Relaxation of risk-sensitive behaviour of prey following disease-induced decline of an apex predator, the Tasmanian devil

Hollings, Tracey; McCallum, Hamish; Kreger, Kaely; Mooney, Nick; Jones, Menna Lloyd

doi:10.1098/rspb.2015.0124

Cited by 23 publications

(26 citation statements)

References 44 publications

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“…GUDs at one study site on Maria Island appeared to deviate from the Figure 2. (a) Effects plot from the best-supported LMM investigating possum GUDs before and after the introduction of devils to Maria Island. This demonstrates that GUDs were indistinguishable between the two regions in the 'before' period (Hollings et al 2015), however following the introduction of devils to Maria Island, GUDs were significantly higher on Maria Island than the control region. The solid dots represent the model fit and the transparent dots show the raw data.…”

Section: Possum Guds Were Initially Indistinguishable Between Mariamentioning

confidence: 80%

“…Analysis during the 'before' period indicated that non-target species rarely took more than 15% of the food and never more than 25% (Hollings et al 2015). Analysis during the 'before' period indicated that non-target species rarely took more than 15% of the food and never more than 25% (Hollings et al 2015).…”

Section: Giving-up Density Experimentsmentioning

confidence: 96%

“…1), causing average population declines of 80% (Lazenby et al 2018) and up to 95% in some long-diseased areas (Hollings et al 2014). Where devils have declined severely, the common brushtail possum Trichosurus vulpecula, a key prey species of devils, now shows relaxed risk-sensitive foraging behaviour, as measured by a giving-up density (GUD) experiment (Hollings et al 2015). In GUD experiments, animals are offered artificial food patches in areas with varying predation risk, and the amount of food remaining when the forager 'gives-up' foraging is used to measure the perceived risk of predation (Brown 1988, Bedoya-Perez et al 2013.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2019

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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.

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Section: Possum Guds Were Initially Indistinguishable Between Mariamentioning

confidence: 80%

Section: Giving-up Density Experimentsmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 99%

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

et al. 2019

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“…It is costly for an organism to respond to predators that are extinct, therefore we should expect behavioural changes among prey to be rapid in the absence of predation (Lahti et al., ). After all, it is not in an animal's best interest to be overly cautious in environments under decreasing predator threat (Hollings et al., ). This assumption may partly explain why some prey responses to new predators are often learned during their development (Blumstein et al., ; Anson & Dickman, ; Carthey & Banks, ; Tortosa et al., ).…”

Section: Neurobiological Mechanisms Underlying Prey Responsesmentioning

confidence: 99%

Biologically meaningful scents: a framework for understanding predator–prey research across disciplines

et al. 2017

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Fear of predation is a universal motivator. Because predators hunt using stealth and surprise, there is a widespread ability among prey to assess risk from chemical information -scents -in their environment. Consequently, scents often act as particularly strong modulators of memory and emotions. Recent advances in ecological research and analytical technology are leading to novel ways to use this chemical information to create effective attractants, repellents and anti-anxiolytic compounds for wildlife managers, conservation biologists and health practitioners. However, there is extensive variation in the design, results, and interpretation of studies of olfactory-based risk discrimination. To understand the highly variable literature in this area, we adopt a multi-disciplinary approach and synthesize the latest findings from neurobiology, chemical ecology, and ethology to propose a contemporary framework that accounts for such disparate factors as the time-limited stability of chemicals, highly canalized mechanisms that influence prey responses, and the context within which these scents are detected (e.g. availability of alternative resources, perceived shelter, and ambient physical parameters). This framework helps to account for the wide range of reported responses by prey to predator scents, and explains, paradoxically, how the same individual predator scent can be interpreted as either safe or dangerous to a prey animal depending on how, when and where the cue was deposited. We provide a hypothetical example to illustrate the most common factors that influence how a predator scent (from dingoes, Canis dingo) may both attract and repel the same target organism (kangaroos, Macropus spp.). This framework identifies the catalysts that enable dynamic scents, odours or odorants to be used as attractants as well as deterrents. Because effective scent tools often relate to traumatic memories (fear and/or anxiety) that cause future avoidance, this information may also guide the development of appeasement, enrichment and anti-anxiolytic compounds, and help explain the observed variation in post-traumatic-related behaviours (including post-traumatic stress disorder, PTSD) among diverse terrestrial taxa, including humans.

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“…Wallabies also responded to the introduction of devils to Maria Island by increasing activity at periods of the day when devils are inactive (Cunningham et al ). Because possums are typically arboreal but often forage on the ground, the trends we show here could reflect changes in abundance or increased ground‐based activity by possums in response to a relaxed landscape of fear (Hollings et al ; Cunningham et al ).…”

Section: Discussionmentioning

confidence: 84%

A native apex predator limits an invasive mesopredator and protects native prey: Tasmanian devils protecting bandicoots from cats

2020

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Apex predators can limit the abundance and behaviour of mesopredators, thereby reducing predation on smaller species. We know less about whether native apex predators are effective in suppressing invasive mesopredators, a major global driver of vertebrate extinctions. We use the severe disease‐induced decline of an apex predator, the Tasmanian devil, as a natural experiment to test whether devils limit abundance of invasive feral cats and in turn protect smaller native prey. Cat abundance was c. 58% higher where devils had declined, which in turn negatively affected a smaller native prey species. Devils had a stronger limiting effect on cats than on a native mesopredator, suggesting apex predators may have stronger suppressive effects on evolutionarily naive species than coevolved species. Our results highlight how disease in one species can affect the broader ecosystem. We show that apex predators not only regulate native species but can also confer resistance to the impacts of invasive populations. Apex predators could therefore be a powerful but underutilised tool to prevent biodiversity loss.

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Relaxation of risk-sensitive behaviour of prey following disease-induced decline of an apex predator, the Tasmanian devil

Cited by 23 publications

References 44 publications

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

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

Biologically meaningful scents: a framework for understanding predator–prey research across disciplines

A native apex predator limits an invasive mesopredator and protects native prey: Tasmanian devils protecting bandicoots from cats

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