This article is protected Allrights bycopyright. reserved. 10.1111/eva.12332 of Record.versiondifferences and article Please between the cite this Version this as doi: through the copyediting, typesetting, pagination for publication accepted This articlehasbeen m [email protected] [email protected] Sydney, 2052,Australia Wales, NSW University NewSouth of 4 3 2 1 Katherine E.Moseby naïveté prey of problem the totackle selection natural Harnessing type:Perspective Article Accepted Date:19-Sep-2015 :04-Sep-2015 Date Revised Received Date :25-May-2015 South, LosSouth, 90095-1606, USA Angeles, CA Australia Centre for Ecosystem Science, Centre forEcosystem and Evol Department ofEcology 5725,Australia 147,RoxbyLtd., Box Downs Arid Recovery P.O. School ofEarthandEnvironmenta

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1,2 , DanielT.Blumstein School of Biological, Earth Biological, Schoolof utionary Biology, University of California, 621 Young Drive 621Young utionary California, Biology, University of l Sciences, The University of Adelaide, Adelaide, SA5005, Adelaide, University of l Sciences,The 3 , Mike Letnic, Mike and undergone full peer review buthasnot been review undergone fullpeer and and proofreading process, which may lead to 4 and Environmental Sciences, and Environmental This article is protected Allrights bycopyright. reserved. Accepted Keywords species threatened way toimproveprey most efficientandexpedient This natura andthrough responses anti-predator learned predators, prey By reintroduced exposing reintroduced prey. e and learning control tokick-starting predator Article in anewparadigm for argue prey naïveté.We of problem the exacerbates, andindeed ignores, which afocus predators, introduced excluding prog Many reintroduction introduced predators. experien of prior absence the to attributed individuals’ inability torecognize, avoid, alien orescape Such predators. prey naïveté isoften endangered or arethreatened Many populations Abstract Running head in situ in-situ : predator exposure should be viewed as al as shouldbeviewed predatorexposure exotic predators, prey, naïveté, natural natural prey, naïveté, predators, exotic : naturalselection naïveté andprey predation could predation enhance success reintroduction by facilitating acquisition of . . ce and co-evolution between native prey and betweennative co-evolution and ce reintroduction biology that expands thefocusfrom expands biology that reintroduction volutionary processes betw volutionary processes rams focus on reducing predation rate by rateby predation focusonreducing rams resulting from predation excessive of because to carefully contro tocarefully responses and assist in broadscale recovery of recovery assist inbroadscale responses and l selection for appropriate l selectionfor selection, predator selection, predator ong term process but is likelyong processbut the term tobe lled levels ofalien learning, reintroduction learning, reintroduction een alien predators and alienpredators een anti-predator traits. anti-predator This article is protected Allrights bycopyright. reserved. Accepted av are prey) (such asover-abundant food sources alternate if species prey onrare “hyper-predation’ in and result beexacerbated to likely are prey onprey populations. effects catastrophic can have High Ritchie, andDickman2012). 2003;Saunders,Gentle (MaCdonald andHarrington fromthepresence benefit of introducedpredators competitors a larger predators, includerelease These introduced predators. Ther very populationdensities. high be encounters of rates high and therefore ArticleBlumstein 2006; Short, Kinnear,andRobley 2002; introducedpred encounter responses whenthey thought prey tobe1)theinability individua of andfailu prey species native ofmany declines population forsignificant reasons 2006; Moseby1999; Johnson et al.2011).Theprimary ofthe inmany parts vertebrates endangered populations ofwildvertebrate for theextinction ma predators, especially Predation by introduced naïveté prey of problem The thrive In predators situationsintroduced many nd parasites as well as as well nd parasites rates of encounters rates between of encounters e are several potential drivers potential several e are tween introduced predators and native prey. prey. andnative predators introduced tween from constraints onpopulationgrowth posedby from world (King 1984; Savidge 1987; Biggins (Kingal. 1987; 1984; Savidge world et re of subsequentrein re of ls to avoidandormount ls to ators (Griffin, Blumstein, andEvans2000; (Griffin, ators and the failure to successfully reintroduce reintroduce thefailuretosuccessfully and mmalian predators, is a ma mmalian predators,isa ailable for predators (S ailable forpredators in their new environments and may occur at may and occur newenvironments intheir of high densities of introduced or native prey of high ofintroducedornativeprey densities These population-level effects of predators on ofpredators effects These population-level Moseby et al. 2011), and 2)thehigh densities al. 2011),and Moseby et , and Dickman 2010; Sih et al. 2010; Letnic,, andDickman2010;Sihetal. facilitation that can occur when populations when facilitationthatcanoccur prey and over-abundant predators predators and over-abundant prey of high population densitiesof population of high troduction programs are programsare troduction effective anti-predator anti-predator effective inclair et al. 1998). inclair etal.1998). jor factor responsible jor factor This article is protected Allrights bycopyright. reserved. butadoptionofinap ofthepredator is recognition 2 level as apredator; aspecies recognize prey to of afailure 1is level predators: alien to naïveté ( and Dickman BanksBlumstein, andEvans2000). insituationswh common (evolutionary naïveté, of an absence through animals)or, captive-bred isolation ofindividualsfrompr (S totheirnaïveté partly due in Mauritius. mammal reintroductionpr individual feral exotic ( cats when intensive control feral was animal successfully implemented at ininland a Australia, site of but alsoduetoanasymmetry intheoutcome isnotjustafunctionofth introduced predators th observationssuggest et al.2011).These Moseby (Chr prey impacts onpopulationsofthreatened individualsofanin few just oneorrelatively populationsandthwa inprey catastrophic declines prevent uncommonbutsignificant preda control reported thatpopulation Accepteda an predator,have the recognize where prey Article The high susceptibility to introduced predators displayed by many prey species isatleast displayed preyThe high many by species tointroducedpredators susceptibility thereWhile isevidence high that densities ogram (Christensen andBurrows Felis catus ih et al. 2010; Carthey and Banks 2014). Naïveté can result from can 2014).Naïveté Banks ih etal.2010;Cartheyand edators lifetime during their ( of an introduced mongoose ( of anintroduced ) were stillable tocauseof a large-scale failure the tion events on the rare pink pigeon ( onthe rarepinkpigeon tion events ppropriate response, but response, ppropriate troduced predator specie troduced predator of introduced predat of introduced e rate of encounters between predators and prey predatorsand between ofencounters e rate istensen and Burrows 1994;Gibsonetal. Burrows istensen and predator-prey encounter predator-prey co-evolution with recently introduced predators introducedpredators withrecently co-evolution ere exotic predators are present) (Griffin, (Griffin, present) are predators ere exotic propriate anti-predator be rt reintroductionattempts at the susceptibility of some nativeprey to at thesusceptibility ofsome 2007) suggested that there are three levelsof three are thatthere 2007) suggested 1994).Similarly, etal Roy ontogenetic naïveté, commonin ontogenetic naïveté, Herpestes javanicus ors can precipitate s have had catastrophic hadcatastrophic s have the predator exhibits exhibits the predator s. For example, even For example, s. havior; andlevel3is , inmany instances Colombus mayeri ) failed to . (2002) (2002) ) This article is protected Allrights bycopyright. reserved. theirsu ratkangaroos) wallabies and (kangaroos, in mammal 80% ofunsuccessful ( red fox the predators, Short 2009;Sherleyal al. 2010;Moseby et et inAustralasia(Fischer reintroduction failure 2012). 1994;ShortandTurn Burrows (Christensen and guarding behaviors. orbrood nest and lackof camouflage strong asflightlessness, novel predatorssuch also posse topredatorsmay evolutionaryexposure superior huntingIn addition toinappropriate skills. Accepted ha programs cases reintroduction all nearly in but exist, predators introduced where ranges former oftheir areas into programs remnant populationsha Innes etal.2010).These pred introduced where inareas species remain In andCree2001). 1984; Towns,Daugherty, Article 2006)andnumerousspecies in Australia(Johnson 5kg than less weighing ofmammals 20species than ofmore extinction and declines widespread topredati vulnerability Australasia. Here, Predation from introduced predator Predation fromintroduced probl a particularly Prey hasbeen naïveté Vulpes vulpes Vulpes troductions (Short 2009). In taxa such as macropodids Introductions (Short suchas 2009). taxa ve failed to establish self-s toestablish ve failed ) and feral cat was the reason for failure of approximately ofapproximately forfailure reason wasthe cat feral ) and s has in most cases been cited as the primary cause of cause cited astheprimary been s hasinmostcases on by introduced mammalian predators has caused hascaused mammalianpredators introduced on by and Lindenmayer andTurner2000; 2000;Short and ematic issue for reintroduction programs in programs issueforreintroduction ematic . 2011). In Australia, predation by In introduced . 2011). Australia,predation some cases, populations of endangered native native cases,populationsofendangered some scent, noisy or conspicuous young, noisy inadequate scent, orconspicuous ator populations are low or absent (Johnson 2006; (Johnson populations areloworabsent ator er 2000; Moseby et al. 2011; Hayward et al. al. 2011;Hayward 2000;Moseby er et ve been used as sources for reintroduction for as sources beenused ve sceptibility to introduced predators is so greatpredators isso tointroduced sceptibility ss other traits that make susceptible them to of birds and lizards in New Zealand (King inNew of birdsandlizards anti-predator behavior, prey that lack species behavior, anti-predator ustaining wildpopulations eradicating introducedpredators islow.Cons eradica predator immigrationfacilitate can of absence and the area a well-defined where systems orfenced island ofsome exception et al.2002;Scofie (Armstrong responses ofprey anti-predator the improving than rather predators eradicating or oncontrolling concentrated highaddress predati To date,strategies to toprey predators from programs of reintroduction focus the Expanding predators. introduced with prey interact native where ecosystems to programs, the concepts andapproaches that have we outline relevance broader application and onimproving thesu our discussionisfocused that aims tokick-start co-evolution between intr Maloney 1999). andVilella2005) Collazo, Jr, Caribbean (White This article is protected Allrights bycopyright. reserved. Accepted andstoats( inAustralia, red foxes (primarily employed onewidely Zealand, Australia andNew thr between encounters of thefrequency reducing improving reintroducedspecies thesurvivalof Articlecited naivetypredation andprey failure also causereintroduction can native predators is predators ofintroduced that nosafedensity anovelappro propose In we thisperspective, as primary reasons forthefailure reasons as primary on rates in reintroduction on rates tion (Nogales et al. 2004), the likelihood of etal.2004),thelikelihood tion (Nogales Mustelus ermina Mustelus equently, many reintrodu equently, many ccess of endangered species reintroduction reintroduction species ofendangered ccess thought to exist (Clayton et al. 2014). However, 2014).However, (Clayton toexist et al. thought by reducing predator population sizes andthereby sizes population predator reducing by oduced predators and native prey. While muchof prey. While andnative predators oduced Seddon,and Heezik, SaudiArabia(van and ld, Cullen, and Wang 2011). However, withthe However, Cullen,andWang 2011). ld, ach to overcome the problem of prey naïveté of prey naïveté overcometheproblem ach to eatened prey andpredat eatened prey strategy tocontrol predators introduced , particularly in captive-bred animals,with incaptive-bred , particularly ) and rats ( ) andrats of bird reintroductions inthe ofbirdreintroductions programs have largely havelargely programs ction programsfocuson Rattus rattus Rattus ors. For example, in example, ors. For ) inNew This article is protected Allrights bycopyright. reserved. Accepted ot toexplore isaneed Sutherland 1997)andthere (s populations threatened species reintroduced while control ofintro Thus, species. populations cannotbesu thefailureof couldleadto these reasons market as variationinfinancial are implement predatorcontrol programs thatrequire 2000).Second, and Wayne 1994;A andDrew overtime(Warburton effective less become thus and technique control the to susceptible areless that forpredators selection poisoning,as biologiccontrol techniquessuch lasting tworeasonswhy atleast are al. 2013).There Article onl may populationsofintroducedpredators excluding Hunteretal.2015). Ritchie, andDickman2012; mes are predators predators (mostintroduced thatnativ effects is toharnessthesuppressive impactsonprey, alleviate introducedpredators A Hill 2011;Ruscoeetal.2011). 2003; Moseby and distributionofpois scale Zealand) isthebroad or onsuppressing rely that persistence species forendangered strategies areas, In larger ppressed to sufficiently low levels low ppressed tosufficiently s and the whims of funding agencies and philanthropists. Any of andphilanthropists. agencies fundings andthewhimsof vulnerable to factors beyond the control of land-managers, such beyond thecontrolofland-managers, tofactors vulnerable ee Marlow et al. 2015), results can be short-lived (Coteand short-lived 2015), resultscanbe etal. ee Marlow a reintroduction program if introduced predator predator programifintroduced a reintroduction opredators) (Crooks and Soulé 1999; Letnic, 1999; (CrooksandSoulé opredators) e apex predators have on populations ofintroduced predatorshaveonpopulations e apex al control, andshooting/trappingal control, may impose oned baits, often from aircraft (Burrows etal. (Burrows oned baits,oftenfromaircraft but remainsuntestedin but duced predators can assist intheprotectionof assist can duced predators her alternatives for long term co-existence. co-existence. term forlong her alternatives funding to sources perennial supportfrom llen, Engeman,andKr nother strategy that has been advocated to beenadvocated nother strategy thathas predator control is difficult to achieve. First, control isdifficulttoachieve. predator y be effective in the short-term (Wayne et (Wayne y intheshort-term effective be to allow the persistence of toallowthepersistence reintroduction programs, reintroduction upa 1996; Kohn, Pelz, upa 1996;Kohn,Pelz, This article is protected Allrights bycopyright. reserved. Accepted nowexist. predators where ranges former reintroduce these individuals from small, isolated systems intolarger, areas natural intheir frompr ofprey response often pooranti-predator itmayand berapidly lo anti-predator behavior Thus,withnopr riskofpredation. an increased expense ofengaging activities, in other avoiding oranimals certain areas there because may be i often anti-predator behaviors relaxe through predator behavior etal.2000). etal.1999;McLean (Biggins Article suchpr from ofindividuals avoidance strategies predator becausethe exclusion by predator exacerbated is naïveté prey of problem the improved, inevitably successis andreintroduction predators from safe kept are prey-species threatened 2001; Short2009; Ferreira (Towns and refuges nowinvolveth reintroductions threatened species ShortandTurner200 Blumstein, andEvans2000; islandsorfenced predator-free oftenusecaptive-bred reintroduction programs programs isontogeneticnaivety. Necessityand availability dictates that threatened species Complete removalofpr In addition to evolutionary another naivety, edation pressure can lead to sign to can lead pressure edation nvolve animals increasing their an nvolve animalsincreasing their enclosures (van Heezik, Seddon,andMaloney 1999;Griffin, (van Heezik, enclosures d selection (Blumstein 2006; Lahti 2006; 2009). Thisisbecause d selection(Blumstein etal. st (Blumstein, Daniel, and Springett 2004). The 2004). The Daniel,andSpringett st (Blumstein, stock or animals sourced from introduced from stockoranimalssourced Scofield,Cullen, edators, there are no benefits from engaging in in engaging from are nobenefits there edators, problem facing threatened species reintroduction species threatened facing problem edator-free areas are often severely compromised compromised oftenseverely are areas edator-free edator-free sanctuaries can hamper efforts to hamperefforts can sanctuaries edator-free e transfer of individuals between predator-free individualsbetweenpredator-free e transferof 0). Indeed,0). inAustralasia, the majority of ificant and rapid loss ofprey anti- and rapidloss ificant ti-predator vigilance atthe ti-predator and Wang 2011).Althoughand Wang This article is protected Allrights bycopyright. reserved. anti-pred mammalian) andeffective mammalian), maypredator retain discrimination abilities forall archetypes(avian and even thos tosome predators, populations exposed will notassort independently and expect ofanti-predator the we evolution Thus, syndromes. behaviors anti-predator that expect we predator, a single than more have prey whenever because ones,aslong extinct even to respondpredators, Accepted reduced. may be with predators encounters prey fromfuture to risks the predators, all eliminate to trying than rather preynaïveté of problem the addressing pred distantlyrelated more towards generalize to likely andless predators closely-related more towards generalize to likely are more predator one recognize to trained offishes studies from comes hypothesis archetype olfactory for the and Milne2007).Additionally, re ha mammalsthat among convergence morphological Lima and (Cox species willrespondtothem loss ofanti-predatorabilities. rapid a to lead however, may, enclosures predator-free completely in isolation True predators. Article pred Springett 2004).Thus,some thelossofkey pr despite predator behavior the multi-predator comes that hypothesis document fromstudies persistence long-term anti- of The multi-predator hypothesis (Blumstein 2006)st The multi-predatorhypothesis The predator archetype hypothesis predicts that if two predators are similar in some key way, keyway, some in are similar predators two if that predicts hypothesis archetype The predator ation may be essential tore essential ation may be lated species maylated species simila share ator behavior even for the mi even forthe ator behavior edators (Byers 1997; Blumstein, Daniel,and 1997;Blumstein, (Byers edators 2006). For instance, there is remarkable For thereisremarkable instance, 2006). ators (Ferrari et al. 2007). Therefore, by by etal.2007). Therefore, (Ferrari ators e from different archetypes (e.g., avian butnot avian (e.g., archetypes e fromdifferent as they are exposed tosomepredators.Thisis exposed as theyare ve similar diets and hunting styles (Wroe (Wroe stylesve similardietsandhunting ates that prey should be retain theability ates thatprey shouldbe tain the ability torespond tain theability r olfactory chemicals. Support r olfactory ssing predator(s). Supportfor ssing predator(s). This article is protected Allrights bycopyright. reserved. Accepted co-exist. to predators introduced To accomplishthiswemu sustainable ecosystems. thenwe reintroduction programs establishment ofself-sustaining populationsof andthe restoration ecological if suggest that we species, endangered preserve may areas fenced (Scofield,Cullen,a thanecosystems like zoos (H base their resource animals haveover-eaten toma and orculling isrequired Islam,Crisp andMosebyIsmail, andBoug 2010; Article (Wiseman exhausted is base the foodresource if sanctuaries the within species on other impacts adverse and species ofreintroduced declines ther thatcanoccur, the environmentaldamage Overpopulation isanimportantcons (C world aroundthe ecosystems linked toenvironmentaldegrad populationsthat herbivore by 2009). Overgrazing Kerley and (Hayward introduced been have they which to ecosystems onthe effects adverse toa speciesincrease populations ofreintroduced Another problem associated with Another problemassociated aremore that ofsanctuaries creation the in and result natural not clearly are These situations ation and fluctuations inhe fluctuations ation and nage populations reintroduced into nage populationsreintroduced ôté et al. 2004; Letnic, Ritchie,andDickman2012). ôté etal.2004; must move beyond predator-free sanctuaries and create andcreate sanctuaries predator-free mustmovebeyond ideration in predator-free sanctu ideration inpredator-free complete fromecosystems ofpredators removal can arise if nd Wang 2011). While introduc Wang 2011).While nd , Page, and O'Connor 2004; Slotow etal.2005; , Page,and O'Connor 2004; e is a serious risk of catastrophic population a seriousriskofcatastrophic e is ayward et al. 2007; Crisp and Moseby 2010). Moseby etal.2007;Crispand 2010). ayward reintroduced species is one of theaims isone species reintroduced point where their consumption of resources has consumption ofresources wheretheir point 2010). In some cases supplementary feeding feeding In supplementary 2010). somecases st address the inability of prey-species and and prey-species st addresstheinability of are unchecked by natural predators has been predatorshasbeen natural by are unchecked rbivore populations inunfenced rbivore populations predator-free sanctuaries after after sanctuaries predator-free aries, because in addition to in because aries, tions toislandsor This article is protected Allrights bycopyright. reserved. Acceptedas demonstrators other which from animals lear can beIn trained toimprovetheir anti-predator skills. cases, some may individuals trained serve andStudh Hölzer, Laland 2003),birds(McLean, 1996)andempi andJarman Lundie-Jenkins, McLean, et al.1990; behavior (Miller Evans 2000).Such pre Blumstein, and (Griffin, predator whereby encounters withpredators, recogn predator have attemptedtoimprove (C ofprey naïveté the mostdamaging form evolu eitherthrough recognition Lack ofpredator captivity islikely notthe answer Why predatoravoidance Article andLima2006). 2006;Cox (Blumstein species-specific is thatsome responses improved anti-predator endangeredintroduced and willco predators prey responses prey of endangered detection isbutoneofse withintroduced encounters species toavoidfatal between pr ofencounters frequency management inreintroduc ofpredator focus the expand needto anurgent is there that argue we predators introduced ac with associated problems potential the Given veral stages of the predation process, we suggest that if the anti-predator anti-predator the if that process,wesuggest predation the of stages veral tion programstonotjustfocusonpr training involving simulated Maloney and McLean 1995; Hölzer, Bergmann, 1995; andMcLean 1995;Hölzer, Maloneyand McLean populations could be improved, populations couldbe

edators and prey), buttoalsoimprovetheabilityand prey), ofprey edators ition prior to re-introductions by simulatingition priortore-introductionsby ox andLima 2006).Some ox cues are paired with an unpleasant experience experience withanunpleasant are paired cues tend to be broad ranging and not necessarily notnecessarily and tend tobebroadranging -release predator training can modify can prey training predator -release n to improve their anti-predator skills(Griffin n toimprove their anti-predator hieving sustained control or eradication of eradication control or hieving sustained olme 1999), and mammals (McLean et al.2000) (McLean olme 1999),andmammals predators. While we recognize that predator thatpredator werecognize predators. While -exist in the-exist wild.Anadditional benefit of tionary or ontogenetic isol tionary orontogenetic rical evidence shows that fish (Brown and that fish(Brown shows rical evidence encounters with encounters with it might be more likelyit might that be edator removal (which reduces the the reduces (which removal edator reintroduction programs reintroduction predators in ation isthought tobe travel large distances, and often exhibit abnor often exhibit and distances, travel large a reasons varietyrelease including for of the are release that individuals site, with unfamiliar can tendtohaveamuch animals 1994). Captive-bred al. et (Beck captivity in aretrained that animals oncaptive-bred focuses often training predator situations donotprovidetheconditioning necessa prey sp in survival reduce post-release 2014).To 2011; Cartheyand Banks This article is protected Allrights bycopyright. reserved. Accepted species(W thantoexotic rather native predators animals captive-bred improved survivaloftrained Of andCrisp2012). 1996;Moseby,Jarman Cameron, etal.1990;Ho (Miller ofsuccess as ameasure differe individuals ratherthana Article oftrained behavior in change pre-release a of have usedevidence training predator release Indeed, most Seddon,andMaloney 1999). Heezik, sp ofreintroduced survival improve post-release and demonstr empirically tested few studieshave direct humaninterventions. which anim by mechanism could beaneffective If soci 2004). widespread, and Evans2003;Griffin In many cases, lab-based predator avoidance training has been unsuccessful because captive captive because unsuccessful hasbeen training avoidance predator lab-based cases, In many Despite the promise of pre-release training c training Despite thepromiseofpre-release nce in post-release survival of survival post-release in nce our knowledge, pre-release training has notbeenshownto has training pre-release our knowledge, ecies exposed to exotic predators. predators. exotic to exposed ecies mal behavior post-release (Snyder etal.1996). mal behaviorpost-release lzer et al. 1996; McLean, Lundie-Jenkins, and Lundie-Jenkins, etal.1996;McLean, lzer oupled with natural social transmission, only withnaturalsocialtransmission, oupled a ecies (White Jr, Collazo Jr, (White ecies from others canlearn als hite Jr, Collazo,hite Jr, andVile ated that pre-release predator training can training predator pre-release that ated lower survival rate than wild animalsupon than lowersurvivalrate ry for survival in the wild. Pre-release survival inthe wild. ry for after release invariably involve a response to aresponse involve invariably after release al transmission of anti-predator behavior al transmissionofanti-predatorbehavior practitionersinvestigating theutility ofpre- particular note is that studiesreporting noteisthat particular trained and untrained individuals and untrained trained , andVilella2005;van ’ experiences without ’ experiences lla 2005;Gaudiosoetal humans. by observed orquantified humans willdothe selecting and thusavoid towards biases particularthat can traits be readily individuals withimprovedanti-pred an forlearning capacity increased an be may there First, predators. real to species prey exposing of advantages three least are at situ This article is protected Allrights bycopyright. reserved. Co Jr, orscent(White than predatormodels rather areused predators live whenactual situations captive in behavior ofanti-predator learning cultural transmissionall occur can life st during useful suggest andpotentially We thatarealistic Kick-starting learning andnatural selection 1999). Seddon,andMaloney Heezik, ( ofhoubarabustards exposure whichdidresultin predator training program encounter(Schakner predatory occu likely that fearconditioning the stimulate to et loud noises(McLean mounted onwheels,and withstimuliprimarily suchas usedharassment Additionally, avoidance predator trials incaptiv Accepted predator Additionally, appropriate Article predator exposure using real encounters between encounters real using predatorexposure Learning is improved because thestimuliar Learning isimprovedbecause Chlamydotis undulata and Blumstein 2016). Notably, Notably, Blumstein 2016). and d reinforcement. Second, thereis reinforcement. d avoidance behavior islikely behavior to avoidance ator behaviors through se natural ator behaviors llazo, andllazo, Vilella2005;Ca improved post-release survival involvedthe survival improvedpost-release with rubber bands, water pistols, stuffedanimals pistols, with rubberbands,water e real, the exposed population is wild,and theexposed real, e ages. Severalstudies ages. ity rarely use real predators but instead have instead but predators real use rarely ity form of predator avoidance training involves avoidance ofpredator form al. 2000). Such unrealistic stimuliareunlikely 2000).Suchunrealistic al. rs naturally when an animal survives a real areal survives animal when an naturally rs ) to live predators prior to their release (van (van release their to prior predators live ) to wild prey populations and predators. There There andpredators. wildprey populations one successful pre-release pre-release one successful be strongly reinforced during during reinforced bestrongly the opportunity to select for toselectfor theopportunity lection. Third,predatorsnot lection. have reported improved reported have rthey and Banks 2014). and Banksrthey 2014). in new, effective anti-predator responses against in responsesagainst anti-predator new, effective predators lostthrough ontogenetic isolation islikely tobe substantially easier than developing enha thatlearning or caution,however, 2000). We social species may have improved opportunities for opportunitiesfor improved social speciesmay have the prey species. Solitary species natural may rely on selection more and filial transfer,while natural selection inimproving anti- success. traits thatdemons forthe and insteadselect biasestowardsselection be thatitcouldreduce This article is protected Allrights bycopyright. reserved. Accepted survival asimproved except humans Article forma predatorsselect improved survivalwhich predat with avoid fatalencounters onsomenaïve imposed by predators introduced traits.T andphysical behavioral, physiological trait,butonasu unlikely onasingle tooperate natural selection toselect forappropriate traits. envisage, We by that selection predators is al. 2000). (Griffinet filial andculturaltransfer in situ

In the case of behavioral responses topredat ofbehavioral case In the Perhaps more importantly, Perhaps moreimportantly, predator exposure duetoprolongedexposur predatorexposure in situ ors. However, it is importantto it ors. However, predator behavior is likely to be influenced by the sociality of thesociality islikely by tobeinfluenced behavior predator . Thus, an advantage of using ofusing . Thus,anadvantage predator exposure allows us to harness the effects of effects the harness usto allows exposure predator trably confer greater greater trably longevity confer and reproductive hus, we propose that strong selection pressure pressure selection weproposethatstrong hus, ite of characters that could conceivably include thatcouldconceivably of characters ite for readily measurable traits imposed by humans imposed traits measurable readily for ors, the relative significance of learning vs. learning of relativesignificance ors, the troduced predators due to evolutionary naïveté. evolutionary dueto naïveté. troduced predators y not be readily observable or quantifiable by orquantifiableby y observable not bereadily prey species should improve their capacity to shouldimprovetheircapacity species prey ncing innate anti-predator responsestonative ncing anti-predator innate e to the predator and the opportunities for andthe e tothepredator learning from conspeci from learning notethatthe traitslinkedto in situ predator exposure may exposure predator fics (Griffin et al. (Griffinet fics This article is protected Allrights bycopyright. reserved. Accepted than isbetter genetic variation when confronted withintroduced justifiable predators tobe and both essential: some reduction in weconsiderselectin extinction, causing population factor important most the is predators exotic from andpredation naïveté prey where case In the occurs. predation from mortality andhigh released are whenanimals lost is diversity Most effort. and time significant requires programs breeding captive in diversity genetic Preserving predators. selection willbedesirabl in thelong genetic term,thenthe bottleneckin suggestWe genetic thatifprey greater variation. with exotic predators eventually leads tolarger diversity islikely ifimproved learni offset tobe populati the selection couldreduce Article oftraitsassoci for asuite threatened species extinct.. become removedshouldther monitored, andthepredators tightly conditions,wher controlled predators under imposeonna can thatpredators selection pressure using when obstacle toovercome From a viewpointfocused onmaintaininggenetic diversity, itmay appearrisky toselect ofpredator theextinction by As evidenced e if it improves threatened species’ca e ifitimprovesthreatened the complete failure to recover a population in thewild. apopulationin torecover thecompletefailure in situ on’s genetic diversity. However, on’s geneticdiversity. predator exposure would be the magnitude of the wouldbethemagnitude of exposure predator ated with anti-predator responses, because such becausesuch anti-predatorresponses, ated with g that inevitably results from aboutofnatural inevitablyg from results that -exposed populations of naïve prey, amajor populationsofnaïveprey, -exposed populations ofthreatenedpopulations species and, ultimately, ng and the long term co-existence of prey species species ofprey co-existence long term andthe ng populations are to survive with exotic predators with exotic aretosurvive populations e be a risk that the prey population could population e beariskthattheprey ïve prey. A solution may be to expose prey to be toexpose ïve prey. Asolutionmay e the rate of prey mortality can be closely closely canbe mortality ofprey rate e the g for traits associated with enhanced survival enhanced survival with traitsassociated g for pacity to co-exist with introduced pacity toco-exist thisinitiallossofgenetic This article is protected Allrights bycopyright. reserved. undergone a bout of selection th of selection undergone about et al.2015). Moseby prey can species the tolerate lowdensities (see trials required forthese in of predators examples resulte andhavenot reserves fenced in recorded Additionally, prev Swenson, andPersson2001). or direct shown tomodify after theirbehavior etal.20 2013;Gérard 2006; AnsonandDickman (K predators resemble natural scentsandsoundsof identifyrespond tothe and species Many prey assumptions. realistic are These experiences. others’ through vicariously withpredatorswhile encounters directly survive prey willbe attacked, some may and Importantly, killed. be assume some we prey that will some that assume We avoid. andpotentially associate to preycan learn that vocalizations) marks, assume that thisenvironment predators willexplore and leave presence scent (e.g., oftheir signs whilstleaving adja are present threatened prey tois added predators couldbe species due, ironically, an absence to ofnatura this sanc andfenced islands Predator-free exposure? Acceptedfacilitated generation.next survival tothe Thereare many examples ofenvironmental change Article Are there populations of threatened pr populationsof Are there Given these assumptions, prey that survive predation, have willeither toavoid or learned in situ process. In some cases these areas expe areas In casesthese process. some ohn, Pelz, and Wayne 2000; Blumstein et al. 2002; Blumstein 2000;Blumstein andWayne etal. ohn, Pelz, lands and fenced enclosures enclosures lands andfenced rough which survivors passedonwh rough whichsurvivors ey species large enough to conduct to enough large ey species vicarious experiences with predators (Berger, (Berger, predators with experiences vicarious cent areas untouched as insurance populations. We We populations. asinsurance areasuntouched cent l predators. Sterilized, and radio-collared single d in mass predation events, suggesting that many many suggesting that events, predation mass d in tuaries offer the best opportunities tomanage opportunities thebest tuaries offer others might have the opportunity to learn might theopportunity have others their predators; even novel predatorsthat evennovel predators; their ious single predator incursions have been havebeen ious single incursions predator 14). Previously naïve survivors have been havebeen survivors 14). Previously naïve rience an oversupply of threatened prey threatened prey of anoversupply rience where healthy populations of healthy populations where atever heritabletraitsthat atever in situ in predator predator demonstrates improvedan betestedduring can generations successive Diogo, (Cooper, distance) varies ashowtheirvigilansounds andmodelsaswell scents, cuesusing topredator prey respond how quantifying by measured canbe prey responses intergenerational in Thechanges manipulations. andexperimental comparisons intergenerational vulnerability inexistingenvironments? predatorThis can be both tested through This article is protected Allrights bycopyright. reserved. more adding gradually environments thatsupportpr toface “ready” res potential baseline naivetétoidentify it isessentialtounderstandthe opportunitiesthatexist stage andthe topredation respond to Farrugia, andKi Hendry, and Wayne 2000; Pelz, bebothevolutionary can al. 2009).Suchchanges sodrivingphenotypic species andindoing rapid associated withhuman activities and biological imposing invasions strongselection pressures on Acceptedtrainedwould be released prey intoexisting pr responses of environments andmeasuring the Article When differences are detected, detected, are differences When whenHow dowe natural predict reduce ifand prey willsufficiently selectionpredators by in situ training islikely considerably tovary depending onvulnerability each life of in situ in ti-predator responses. ti-predator responses. predators uptothe recorded densities inexisting predator life history aspecies strategies and Blumstein 2015). Additiona Blumstein 2015). and manipulations can be manipulations can ponsive populations and species for such andspeciesfor ponsive populations in situ edator populations. These can be conducted by conductedby populations.Thesecanbe edator prey. Ultimately, successive generations of successive Ultimately, prey. edator areasedator with varying densities predator and ce and escape behavior (e.g., flight initiation (e.g., behavior and escape ce change (PhillipsandShine2004;Darimontet change nnison 2008). The capacity of native species to ofnativespecies nnison 2008).Thecapacity and/or represent phenoptypic plasticity (Kohn, phenoptypic represent and/or for filial and cultural transfer. We suggest that suggest We transfer. for filialandcultural predation experiments: increased survival survival increased experiments: predation conducted to determine when prey are are whenprey conductedtodetermine uses as well as documenting aswell uses lly, the survival ratesof lly, thesurvival in situ training. training. in situ

the importance of thinking about the welfare of welfare aboutthe the importanceofthinking This article is protected Allrights bycopyright. reserved. Accepted By ecosystems. populationsandrestore recover conser goal as our primary Samways because 2010) What aboutthewelfare species? endangered Is this considerations Ethical modelled priortoinitiatingexperiment. an natural mortality,and thecapacity toremove th population, species individuals ofthereintroduced in-situ In practice, ordesirable. may notbepractical Article however, species, endangered or threatened a of reductions Massive behavior. anti-predator its w resultingkilled), themorelikely population the animals more the (i.e., selection the stronger the that predicts ceased.Theory is experiment willbethethre responses species anti-predator the limitations of andprogressively untrained by can betolerated individua untrained with compared survival their We adopt here an explicitly ecologistic ecologistic explicitly adoptherean We thatuse forprograms An importantconsideration predationbetween number willbe of determined as the such factors trade-offs by in situ predator exposure ethically defensible? defensible? ethically exposure predator in situ predator training and the importance and the predator training perspective (e.g., Kellert 1997;Simaikaand Kellert (e.g., perspective of individual prey species and predators? predators? and individualprey of species the threshold levelof thethreshold shold levelofpopulation shold e predator. Such demographic factors could be could factors demographic Such e predator. individuals that may suffer in a conservation in aconservation thatmay individuals suffer trained prey willalsoa trained contrast, Vucetich and Vucetich contrast, ls. Understanding the predation thresholdsthat thepredation ls. Understanding ill be different from theoriginal populationin ill bedifferent the expected rates of intrinsicgrowth and ratesof theexpected vation biologists andecologists istohelp Will itresultWill inexcessive mortality of in situ predation to improve reintroduced predationtoimprovereintroduced of simultaneous predator control. predatorcontrol. of simultaneous population reductionusing population ssist withunderstanding Nelson (2007) emphasize (2007)emphasize Nelson reduction atwhichthe reduction suffering prey imposed onindividual who might killed while be inan enclosure witha captive and popula prey, endangered of predator responses that notall willagree ourviewpoint, we believe with that if This article is protected Allrights bycopyright. reserved. Accepted towork,someindi our proposedinterventions For experiments. well-designed of aset with idea the exploring worth certainly is it and therefore that individual preyand predators strategies. novelmanagement explore boldmustbedone.View with naïveprey, something Ifaim to restor USA. we Species Actofthe sustainable wildpopulationsinsomejurisdictions increasing However, questionable (Bekoff2002). reintroduc argued that absolute. Thus,somehave Articledriven Inby predation. cases where naïve prey animals have a particularly mortality high releaserate that intothe thisisoften upon wildand animals. released onrecently is inresponsetopredation tor andapproaches tools effective need more orendanger populationsofthreatened recovering ofindividuals,it withthewelfare concerned ourfocusonpopulationreco intervention. While Does thisneed more todevelop effective strategies introduction outweigh costs to the believethatthelessons We from reintroduction biology have shown us that captivebred shownusthat have from reintroductionbiology might be involved insuchan might beinvolved e ecosystems where introduced predators interact predatorsinteract introduced where e ecosystems does focus our goals on the ultimate goal of goal goals ontheultimate does focusour ecover populations; particularly those where failure thosewhere populations;particularly ecover vidual prey willlikely di encounter introduced predat introduced encounter very does not mean that we shouldnotbe we doesnotmeanthat very tions, given their low success rate, are ethically rate,are given theirlowsuccess tions, ed species. We believe species.We ed populations of endangered species and creating speciesand populations ofendangered are mandated by laws such as the Endangered astheEndangered lawssuch by are mandated tions are ultimately reco tions areultimately ed this way, there is a moral imperativeto isa ed thisway, there in situ intervention? We believeitcould We intervention? predationimprovestheanti- e. While weunderstand While e. that wildlifemanagers that vered, theindividual ors, predationmay be 2007). questions thatmustbediscu are these that think We forrelease. mammal a small prepare to tool as a example, Australian and furtherdiscussion warrant andana predator a native consider contrast, in thefuture andsore kill introducedpredators anti the successful atimproving is welfare iftheir exposure predator This article is protected Allrights bycopyright. reserved. predators, wouldbe killed, whootherwise inexperiments todetermine the efficacy of Thus reserve. a fenced are tosurviveoutside nativeAustralia etal.2011).Nonetheless, (Moseby and shottoredu degree trapped pr 2006). Thus,inmany theseintroduced places had adisproportionately implementation. its for astools are used they prey between killing by and reduce ofencounters predators rate predators. the ofreco the benefits bypredator isoutweighed Accepted Article Ne novel onesandnativepredators. thatwouldbeused envision twotypes ofpredators Consider introduced cats inAustralia and foxes predat the of welfare the to relevant Issues negative impact on small andmi negative impactonsmall ssed and debated on a case-by-case case-by-case ona ssed anddebated debate about whether to use a native canid, dingoes inthe canid,dingoes touseanative about whether debate ce population density or eliminate them in fenced reserves reserves oreliminatetheminfenced density ce population -responses of endangered mammals ofendangered -responses ither directly benefits from benefits ither directly taken into account. Furthermore, if Furthermore, taken intoaccount. tive prey. Depending on the situation, itmight onthesituation, Depending tive prey. , it may be defensible to use these abundant , itmay tousethese defensible be vering the population by programs whichaimto programs thepopulationby vering or are worthy of discussion and debate. We We anddebate. ofdiscussion worthy or are duce the suffering experienced by predators. By by predators. experienced thesuffering duce edators are primarily poisoned and to a lesser poisonedandtoalesser areprimarily edators in this sort of experiment: evolutionarily inthissortofexperiment: . Introduced by Europeans, these species have species these Europeans, by Introduced . n mammalsmustinteractwiththemifthey d-sized Australian mammals (Johnson Australianmammals(Johnson d-sized in situ basis (e.g., Vucetich and Nelson Vucetich and basis (e.g., in may negate the need to negate theneed inmay predator exposure; indeed, exposure; predator in situ predationis in situ

potentially genetic change is one example ofhow isoneexample geneticpotentially change ofusing suggestion environments". Our relationships between thetraits Carrollet through what environmental outcomes integration ofevolutionary in minimizing generations thenumberof su reintroduction forimproving Recommendations adapt to astheysubjected tocaptivehousing animals in frames time short occurover can changes genetic that recognize already managers 1998;Hendry, Fa short timeframes(Thompson emphasizing that decisions (Ashley etal.2003), a ofboththeecological consideration called for thera doesnotexceed mortality predator-driven This article is protected Allrights bycopyright. reserved. Accepted and toCalifornia of theredfox a prom predatorsbeing species despiteintroduced To date there has been little focus onthe prey role of naïveté A paradigm shift reduced predators. tokillextant need where itispossible, that itmay we think ultimatelya usefulbe toolthat might even result ina popu we havethreatened adopt inallcaseswhere do success.We used toimprovereintroduction Article The ultimate goal of in situ biology with reintroduction biology withreintroduction biology toimprove islikely predator exposure is to reduce mortality rates so that the rate of rate the that so rates reducemortality to is exposure predator of organisms and the patterns of selection imposed by their imposed patterns ofselection oforganisms andthe subsequent fauna declines (Lewis subsequent fauna in situ captivity (Williams andHoffman2009).Closer (Williams captivity captive conditions (Williams and Hoffman 2009). conditions(Williams and Hoffman2009). captive predation to force rapid behavioral and behavioral toforcerapid predation nd evolutionary cost of resource management management evolutionarycost ofresource nd rrugia, and Kinnison 2008). For instance, and Kinnison2008). rrugia, evolutionary changes can occur over relatively relatively occur over can evolutionary changes not envision this technique being possibleto envisionthistechniquebeing not te of population growth. Recent studieshave of populationgrowth. Recent te al. (2014 pg. 1) term "manipulating the (2014pg. al. 1)term lations ofcaptiveanimal inent cause of species declines. Introductions declines. inent causeofspecies these manipulationsand ccess using captive-bred animals include captive-bred ccess using

in the decline of threatenedin the wildlife decline , Sallee, and Golightly, Sallee,and 1999) Jr s, butinthosecases integrations couldbe change the way that future faunal reintroductions faunal way thatfuture change the situ essential to determine the ultimat essential todeterminethe Detailed tracking versus predator-experiencedprogeny control willbe animals of and their reintroduction increase actually predators with predator versus predator-exposed physic behaviour, theanti-predator by comparing or thetraitsofpopulatio This article is protected Allrights bycopyright. reserved. Acceptedtraits ofwildlifeprey s species Articleintegrated, multi-level approach tothreatened management. species would notdiminishthe importance butrather control, ofpredator assist infacilitatingan resilienceand toco-existence possibleexclusion co-existence. shiftfrompredator Thisparadigm ofintroducedpredatorstoimproving exclusion establish populationsofendange callfornovelstrategies We introduced predators. (Car naïveté ofprey ourunderstanding advancing humans. speciesby inadvertent movementsof in offuturepredator global risk countries. The are predators introduced of impacts the show that predator exposure has thepotential torevolu has predatorexposure With propermonitoring,With The effectiveness of The effectiveness ns have changed after being exposed to exposed being after havechanged ns in situ in situ hould be evaluated. First, wemu hould beevaluated. predator exposure as a method a as predatorexposure red wildlife and strongly encourage a shift in focusfrom ashiftin encourage wildlife andstrongly red e success of this strategy. e successofthisstrategy. naïve individuals.Second,we naïve predator can exposure ethically be Ultimately, defensible. cursions is high, fuelled by the deliberate and deliberate ishigh, the fuelledby cursions Reviews have highlighted the importance of theimportanceof havehighlighted Reviews success outside of predator-free sanctuaries. sanctuaries. outsideofpredator-free success prey responses in order to facilitate future tofacilitate inorder preyresponses tionize reintroduction biologytionize andsignificantly to helpwildlifebiologists protectandre- to al and physiological traits and survival of theyand Banks2014)partic are designed and implemented. Indeed, if the Indeed, ifthe and implemented. designed are not confined toisland ecosystems orspecific of improving anti-predator the st know if animals have learned havelearned st knowifanimals a predator. This can be evaluated This canbeevaluated apredator. must know if these experiences iftheseexperiences must know ularly inrelation to ularly in This article is protected Allrights bycopyright. reserved. L., H.Krupa.1996.Ev Allen, and R.Engeman, Cited Literature and contribution. dr onanearlier and theBlumstein labcommented theAu Fundingwas providedby Acknowledgements essential. thatcontainboth goal ecosystems istorestore Armstrong, D. P., R. S. Davidson, W. J. Dimond, J. Armstrong,D. P.,R.S.Davidson,W. R.andC.Dickman. 2013.Behavi Anson, J. Accepted S.Price,andA. L. M. B.,Beck, Rapaport, Banks,and C.R.Dickman.2007.Alienpreda P.B. Ashley, S.Brown. O.R.Pergams,F.and O'Dowd, S.M.Gende, Willson, J. M.V., D.J. Article assessing dingo populations. Wildlife Research 23:197-205. 23:197-205. Research Wildlife assessing populations. dingo naiveté. Trends in Ecology & Evolution22:229-230. inEcology naiveté. Trends manageme 2003. Evolutionarily enlightened 29:609-621. ofBiogeography Zealand islands.Journal Taylor. Populationdy Griffiths, andJ. 2002. andpredator predators: naiveté animals. 265-286Book. Reintroduction of animals. 265-286Book.

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