Deep evolutionary experience explains mammalian responses to predators

Atkins, Rosemary; Blumstein, Daniel T.; Moseby, Katherine E.; West, Rebecca; Hyatt, Matthew; Letnic, Mike

doi:10.1007/s00265-016-2181-4

Cited by 20 publications

(15 citation statements)

References 36 publications

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“…We compare the volatile chemical profiles of scat, urine and bedding (intended to capture integumentary or “skin/fur” odour) samples from four placental (dingoes, dogs, foxes and cats) and three marsupial (tiger quoll D. maculatus , eastern quoll D. viverrinus , and Tasmanian devil) predators of small and medium sized Australian mammal prey. Naivety of native prey to these placental predators’ cues has been well-documented 10 – for example, bush rats ( Rattus fuscipes ) do not avoid dog faecal odour 14 , 15 , tammar wallabies ( Macropus eugenii ) and red-necked pademelons ( Thylogale thetis ) ignore red fox faecal odour 12 , and bettongs ( Bettongia lesueur ) do not respond to red fox models 13 . We predicted that placental carnivore odour profiles would differ significantly and substantially from those of marsupial carnivores.…”

Section: Introductionmentioning

confidence: 99%

Novel predators emit novel cues: a mechanism for prey naivety towards alien predators

Carthey

Bucknall

Wierucka

et al. 2017

Sci Rep

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Detecting enemies is crucial for survival and a trait that develops over an evolutionary timeframe. Introduced species disrupt coevolved systems of communication and detection in their new ranges, often leading to devastating impacts. The classic example is prey naivety towards alien predators, whereby prey fail to recognise a new predator. Yet exactly why native prey fail to recognise alien predators remains puzzling. Naivety theory predicts that it is because novel predators emit novel cues. Distantly related animals have distinct evolutionary histories, physiologies and ecologies, predicting they will emit different cues. Yet it also possible that all predators emit similar cues because they are carnivorous. We investigate whether odour cues differ between placental and marsupial carnivores in Australia, where native prey experienced only marsupial mammal predation until ~4000 years ago. We compared volatile chemical profiles of urine, scats and bedding from four placental and three marsupial predators. Chemical profiles showed little overlap between placental and marsupial carnivores across all odour types, suggesting that cue novelty is a plausible mechanism for prey naivety towards alien predators. Our results also suggest a role for olfactory cues to complement visual appearance and vocalisations as biologically meaningful ways to differentiate species.

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Section: Introductionmentioning

confidence: 99%

Novel predators emit novel cues: a mechanism for prey naivety towards alien predators

Carthey

Bucknall

Wierucka

et al. 2017

Sci Rep

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“…This seems plausible, as long-nosed bandicoots (Perameles nasuta) do not recognize domestic dogs (Canis lupus familliaris; a close relative of the dingo) as a predation threat in Tasmania, despite >100 years of experience with dogs (Frank et al, 2016), yet they do recognize dogs on the Australian mainland, where dingoes have been present for ~4,000 years (Carthey & Banks, 2012). Thus, the historic predator community and the level of experience of prey with different predators is an important consideration when assessing the role of naiveté in novel predator-prey interactions, especially in facilitating discrimination (Atkins et al, 2016;Carthey & Blumstein, 2017;Ferrari, Wisenden, & Chivers, 2010).…”

Section: Discussionmentioning

confidence: 99%

“…The spread of alien species has been identified as one of the most important types of human‐induced rapid environmental change (HIREC; Sih, Ferrari, & Harris, ), which continues to force prey into evolutionarily novel situations. Understanding how native species are able to mount antipredator responses to alien predators (e.g., via learning and adaptation; Strauss, Lau, & Carroll, ) is thus crucial to determining their persistence (Atkins et al., ; Saxon‐Mills, Moseby, Blumstein, & Letnic, ).…”

Section: Introductionmentioning

confidence: 99%

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Overcoming prey naiveté: Free‐living marsupials develop recognition and effective behavioral responses to alien predators in Australia

Bytheway

Banks

2019

Global Change Biology

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Naiveté in prey arises from novel ecological mismatches in cue recognition systems and antipredator responses following the arrival of alien predators. The multilevel naiveté framework suggests that animals can progress through levels of naiveté toward predator awareness. Alternatively, native prey may be preadapted to recognize novel predators via common constituents in predator odors or familiar predator archetypes. We tested predictions of these competing hypotheses on the mechanisms driving behavioral responses of native species to alien predators by measuring responses of native free‐living northern brown bandicoots (Isoodon macrourus) to alien red fox (Vulpes vulpes) odor. We compared multiple bandicoot populations either sympatric or allopatric with foxes. Bandicoots sympatric with foxes showed recognition and appropriate antipredator behavior toward fox odor via avoidance. On the few occasions bandicoots did visit, their vigilance significantly increased, and their foraging decreased. In contrast, bandicoots allopatric with foxes showed no recognition of this predator cue. Our results suggest that vulnerable Australian mammals were likely naïve to foxes when they first arrived, which explains why so many native mammals declined soon after fox arrival. Our results also suggest such naiveté can be overcome within a relatively short time frame, driven by experience with predators, thus supporting the multilevel naiveté framework.

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“…The most often tested odours have been those of native predators, mainly mustelids, cats and foxes. Rodents, in general, are the bottom of many terrestrial predator–prey systems, especially those with small‐ and medium‐sized carnivores and birds (Jędrzejewska & Jędrzejewski, ); they are therefore subject to an intensive selection pressure, resulting in adaptive responses to spatial variation in predation and predation risk (e.g., Anson, Dickman, Boonstra, & Jessop, ; Atkins et al, ; Grason, ). In rodents, behavioural responses to predator odour rely on changes in their mobility, activity patterns, microhabitat and space use (Borowski, ; Fey, Banks, & Korpimäki, ; Fey, Banks, Ylönen, & Korpimäki, ; Jędrzejewski, Rychlik, & Jędrzejewska, ; Norrdahl & Korpimäki, ; Perrot‐Sinal, Heale, Ossenkopp, & Kavaliers, ).…”

Section: Introductionmentioning

confidence: 99%

The influence of American mink odour on the spatial distribution and behaviour of water voles

et al. 2019

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The perception and assessment of predation risk often cause changes in the activities of animals and induce behavioural responses that may in turn affect their movements and distribution. To simulate high predation risk in a midfield pond riparian habitat, we used fresh faeces from ranch American mink Neovison vison and recorded behavioural responses of water voles Arvicola amphibius. In areas where mink odour was deployed, the numbers of captured vole individuals and their trappability were significantly lower than in control areas. Several voles migrated from the zones with deployed mink faeces to the areas without faeces, thus proving that increased predation risk affects the distribution of individuals in a population. The response to mink odour was much more pronounced in females than in males; in areas with deployed mink faeces, not a single female was trapped. We conclude that although American mink is a non‐native, invasive predator, water voles respond to mink odour by reducing their activity and/or by avoiding places with higher predation risk.

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Deep evolutionary experience explains mammalian responses to predators

Cited by 20 publications

References 36 publications

Novel predators emit novel cues: a mechanism for prey naivety towards alien predators

Novel predators emit novel cues: a mechanism for prey naivety towards alien predators

Overcoming prey naiveté: Free‐living marsupials develop recognition and effective behavioral responses to alien predators in Australia

The influence of American mink odour on the spatial distribution and behaviour of water voles

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