marlow overlook many studies of carnivores that show track indices capture a large amount of the variation in the density of medium- and large-sized carnivores. Synthesis and applications. Practitioners cannot afford to wait to act given the perilous state of Australia's mammal species, and we argue that the evidence is sufficiently strong to justify managing dingoes for biodiversity conservation.

Resolving the value of the dingo in ecological restoration

There is global interest in restoring populations of apex predators, both to conserve them and to harness their ecological services. In Australia, reintroduction of dingoes (Canis dingo) has been proposed to help restore degraded rangelands. This proposal is based on theories and the results of studies suggesting that dingoes can suppress populations of prey (especially medium- and large-sized herbivores) and invasive predators such as red foxes (Vulpes vulpes) and feral cats (Felis catus) that prey on threatened native species. However, the idea of dingo reintroduction has met opposition, especially from scientists who query the dingo's positive effects for some species or in some environments. Here, we ask 'what is a feasible experimental design for assessing the role of dingoes in ecological restoration?' We outline and propose a dingo reintroduction experiment-one that draws upon the existing dingo-proof fence-and identify an area suitable for this (Sturt National Park, western New South Wales). Although challenging, this initiative would test whether dingoes can help restore Australia's rangeland biodiversity, and potentially provide proof-of-concept for apex predator reintroductions globally.

Incorporating anthropogenic effects into trophic ecology: predator-prey interactions in a human-dominated landscape

Apex predators perform important functions that regulate ecosystems worldwide. However, little is known about how ecosystem regulation by predators is influenced by human activities. In particular, how important are top-down effects of predators relative to direct and indirect human-mediated bottom-up and top-down processes? Combining data on species' occurrence from camera traps and hunting records, we aimed to quantify the relative effects of top-down and bottom-up processes in shaping predator and prey distributions in a human-dominated landscape in Transylvania, Romania. By global standards this system is diverse, including apex predators (brown bear and wolf), mesopredators (red fox) and large herbivores (roe and red deer). Humans and free-ranging dogs represent additional predators in the system. Using structural equation modelling, we found that apex predators suppress lower trophic levels, especially herbivores. However, direct and indirect top-down effects of humans affected the ecosystem more strongly, influencing species at all trophic levels. Our study highlights the need to explicitly embed humans and their influences within trophic cascade theory. This will greatly expand our understanding of species interactions in human-modified landscapes, which compose the majority of the Earth's terrestrial surface.

Multiple threats, or multiplying the threats? Interactions between invasive predators and other ecological disturbances

Invasive species have reshaped the composition of biomes across the globe, and considerable cost is now associated with minimising their ecological, social and economic impacts. Mammalian predators are among the most damaging invaders, having caused numerous species extinctions. Here, we review evidence of interactions between invasive predators and six key threats that together have strong potential to influence both the impacts of the predators, and their management. We show that impacts of invasive predators can be classified as either functional or numerical, and that they interact with other threats through both habitat- and community-mediated pathways. Ecosystem context and invasive predator identity are central in shaping variability in these relationships and their outcomes. Greater recognition of the ecological complexities between major processes that threaten biodiversity, including changing spatial and temporal relationships among species, is required to both advance ecological theory and improve conservation actions and outcomes. We discuss how novel approaches to conservation management can be used to address interactions between threatening processes and ameliorate invasive predator impacts.

How small-scale variation in oyster reef patchiness influences predation on bivalves

As oyster fishing continues to degrade reef habitat along the US Atlantic coast, oyster reefs appear increasingly fragmented on small spatial scales. In outdoor mesocosms, experiments tested how consumption of representatives of 4 different bivalve guilds by each of 3 mesopredators varies between continuous and fine-scale patches of oyster reef habitat. The mesopredator that fed least (stone crab) exhibited no detectable change in consumption on any bivalve (ribbed mussel, bay scallop, hard clam, and 3 size classes of eastern oyster). Consumption of bay scallops by both blue crabs and sheepshead fish was greater in small patches than in continuous oyster reef habitat. Of the bivalve guilds tested, only the scallop possesses swimming motility sufficient to reduce predation, an escape response that would likely leave the bivalve protected within structured habitat in larger continuous oyster reefs. Sheepshead consumed more small oysters in the continuous habitat than in the fine patches, while no other predator-prey interaction exhibited differential feeding as a function of habitat patchiness. Consequently, predation by mesopredators on bivalves can vary with the scale of oyster reef patchiness, but this process may depend upon the bivalve guild. Understanding the role of habitat patchiness on fine scales may be increasingly important in view of the declines in apex predatory sharks leading to mesopredator release, and global climate change directly and indirectly enhancing stone crab abundances, thereby increasing potential predation on bivalves.

Stop jumping the gun : a call for evidence-based invasive predator management

Invasive mammalian predators are major drivers of species extinctions globally. To protect native prey, lethal control is often used with the aim of reducing or exterminating invasive predator populations. The efficacy of this practice, however, is often not considered despite multiple practical and ecological factors that can limit success. Here, we summarize contemporary knowledge regarding the use and challenges of both lethal control and alternative approaches for reducing invasive predator impacts. As the prevailing management approach, we outline four key issues that can compromise the effectiveness of lethal control: release of herbivore and mesopredator populations, disruption of predator social systems, compensatory predator immigration, and ethical concerns. We then discuss the relative merits and limitations of four alternative approaches that may enhance conservation practitioner's ability to effectively manage invasive predators: top-predator conservation or reintroduction, maintaining habitat complexity, exclusion fencing, and behavioral and evolutionary ecology. Considerable uncertainty remains regarding the effectiveness of management approaches in different environmental contexts. We propose that the deficiencies and uncertainties outlined here can be addressed through a combination of adaptive management, expert elicitation, and cost-benefit analyses. Improved management of invasive predators requires greater consideration and assessment of the full range of management approaches available.

Crying wolf: limitations of predator-prey studies need not preclude their salient messages.

A rapidly growing body of the literature reveals the important roles apex predators play in shaping the composition and functioning of ecological communities worldwide. The principal effects of apex predators—namely herbivore and mesopredator population suppression—are often evident following their removal from environments, or their reintroduction, including rewilding initiatives. What remains less clear, however, is to what extent humans versus other apex predators affect ecosystems, how both interact across gradients of anthropogenic pressure and how such interactions can be affected by underlying bottom-up processes. Such questions are critical to answer in the Anthropocene, where effective management of ecosystems and conservation of biodiversity requires a better understanding of how top-down and bottom-up processes vary according to anthropogenic influences.