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Harnessing Natural Selection to Tackle the Problem of Prey Naıveté

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Harnessing Natural Selection to Tackle the Problem of Prey Naıveté Evolutionary Applications Evolutionary Applications ISSN 1752-4571 PERSPECTIVE Harnessing natural selection to tackle the problem of prey na€ıvete Katherine E. Moseby,1,2 Daniel T. Blumstein3 and Mike Letnic4 1 School of Earth and Environmental Sciences, The University of Adelaide, Adelaide, SA, Australia 2 Arid Recovery Ltd., Roxby Downs, SA, Australia 3 Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA, USA 4 Centre for Ecosystem Science, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW, Australia Keywords Abstract exotic predators, na€ıvete, natural selection, predator learning, prey, reintroduction. Many populations are threatened or endangered because of excessive predation resulting from individuals’ inability to recognize, avoid, or escape alien predators. Correspondence Such prey na€ıvete is often attributed to the absence of prior experience and co- Katherine E. Moseby Arid Recovery Ltd., P.O. evolution between native prey and introduced predators. Many reintroduction Box 147, Roxby Downs 5725, Australia. programs focus on reducing predation rate by excluding introduced predators, a Tel.:/Fax +61 886481878 focus which ignores, and indeed exacerbates, the problem of prey na€ıvete. We e-mail: [email protected] argue for a new paradigm in reintroduction biology that expands the focus from Received: 25 May 2015 predator control to kick-starting learning and evolutionary processes between Accepted: 19 September 2015 alien predators and reintroduced prey. By exposing reintroduced prey to carefully controlled levels of alien predators, in situ predation could enhance reintroduc- doi:10.1111/eva.12332 tion success by facilitating acquisition of learned antipredator responses and through natural selection for appropriate antipredator traits. This in situ predator exposure should be viewed as a long-term process but is likely to be the most effi- cient and expedient way to improve prey responses and assist in broadscale recovery of threatened species. larger predators, competitors, and parasites as well as facili- The problem of prey na€ıvete tation that can occur when populations of introduced Predation by introduced predators, especially mammalian predators benefit from the presence of high densities of predators, is a major factor responsible for the extinction introduced or native prey (MacDonald and Harrington of wild vertebrate populations and the failure to success- 2003; Saunders et al. 2010; Sih et al. 2010; Letnic et al. fully reintroduce endangered vertebrates in many parts of 2012). High rates of encounters between prey and over- the world (King 1984; Savidge 1987; Biggins et al. 1999; abundant predators can have catastrophic effects on prey Johnson 2006; Moseby et al. 2011). The primary reasons populations. These population-level effects of predators on for significant population declines of many native prey spe- prey are likely to be exacerbated and result in ‘hyperpreda- cies and failure of subsequent reintroduction programs are tion’ on rare prey species if alternate food sources (such as thought to be (1) the inability of prey individuals to avoid over-abundant prey) are available for predators (Sinclair and/or mount effective antipredator responses when they et al. 1998). encounter introduced predators (Griffin et al. 2000; Short While there is evidence that high densities of introduced et al. 2002; Blumstein 2006; Moseby et al. 2011) and (2) predators can precipitate catastrophic declines in prey pop- the high densities and therefore high rates of encounters ulations and thwart reintroduction attempts, in many between introduced predators and native prey. instances, just one or relatively few individuals of an intro- In many situations, introduced predators thrive in their duced predator species have had catastrophic impacts on new environments and may occur at very high population populations of threatened prey (Christensen and Burrows densities. There are several potential drivers of high popu- 1994; Gibson et al. 1994; Moseby et al. 2011). These obser- lation densities of introduced predators. These include vations suggest that the susceptibility of some native prey release from constraints on population growth posed by to introduced predators is not just a function of the rate of 334 © 2015 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Moseby et al. Natural selection and prey na€ıvete encounters between predators and prey but also due to an red fox (Vulpes vulpes), and feral cat was the reason for fail- asymmetry in the outcome of predator–prey encounters. ure of approximately 80% of unsuccessful mammal intro- For example, even when intensive feral animal control was ductions (Short 2009). In taxa such as macropodids successfully implemented at a site in inland Australia, indi- (kangaroos, wallabies, and rat kangaroos), their susceptibil- vidual exotic feral cats (Felis catus) were still able to cause ity to introduced predators is so great that no safe density the failure of a large-scale mammal reintroduction program of introduced predators is thought to exist (Clayton et al. (Christensen and Burrows 1994). Similarly, Roy et al. 2014). However, native predators can also cause reintro- (2002) reported that population control of an introduced duction failure, particularly in captive-bred animals, with mongoose (Herpestes javanicus) failed to prevent uncom- predation and prey naivety cited as primary reasons for the mon but significant predation events on the rare pink failure of bird reintroductions in the Caribbean (White pigeon (Colombus mayeri) in Mauritius. et al. 2005) and Saudi Arabia (van Heezik et al. 1999). The high susceptibility to introduced predators displayed In this perspective, we propose a novel approach to over- by many prey species is at least partly due to their na€ıvete come the problem of prey na€ıvete that aims to kick-start (Sih et al. 2010; Carthey and Banks 2014). Na€ıvete can co-evolution between introduced predators and native result from isolation of individuals from predators during prey. While much of our discussion is focused on improv- their lifetime (ontogenetic na€ıvete, common in captive- ing the success of endangered species reintroduction pro- bred animals) or through an absence of co-evolution with grams, the concepts and approaches that we outline have recently introduced predators (evolutionary na€ıvete, com- broader relevance and application to ecosystems where mon in situations where exotic predators are present) native prey interact with introduced predators. (Griffin et al. 2000). Banks and Dickman (2007) suggested that there are three levels of na€ıvete to alien predators: level Expanding the focus of reintroduction programs 1 is a failure of prey to recognize a species as a predator; from predators to prey level 2 is recognition of the predator but adoption of inap- propriate antipredator behavior; and level 3 is where prey To date, strategies to address high predation rates in rein- recognize the predator, have an appropriate response, but troduction programs have largely concentrated on control- the predator exhibits superior hunting skills. In addition to ling or eradicating predators rather than improving the inappropriate antipredator behavior, prey species that lack antipredator responses of prey (Armstrong et al. 2002; Sco- evolutionary exposure to predators may also possess other field et al. 2011). However, with the exception of some traits that make them susceptible to novel predators such island or fenced systems where a well-defined area and the as flightlessness, strong scent, noisy or conspicuous young, absence of immigration can facilitate predator eradication inadequate camouflage, and lack of nest or brood guarding (Nogales et al. 2004), the likelihood of eradicating intro- behaviors. duced predators is low. Consequently, many reintroduction Prey na€ıvete has been a particularly problematic issue for programs focus on improving the survival of reintroduced reintroduction programs in Australasia. Here, vulnerability species by reducing predator population sizes and thereby to predation by introduced mammalian predators has reducing the frequency of encounters between threatened caused widespread declines and extinction of more than 20 prey and predators. For example, in Australia and New species of mammals weighing less than 5 kg in Australia Zealand, one widely employed strategy to control intro- (Johnson 2006) and numerous species of birds and lizards duced predators (primarily red foxes in Australia, and in New Zealand (King 1984; Towns et al. 2001). In some stoats (Mustelus ermina) and rats (Rattus rattus) in New cases, populations of endangered native species remain in Zealand) is the broad-scale distribution of poisoned baits, areas where introduced predator populations are low or often from aircraft (Burrows et al. 2003; Moseby and Hill absent (Johnson 2006; Innes et al. 2010). These remnant 2011; Ruscoe et al. 2011). Another strategy that has been populations have been used as sources for reintroduction advocated to alleviate introduced predators impacts on programs into areas of their former ranges where intro- prey, but remains untested in reintroduction programs, is duced predators exist, but in nearly
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