Prey may have ontogenetic experience, evolutionary experience, or both types of experiences with their predators and how such experiences influences their ability to identify their predators is of great theoretical and applied interest. We capitalized on predator-free exclosures containing populations of native burrowing bettongs (Bettongia lesueur) and introduced rabbits (Oryctolagus cuniculus) that ensured we had knowledge of our subjects’ ontogenetic experiences with predators and asked whether evolutionary experience influenced their visual predator discrimination abilities. Rabbits evolved with red foxes (Vulpes vulpes) and wolves (Canis lupus) but had less than 200 years of prior exposure to dingoes. The rabbit population we studied had been exposed to dingoes (Canis dingo) and foxes 8 months prior to our study and had heightened responses to red fox models, but not dingo/dog (Canis dingo/Canis familiaris) models. The insular burrowing bettong population had no ontogenetic exposure to mammalian predators, brief evolutionary exposure to domestic dogs and possibly dingoes, and a deeper evolutionary history of exposure to thylacines (Thylacinus cynocephalus)—another large mammalian predator with convergent body morphology to dingoes/dogs but no evolutionary or ontogenetic exposure to foxes. Bettongs showed a modest response to the dingo/dog model and no response to the fox model. These results are consistent with the hypothesis that deep evolutionary history plays an essential role in predator discrimination and provides support for the multipredator hypothesis that predicts the presence of any predators can maintain antipredator behavior for other absent predators.
Prey may have ontogenetic experience and or evolutionary experience with their predators. How such experiences influence prey species’ ability to identify their predators is of significance to theory on the evolution of antipredator response and to improve the success of translocations and reintroductions for conservation purposes which often fail because of predation on predator naïve prey. Here, we show that prey recognition for two prey species with limited or no ontogenetic exposure to predators, rabbits, and burrowing bettongs was greatest toward the predator to which they had the longest period of coevolution. The results are consistent with the hypothesis that evolutionary history plays an essential role in predator discrimination and provides support for the multipredator hypothesis that predicts the presence of any predators can maintain antipredator behavior for other absent predators.
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Anson JR, Dickman CR (2013) Behavioral responses of native prey to disparate predators: naiveté and predator recognition. Oecologia 171:367–377
Banks PB, Dickman CR (2007) Alien predation and the effects of multiple levels of prey naiveté. Tr Ecol Evol 22:229-230.
Barrio IC, Bueno CG, Banks PB, Tortosa FS (2010) Prey naivete? In an introduced prey species: the wild rabbit in Australia. Behav Ecol 21:986–991
Berger J, Swenson J, Persson I (2001) Recolonizing carnivores and naive prey: conservation lessons from Pleistocene extinctions. Science 291:1036–1039
Biggins DE, Vargas A, Godbey JL, Anderson SH (1999) Influence of prerelease experience on reintroduced black-footed ferrets (Mustela nigripes). Biol Conserv 89:121–129
Blumstein DT (2002) Moving to suburbia: ontogenetic and evolutionary consequences of life on predator-free islands. J Biogeogr 29:685–692
Blumstein DT (2006) The multipredator hypothesis and the evolutionary persistence of antipredator behavior. Ethology 112:209–217
Blumstein DT, Daniel JC (2005) The loss of anti-predator behaviour following isolation on islands. Proc R Soc Lond B 272:1663–1668
Blumstein DT, Daniel J, Griffin A, Evans C (2000) Insular tammar wallabies (Macropus eugenii) respond to visual but not acoustic cues from predators. Behav Ecol 11:528–535
Blumstein DT, Ferando E, Stankowich T (2009) A test of the multipredator hypothesis: yellow-bellied marmots respond fearfully to the sight of novel and extinct predators. Anim Behav 78:873–878
Bowen Z, Read J (1998) Population and demographic patterns of rabbits (Oryctolagus cuniculus) at Roxby Downs in arid South Australia and the influence of rabbit haemorrhagic disease. Wildl Res 25:655–662
Brown JS (1988) Patch use as an indicator of habitat preference, predation risk, and competition. Behav Ecol Sociobiol 22:37–47
Burbidge AA, McKenzie NL (1989) Patterns in the modern decline of western Australia’s vertebrate fauna: causes and conservation implications. Biol Conserv 50:143–198
Carthey AJR, Banks PB (2012) When does an alien become a native species? A vulnerable native mammal recognizes and responds to its long-term alien predator. PLoS One 7:e31804
Cooper WE Jr, Blumstein DT (eds) (2015) Escaping from predators: an integrative view of escape decisions. Cambridge University Press, Cambridge
Cox JG, Lima SL (2006) Naiveté and an aquatic-terrestrial dichotomy in the effects of introduced predators. Trends Ecol Evol 21:674–680
Cupples JB, Crowther MS, Story G, Letnic M (2011) Dietary overlap and prey selectivity among sympatric carnivores: could dingoes suppress foxes through competition for prey? J Mammal 92:590–600
Dortch CE, Morse K (1984) Prehistoric stone artefacts on some offshore islands in Western Australia. Aust Archaeol 19:31–47
Griffin A, Blumstein DT, Evans C (2000) Training captive-bred or translocated animals to avoid predators. Conserv Biol 14:1317–1326
Hänninen L, Pastell M. (2009) CowLog: Open-source software for coding behaviors from digital video. Behavior Research Methods 41:472-476
Johnson C (2006) Australia’s mammal extinctions: a 50000 year history. Cambridge University Press, Cambridge
Johnson CN, Isaac JL (2009) Body mass and extinction risk in Australian marsupials: the “critical weight range” revisited. Austral Ecol 34:35–40
Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394
King CM (1984) Immigrant killers: introduced predators and the conservation of birds in New Zealand. Oxford University Press, Auckland
Lahti DC, Johnson NA, Ajie BC, Otto SP, Hendry AP, Blumstein DT, Coss RG, Donohue K, Foster SA (2009) Relaxed selection in the wild: contexts and consequences. Trends Ecol Evol 24:487–496
Letnic M, Fillios M, Crowther MS (2012a) Could direct killing by larger dingoes have caused the extinction of the thylacine from mainland Australia? PLoS One 7:e34877
Letnic M, Ritchie EG, Dickman CR (2012b) Top predators as biodiversity regulators: the dingo Canis lupus dingo as a case study. Biol Rev 87:390–413
Lima S, Dill L (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640
Lombardi L, Fernández N, Moreno S, Villafuerte R (2003) Habitat-related differences in rabbit abundance, distribution and activity. J Mammal 84:26–36
Moseby KE, Blumstein DT, Letnic M (2015) Harnessing natural selection to tackle the problem of prey naïveté. Evol Appl 9:334–343
Moseby KE, Hill BM, Read JL (2009) Arid recovery—a comparison of reptile and small mammal populations inside and outside a large rabbit, cat and fox-proof exclosure in arid South Australia. Austral Ecol 33:156–169
Moseby KE, Read JL, Paton DC, Copley P, Hill BM, Crisp HA (2011) Predation determines the outcome of 10 reintroduction attempts in arid South Australia. Biol Conserv 1442:863–872
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
Robley A, Short J, Bradley S (2001) Dietary overlap between the burrowing bettong (Bettongia lesueur) and the European rabbit (Oryctolagus cuniculus) in semi-arid coastal Western Australia. Wildl Res 28:341–349
Savidge JA (1987) Extinction of an island forest avifauna by an introduced snake. Ecology 68:660–668
Short J, Turner B (1993) The distribution and abundance of the burrowing bettong (Marsupialia: Macropoidea). Wildl Res 20:525–534
Short J, Turner B (2000) Reintroduction of the burrowing bettong Bettongia lesueur (Marsupialia: Potoroidae) to mainland Australia. Biol Conserv 96:185–196
Short J, Turner B. (1999) Ecology of burrowing bettongs, Bettongia lesueur (Marsupialia: Potoroidae), on Dorre and Bernier Islands, Western Australia. Wildl Res, 26:651-669
Short J, Turner B, Majors C Leone J, (1997) The fluctuating abundance of endangered mammals on Bernier and Dorre Islands, Western Australia-conservation implications. Aust. Mammal. 20:53-62
Shortridge GC (1910) Account of the geographical distribution of the marsupials and monotremes of south-west Australia, having special reference to the specimens collected during the Balston expedition of 1904-1907. Proc Zool Soc London 1909:803–848
Stringmore JL (2010) Surviving the "cure": life on Bernier and Dorre Islands under the lock hospital regime. PhD Dissertation, University of Western Australia
Tortosa FS, Barrio IC, Carthey AJ, Banks PB (2015) No longer naïve? Generalized responses of rabbits to marsupial predators in Australia. Behav Ecol Sociobiol 69:1649–1655
Vanak AT, Gompper ME (2009) Dogs Canis familiaris as carnivores: their role and function in intraguild competition. Mammal Rev 39:265–283
We acknowledge the Arid Recovery staff and volunteers for their assistance with the study and the anonymous reviewers for their constructive comments on the manuscript.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors. Work was conducted under animal ethics APEC Approval Number 15/19A and in accordance with The Australian Code of Practice for the Care and Use of Animals for Scientific Purposes (1997).
Funding for this project was provided by the Australian Research Council (LP130100173).
Conflict of interest
The authors declare that they have no competing interests.
Communicated by A. I. Schulte-Hostedde
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Atkins, R., Blumstein, D.T., Moseby, K.E. et al. Deep evolutionary experience explains mammalian responses to predators. Behav Ecol Sociobiol 70, 1755–1763 (2016). https://doi.org/10.1007/s00265-016-2181-4
- Antipredator behavior
- Visual predator discrimination
- Multipredator hypothesis