fear and stressing in predator--prey ecology: considering ... · fear and stressing in...

Fear and stressing in predatorndashpreyecology considering the twin stressors ofpredators and people on mammalsLoren L Fardell1 Chris R Pavey2 and Christopher R Dickman1

1 School of Life and Environmental Sciences University of Sydney Sydney NSW Australia2 Land and Water CSIRO Winnellie NT Australia

ABSTRACTPredators induce stress in prey and can have beneficial effects in ecosystems but canalso have negative effects on biodiversity if they are overabundant or have beenintroduced The growth of human populations is at the same time causingdegradation of natural habitats and increasing interaction rates of humans withwildlife such that conservation management routinely considers the effects ofhuman disturbance as tantamount to or surpassing those of predators The need tosimultaneously manage both of these threats is particularly acute in urban areas thatare increasingly being recognized as global hotspots of wildlife activity Pressuresfrom altered predatorndashprey interactions and human activity may each initiate fearresponses in prey species above those that are triggered by natural stressors inecosystems If fear responses are experienced by prey at elevated levels on top ofresponses to multiple environmental stressors chronic stress impacts may occurDespite common knowledge of the negative effects of stress however it is rare thatstress management is considered in conservation except in intensive ex situsituations such as in captive breeding facilities or zoos We propose that mitigation ofstress impacts on wildlife is crucial for preserving biodiversity especially as the valueof habitats within urban areas increases As such we highlight the need for futurestudies to consider fear and stress in predatorndashprey ecology to preserve bothbiodiversity and ecosystem functioning especially in areas where human disturbanceoccurs We suggest in particular that non-invasive in situ investigations ofendocrinology and ethology be partnered in conservation planning with surveys ofhabitat resources to incorporate and reduce the effects of fear and stress on wildlife

Subjects Animal Behavior Conservation Biology Ecology Coupled Natural and Human SystemsEnvironmental ImpactsKeywords Fear Stress Anthropogenic Urban Endocrinology Ethology Landscape of fearCumulative CEA Predator

INTRODUCTIONPredators in many systems positively influence the local distribution and abundance oftheir prey (Polis et al 1998 Ayal 2007 Estes et al 2011Weissburg Smee amp Ferner 2014)and indirectly but positively influence the functioning of whole ecosystems via trophiccascades (Prugh et al 2009 Ritchie amp Johnson 2009 Estes et al 2011 Ripple et al 2014)Predators often elicit fear responses in prey that affect prey behaviour energy budgets

How to cite this article Fardell LL Pavey CR Dickman CR 2020 Fear and stressing in predatorndashprey ecology considering the twinstressors of predators and people on mammals PeerJ 8e9104 DOI 107717peerj9104

Submitted 26 September 2019Accepted 9 April 2020Published 30 April 2020

Corresponding authorLoren L Fardelllfar3796unisydneyeduau

Academic editorMax Lambert

Additional Information andDeclarations can be found onpage 19

DOI 107717peerj9104

Copyright2020 Fardell et al

Distributed underCreative Commons CC-BY 40

and the way they interact with the environment (Brown amp Kotler 2004 Clinchy et al 2004Romero 2004) For example the fear response of an individual of a prey species to apredator may be to change the locations or times in which they forage which can havepositive impacts on the structure of the environment (Laundreacute Hernaacutendez amp Ripple2010) Such fear responses can in turn influence ecosystem function (Schmitz Krivan ampOvadia 2004 Schmitz Beckerman amp OrsquoBrien 1997 Hawlena et al 2012) These effectsarise due to the lsquolandscape of fearrsquo that prey individuals perceivemdashthat is the spatialdistribution of perceived predation risk that influences prey movement and behaviour asprey individuals attempt to mitigate risk and obtain essential resources (LaundreacuteHernaacutendez amp Altendorf 2001 Laundreacute Hernaacutendez amp Ripple 2010)

Recent studies suggest that the effects of predators are being altered and oftenamplified by human activities For example the demise of top predators in many parts ofthe world has lsquoreleasedrsquo populations of smaller predators or mesopredators that have sincebecome overabundant and now exert strong pressure on smaller species (Prugh et al2009) Predators that have been introduced to new areas also exert much stronger pressureon prey populations than do native predators (Salo et al 2007) Climate change andassociated shifts in primary productivity can also have bottom-up impacts onpredatorndashprey interactions (Laws 2017) Such novel alterations to predatorndashpreydynamics can depress prey populations and disrupt community structure and as suchrequire novel approaches to recognize and manage their effects (Carthey amp Blumstein2018 Fleming amp Bateman 2018 Guiden et al 2019)

Altered predatorndashprey interactions may contribute to declines in biodiversity but aprimary cause of biodiversity loss is the rapid global increase in human populationsdriving agricultural industrial and urban expansions that change or destroy naturalhabitats (Madsen Carroll amp Moore Brands 2010) Such expansions are resulting in novelhumanndashwildlife interactions and secondary impacts that arise from human activities inclose proximity to natural environments and thus increasingly are becoming an additionalstressor that influences ecosystem function Pressures exerted both directly and indirectlyby human activities have been likened to the pressures exerted by the presence of atop predator on prey (Frid amp Dill 2002 Rehnus Wehrle amp Palme 2014 Patten amp Burger2018) Natural predation pressures coupled with human-imposed predation-like pressuresandor additional exogenous stressors such as pollution arising from anthropogenicactivities are likely to negatively affect prey species by increasing their levels or frequencyof stress Current research is developing a more nuanced understanding of the effectsof human activity and predator presence on the stress of prey (Arlettaz et al 2015Jaatinen Seltmann amp Oumlst 2014 respectively) However few studies in terrestrialecosystems have considered both of these pressures simultaneously or have linkedbehavioural responses with endocrinological evidence of stress In one instructive recentstudy human activity was shown to be positively correlated with physiological stress inungulates whilst in areas occupied by large predators stress was found to be lower and lessvariable (Zbyryt et al 2017)

Conservation management and associated scientific research is often viewed from theperspective of a single discipline However ecological changes arising from anthropogenic

Fardell et al (2020) PeerJ DOI 107717peerj9104 235

disturbances including the alteration of predatorndashprey encounter rates creation of novelspecies interactions (including between people and wildlife) introduction of novel speciesand the alteration of natural habitats call for multidisciplinary solutions This isparticularly pertinent as urban edge habitats are becoming increasingly valuable globalhotspots of wildlife activity (Ives et al 2016) and human influences are spreading furtherinto natural habitats (Otto 2018) There is growing evidence that multiple introducedstressors (eg altered predatorndashprey interactions and disturbance from humans) can havecompounding impacts on wildlife especially when interacting with natural stressors inecosystems (Geary et al 2019) For these reasons it is timely to review relevantinformation from the broad knowledge bases of conservation physiology ethology andecology to communicate the urgent need for wildlife managers and urban planners toroutinely consider how fear and stress effects from multiple sources particularly novelpredator interactions and human activities can affect prey species and ecosystemfunctioning in increasingly altered systems Our focus in this review is on mammalsbecause of the wealth of information on this group but we note relevant studies from othergroups where appropriate We begin our review by describing physiological responsesof mammals to fear and stress then we consider the behavioural responses of mammals tothese factors and argue that human activity should be considered as part of the ecosystemso that overall stress impacts can be managed accordingly We then demonstrate howfear and stress can influence habitat use how vegetation and microhabitat managementpotentially may be used to alleviate stress and how to monitor for fear and stress tothen create management change Finally we use Australia as an example to show thebenefits of considering cumulative fear and stress impacts to mitigate the effects ofintroduced eutherian predators increased human activity and the possible interactiveeffects of the two

REVIEW METHODThis is not a systematic review but rather a novel synthesis of existing knowledge It seeksto extend ideas on the physiological impacts of fear and stress behavioural ecologypredatorndashprey dynamics and conservation management to explore the influence ofhumans and altered predatorndashprey interactions in the urban environment To ensure thatall key topic areas were thoroughly covered we conducted literature searches via GoogleScholarcopy Web of Sciencecopy JSTORcopy and Wiley Interscience Online LibrarycopyManuscripts were mined for information relevant to wildlife fear and stress in terms ofecological management under anthropogenic pressures including introduced predatorsand altered predatorndashprey interactions The literature searches were undertaken usingthe following key terms as part of their title keywords andor within the abstract lsquoacutestressrsquo lsquochronic stressrsquo lsquohomeostasisrsquo lsquocumulative stressrsquo lsquomultiple stressorsrsquo lsquomultiplethreatsrsquo lsquoallostatic loadrsquo lsquoallostatic overloadrsquo lsquoacclimitisationrsquo lsquoglucocorticoid responsersquolsquohypothalamic pituitary adrenal axisrsquo lsquofear arousalrsquo lsquofear evolutionrsquo lsquofear predationrsquolsquoamygdalarsquo lsquofearrsquo lsquoPavlovian fear conditioningrsquo lsquoglucocorticoid assayrsquo lsquof(a)ecalglucocorticoidrsquo lsquonon-invasive glucocorticoid assayrsquo lsquoreactive scope modelrsquo lsquolandscape(s) offearrsquo lsquorisk allocation hypothesisrsquo lsquoolfactionrsquo + lsquofearrsquo + lsquomammalrsquo lsquopost-traumatic stress


disorderrsquo lsquopredatorrsquo + lsquoodo(u)rrsquo + lsquofearrsquo lsquopredator cue(s)rsquo lsquopredation stress hypothesisrsquolsquopredator-sensitive food hypothesisrsquo lsquohuman activityrsquo + lsquostressrsquo + lsquowildlifersquo lsquohumandisturbancersquo lsquointeractive stressrsquo lsquomultiple stress(ors)rsquo lsquoadditive stress impactsrsquo lsquosynergisticstress impactsrsquo lsquoantagonistic stress impactsrsquo lsquohumanrsquo + lsquowildlifersquo + lsquoresource subsidiesrsquolsquopredator trophic cascadersquo lsquowildlife urban adaptationrsquo lsquourban ecologyrsquo + lsquowildlifersquolsquoAustralian mammal extinctionrsquo lsquocritical weight range mammalrsquo lsquodietrsquo + lsquochangersquo +lsquoAustralianrsquo + lsquopredatorrsquo lsquored foxrsquo + lsquoAustraliarsquo lsquodomestic catrsquo + lsquoAustraliarsquo lsquohumanactivityrsquo + lsquowildlifersquo + lsquoAustraliarsquo lsquoAustraliarsquo + lsquobiodiversityrsquo + lsquoconservation policyrsquo +lsquourban hotspotrsquo lsquoAustralian environment protection and biodiversity conservation actrsquo +lsquocumulative stressrsquo lsquoAustraliarsquo + lsquoconservationrsquo + lsquoglucocorticoidsrsquo lsquointroduced predatorcontrolrsquo lsquohabitat structural complexityrsquo lsquohabitat structural diversityrsquo lsquovegetation diversityrsquolsquovegetation heterogeneityrsquo lsquohabitat heterogeneity hypothesisrsquo lsquocumulative effectsassessmentsrsquo Supplementary articles supporting the review narrative suggested byreviewers on earlier versions of the manuscript have also been included

MAMMALIAN PHYSIOLOGICAL RESPONSES TO FEARAND STRESSPhysiological stress can be broadly defined as a change in the physiological well-being of anindividual following exposure to an aversive extrinsic stimulusmdashfrequently referred to asa stressor (Selye 1936) The physiological stress response that follows aims to restoreinternal homeostasis (Cannon 1932) An individual animal experiences stress in responseto conditions that threaten its survival or compromise its ability to maintain homeostasisExamples include acute or chronic encounters with predators inclement weathersignificant natural disturbances including fire and flood reduced oxygen availability anddepleted food resources (Lima 1998 King amp Bradshaw 2010 Malcolm et al 2014Santos et al 2014 Crocker Khudyakov amp Champagne 2016)

In mammals activation of the hypothalamic-pituitary-adrenal (HPA) axis is a commonstress response but this may vary depending on the nature of the stressor (Mason 1971)it is important to consider this when assessing stress impacts Changes in abioticconditions such as in food availability or the introduction of toxins or diseases can bestressful but such changes do not arouse fear However a stress response involvingperipheral autonomic and neuroendocrine changes (Yates Russell amp Maran 1971Sapolsky Romero amp Munck 2000 McEwen amp Wingfield 2003) can be initiated by feararousal (LeDoux 2003 Labar amp Ledoux 2011) Animals with sophisticated nervoussystems such as mammals exhibit a central motive state between threat stimulus andresponse that is driven by the amygdala (Pitkanen 2000) and can be identified as lsquofearrsquo(Mineka 1979 Oumlhman 2000) Fear has been defined as a psychological state that triggersphysiological responses to avoid or escape from a stressor (Epstein 1972 LeDoux 1996)The development of successful defense mechanisms to fear-inducing stressors has clearsurvival benefits for animals and thus fear can be seen as a driver of evolutionaryadaptations (Tooby amp Cosmides 1990) Common strategies of escape and avoidance allowanimals to cope with recurrent stressors such as the fear-inducing threat of predation(Lima amp Dill 1990)


The sections of the mammalian amygdala associated with fear behaviour serve as aninterface between sensory input and information transport and processing endocrineresponse and motor output (Davis amp Whalen 2001) These interactions are associatedwith learning and memory via the involvement of the lateral and basal nuclei asdemonstrated on captive rodents using neurotoxic lesions on the basal and lateral nuclei ofthe amygdala (Wallace amp Rosen 2001) and are evident in Pavlovian fear conditioningparadigms (Davis 1992 Maren 2001) Activation of hormones specificallyglucocorticoids and norepinephrine in stress responses initiated by fear arousal providesfeedback to the brain that influences emotion control and cognition which contributes tofear conditioning (Rodrigues LeDoux amp Sapolsky 2009) Fear responses may thereforebe both conditioned as aversive learnt behaviours (Fanselow amp Poulos 2005) andunconditioned as innate freezing responses (eg Schulkin Thompson amp Rosen 2003)

Given that fear motivates a stress responsemdashinitiating the freeze and fight or flightactionsmdashquantifying glucocorticoid outputs from the autonomic nervous and HPAsystems should yield a measurable indication of fear from predation as a stressorMinimally invasive techniques are available that assay glucocorticoid levels in faeces furor feathers (Sheriff et al 2011 Cook 2012 Palme 2019) Using minimally invasivemethods to measure glucocorticoid levels in the wild does not necessarily yield an isolatedlsquooutputrsquo of a fear or predatorhuman-induced stress response (Rosen amp Schulkin 2004)This situation results from glucocorticoids not being a molecule of fear per se but having afundamental role in maintaining energy balance (Rosen amp Schulkin 2004) As suchglucocorticoids may change not just because of fear but also in response to otherexogenous stressors like food shortage (McEwen amp Wingfield 2003) Nevertheless suchmethods could usefully compare longer-term stress responses among habitats or alongdisturbance gradients with variable exposure to predators by following experimentaldesigns that are considerate of additional stressors that may be present (MacDougall-Shackleton et al 2019)

If two or more stressors are present the resultant combined stress may present severechallenges to an individualrsquos physiological systems (Johnstone Lill amp Reina 2012 Brearleyet al 2013 Malcolm et al 2014 Arlettaz et al 2015 Geary et al 2019 Legge et al2019) Interactive fear and stress effects are context-dependent (Belarde amp Railsback2016) They can be additive and combine the multiple impacts synergistic whereby thepresence of one threat amplifies another (Doherty et al 2015) or antagonistic whereby onethreat cancels the effects of the other A reduction in the activity of mesopredators inthe presence of humans provides an example of antagonism (Clinchy et al 2016)Additive synergistic and antagonistic reactions have each been observed in mammalianprey in natural systems in response to exposure to multiple stressors (Crain Kroeker ampHalpern 2008 Cocircteacute Darling amp Brown 2016 Gunderson Armstrong amp Stillman 2016Jackson et al 2016 Geary et al 2019 Legge et al 2019)

Exposure to a stressor(s) that is prolonged constant or recurring can have chronicimpacts as recovery from a stressor cannot occur whilst the threat remains (SapolskyRomero amp Munck 2000) Acute stress occurs as the initial response to a threat to sustainfitness in the short term it subsides once the responding actionmdashbe it freezing fighting or


fleeingmdashdiminishes the threat (Wingfield amp Kitaysky 2002) Activation of the HPA axis inan acute stress response has rapid effects that increase immune system function energisemuscles via enhanced cardiovascular tone and heighten cognition including memory(Sapolsky Romero ampMunck 2000) These responses occur via increased cerebral perfusionrates and use of glucose all of which come at the cost of decreased appetite andreproductive behaviours (Sapolsky Romero amp Munck 2000) Effectively the acute stressresponse suspends non-essential behaviours in favour of altered behaviours that minimizethe threat (Wingfield amp Kitaysky 2002)

Continued exposure to a stressor or stressors creates a state of chronic stress which isclassically described as allostatic overload (Dantzer et al 2014) Allostatic load describesthe bodyrsquos ability to maintain homeostasis in response to a stressor (Sterling amp Eyer1988 McEwen amp Stellar 1993 McEwen amp Wingfield 2003) Allostatic overload byextension refers to the inability to maintain homeostasis and thus an organismrsquos increasedsusceptibility to external stressors (Sterling amp Eyer 1988 McEwen amp Stellar 1993McEwen amp Wingfield 2003) Chronic stress reduces an organismrsquos resilience to futurestressors by inducing extended behavioural changes in feeding fighting and mating(Mineur Belzung amp Crusio 2006) Chronic stress also affects an organismrsquos physiologicalstate by suppressing or impairing the reproductive system and decreasing physiologicalresistance to pathogens and toxins through the suppression of immune function(Dhabhar ampMcEwen 1999McEwen ampWingfield 2003 Romero 2004 Travers et al 2010Feng et al 2012) Repeated exposure to a stressor can have population and communitylevel consequences as homeostasis is compromised and it increases susceptibility toadditional stressors and can have flow-on effects For example chronic risk of predationwhich facilitates changes in nutrient demand for prey species and thus changes in theelemental composition of their excreta can alter nutrient cycling in the community andecosystem (Hawlena amp Schmitz 2010)

Cases of acclimatisation to chronic or repeated acute stressors have been observedalthough the process often results in enhanced activation of the HPA axis to novelstressors and thus may not be beneficial to fitness (Romero 2004) Instead of acclimatisingto a chronic or repeated stressor glucocorticoid levels can remain the same or becomechronically elevated or the HPA axis can shut down completely and render an animalvulnerable to future threats (Romero 2004) Physiological impairment of the neurologicalcardiovascular and musculoskeletal systems may also result from chronic stress neuronsof the brain can atrophy and impair memory or grow and enhance fearfulness withextensive releases of adrenaline and cortisol (Roozendaal 2000 McEwen 2004)atherosclerotic plaques also may form and impede blood flow from repeated elevation ofblood pressure (Manuck et al 1988) and skeletal muscle can suffer severe protein loss(Wingfield amp Kitaysky 2002)

Although chronic and acute stress responses have been well defined for mammals inlaboratory studies results from in situ studies show that reactions vary with the stressortype that animals are exposed to as well as habituation potential food availabilitysocial interactions and density (Dickens amp Romero 2013) In situ mammalian endocrineresponses to a consistent stressor such as human activity have not been studied


sufficiently to be able to determine if there is a particular pattern of response Avianendocrine responses to such stressors have been more extensively studied and they revealthat urban habitats perceived as a consistent stressor can shape endocrine responsesin birds However a consistent stress response pattern has yet to be observed in birds(Bonier 2012) Inconsistent behavioural responses of mammals and other animals tohuman activities that are often observed can perhaps be linked to modulating factors suchas the level of human activity the species and condition of the animal being observed andthe spatio-temporal context (Tablado amp Jenni 2017)

MAMMALIAN BEHAVIOURAL RESPONSES TO FEAR ANDSTRESS THE LANDSCAPE OF FEAR CONCEPTThe landscape of fear concept (Laundreacute Hernaacutendez amp Altendorf 2001) postulates thatprey are aware of microhabitat patches associated with high and low predation risk wherepredators are either active and ubiquitous or scarce (Laundreacute Hernaacutendez amp Altendorf2001 Shrader et al 2008 Van Der Merwe amp Brown 2008 Laundreacute Hernaacutendez ampRipple 2010) Theoretically landscape of fear effects should increase with landscapeheterogeneity since the differences between high and low risk sites become morepronounced and prey can more easily avoid high-risk sites (Bleicher 2017 Gaynor et al2019) However this relationship can depend on the species and condition of thehabitat and for some species simple habitats can be the safest (Hammerschlag et al 2015Schmidt amp Kuijper 2015 Atuo amp OrsquoConnell 2017) Landscape of fear effects will also bemore pronounced in systems where interactions between predators and prey are lessfrequent (Schmitz 2008) as is evident in findings from Pavlovian fear conditioning andthe lsquorisk allocation hypothesisrsquomdashwhich states that animals exposed to constant highpredation risk will increase their foraging risks over time (Lima amp Bednekoff 1999Van Buskirk et al 2002) Fear arousal in a landscape of fear results in two predictableoutcomes either avoidance of high risk areas or modulation of behaviour (eg increasedvigilance) to reduce predation risk when foraging in such areas (Gaynor et al 2019)These outcomes indicate the potential positive benefits to conservation management ofconsidering fear arousal and stress levels and the direct and indirect cues that may triggerthese effects (Atkins et al 2017)

The likelihood of survival of a prey species is improved by having a well-developedperception of high predation risk as it allows adaptive behavioural responses to beestablished (Boacutekony et al 2009) Habitat shifts temporal shift grouping vigilance andfreeze fly and fight responses are the most studied such responses to the non-consumptiveeffects of predators (Say-Sallaz et al 2019) These often develop due to increasedinteraction rates between predators and prey However chronic stress impacts that aresufficient to affect reproduction and long-term survival can be experienced by prey speciesperceiving recurring predation risks (Thomson et al 2010 Clinchy et al 2011)Chronic perceived predation risk may also result in altered foraging activity driven by fearThis can affect where and what prey eat (Schmitz Krivan amp Ovadia 2004) causing themto move from risky to sheltered microhabitats (Trussell Ewanchuk amp Matassa 2006)


in turn altering the distribution and availability of resources Fear-based adaptivebehavioural responses such as these underlie the landscape of fear concept

For mammals fear arousal can be triggered both by a predatorrsquos presence or by apredator cue such as an associated scent Olfaction can be a key driver of fear arousal(Soso et al 2014 Banks Daly amp Bytheway 2016 Jones et al 2016 Parsons et al 2017)The mechanics of this are best understood in mammals odours are detected by theaccessory olfactory bulb that transmits information directly to the amygdala andhypothalamus where fight or flight responses are developed (Fogaca et al 2012 CanterasPavesi amp Carobrez 2015) Laboratory studies exploring the effects of post-traumaticstress disorder have exposed small mammals to predators or their cues to induce stressand in doing so revealed that exposure to predator cues alone can affect the neural circuitryassociated with fear (Rosen amp Schulkin 1998 2004)

Subtle cues such as predator odours may precede threats and allow for a mammalianprey animalrsquos fear state to be conditioned to a cue that occurs before or in correlation witha previously encountered predation threat (Rescorla amp Solomon 1967 Rosen 2004)Predation risk may therefore be perceived by prey species eavesdropping on predatorscent marks such as urine faeces or fur in the environment (Banks Daly amp Bytheway2016 Jones et al 2016) Such odours have been observed experimentally to induce fear-likeresponses of freezing (Wallace amp Rosen 2000) vigilance (Nersesian Banks amp McArthur2012) fleeing (Anson amp Dickman 2013) and avoidance (Hayes Nahrung amp Wilson2006) across a wide range of species in both field and laboratory experiments (Apfelbachet al 2005 2015) Consequently landscape of fear topography where predators indirectlyinfluence prey behaviour across a range of microhabitats can arise from the influenceof predator olfactory cues on mammalian prey foraging behaviours as much as it can fromthe direct threat of predation (Brown amp Kotler 2004 Parsons amp Blumstein 2010 CremonaCrowther amp Webb 2014 Mella Banks amp McArthur 2014 Hoffman Sitvarin ampRypstra 2016) It is worth noting however that whilst predator olfactory cues can elicit afear or stress response they do not always do so (Apfelbach et al 2005) This may bebecause predators often leave the site after depositing a cue and the cue intensitydiminishes Predator cues elicit responses that are modulated according to the differentialintensity of the perceived threat prior experience or pending further informationgathering and thus can be perceived as a low risk by prey (Bedoya-Peacuterez et al 2019)

Fear arousal due to predator presence or cues can deplete a prey individualrsquos energybudget resulting in poor reproduction and health either via energy exhaustion from stress(ie the predation stress hypothesis Boonstra et al 1998 Clinchy et al 2004 Romero2004 Stoslashen et al 2015) or reduced nutrition from foraging compromises (Brown ampKotler 2004 Clinchy et al 2016) As food resources become limited additionally preymay take greater risks to meet nutritional needs (ie the predation-sensitive foodhypothesis Sinclair amp Arcese 1995) but at a possible cost of additional stress In areas ofhigh human activity this may result in wildlife increasing the stressors they are exposedto as they seek human-based food sources such as waste or pet food and in doing soincrease their exposure to domestic pets altered light increased sound and vehicles(Navara amp Nelson 2007 Morgan et al 2009 Riley et al 2014 Shannon et al 2016


Doherty et al 2017) For managers mitigating fear arousal mapping landscapes of fear(Van Der Merwe amp Brown 2008 Kauffman Brodie amp Jules 2010 Iribarren amp Kotler 2012Smith et al 2019) to identify protect and extend safe foraging areas could assist in theconservation of wildlife subject to human activity or multiple stressors such as humanactivity and predators

HUMAN ACTIVITY AS A FEAR-INDUCING STRESSORHuman activity can influence wildlife in a wide variety of ways (Albert amp Bowyer 1991Bowyer et al 1999) Pressure from increased proximity to human activity or developmentthat encroaches upon animal home ranges results in wildlife becoming either (1) lsquourbanavoidersrsquo that move away from human activity (2) lsquourban adaptersrsquo that make someuse of anthropogenic resources but still rely largely upon those found naturally or(3) lsquourban exploitersrsquo that are synanthropic and make full use of anthropogenic resources(McKinney 2006) The effects of human activity can therefore differ between speciesand trophic levels and even within the same species depending on personalityFurthermore the negative effects of a disturbance on one species may result in flow-onresponses of positive consequences for its prey predators or competing species (GillSutherland amp Watkinson 1996 Crooks amp Souleacute 1999 Leighton Horrocks amp Kramer2010) These effects however depend strongly on the availability of necessary resourceswithin the human occupieddisturbed areas and will often differ between systems

It has been postulated that humans may impose widespread effects on ecosystemfunction if they induce greater fear responses in ubiquitous small predators than in toppredators (Clinchy et al 2016) or by increasing physiological stress in large ungulatesthrough antagonistic behaviours (Vijayakrishnan et al 2018) Indeed human activity canbe comparable to the above-mentioned impacts of predation creating landscapes offear (Hofer amp East 1998 Frid amp Dill 2002 Rehnus Wehrle amp Palme 2014 Patten ampBurger 2018) and disrupting foraging (Ciuti et al 2012 Clinchy et al 2016) Humans canalso act as lsquosuper-predatorsrsquo that disproportionately kill carnivores and drive trophiccascades (Darimont et al 2015) Trophic cascades can also arise when human activity hasnon-consumptive effects on the ecological roles of large predators (Smith et al 2017)For example large predators may increase their hunting efforts in urban areas if their ownfear response to human activity results in less time spent consuming a kill this in turnmay increase their kill rate of prey in urban areas to meet their energy needs (Smith et al2017) When large predators avoid human activity andor meso-predators reduce theirforaging around human activity prey species may respond by increasing their ownforaging activity (Suraci et al 2019) effectively taking refuge behind the lsquohuman shieldrsquothat is reducing predation pressure for them (Berger 2007 Leighton Horrocks amp Kramer2010 Kuijper et al 2015)

Human activity can affect the trophic structure of communities not only via top-downpressure but also by exerting bottom-up pressure through the constant provision ofalternative resources (Fischer et al 2012) such as subsidies of shelter water and food withyear-round primary production These resources can outweigh the stresses of humandisturbance and influence population and community behaviours (Parris 2016) resulting


in urban colonisation by wildlife (Shochat Lerman amp Fernaacutendez-Juricic 2010 Jokimaumlkiet al 2011) As such human activity does not always result in fear responses particularlyfor prey species that benefit from the human shield and access to food water or sheltersubsidies (Lyons et al 2017) It is possible that given these conditions and providedthat resource subsidies are nutritionally rich and accessing them does not increasepathogen transmission risk (Murray et al 2016) prey species like small mammals wouldexperience fitness benefits in urban areas Resource subsidies can also be exploited bypredators resulting in increased predator activity in urban areas but also in alteredforaging behaviours that either decrease or increase predation on small prey (Iossa et al2010 Bateman amp Fleming 2012 Fischer et al 2012 Newsome et al 2014 2015)

Despite such positive effects of human activity on wildlife negative impacts are morepervasive for many species The negative effects of high levels of disturbance for examplefrom roads and vehicles or of active interference from recreational activities conductedin designated conservation areas can lead to physiological stress or displacementcountervailing any positive effects of humans on wildlife (Kloppers St Clair amp Hurd 2005Banks amp Bryant 2007 Berger 2007 Ciuti et al 2012 Rehnus Wehrle amp Palme 2014Arlettaz et al 2015 Patten amp Burger 2018 Vijayakrishnan et al 2018)

A common response in mammals to increased exposure to human activity is a temporalshift in activity patterns from diurnal to crepuscular or nocturnal to avoid interactionwith humans (McClennen et al 2001 Tigas Van Vuren amp Sauvajot 2002 Riley et al2003 Ditchkoff Saalfeld amp Gibson 2006 Gaynor et al 2018) the same or reverse mayoccur too to reduce interactions with predators (Brown 2000 Laundreacute Hernaacutendez ampAltendorf 2001 Kohl et al 2018 Smith et al 2019) Temporal shifts can have stronglynegative effects if they limit a foragerrsquos ability to locate and capture prey (DitchkoffSaalfeld amp Gibson 2006) Regardless of the response it is evident that human activitycan have profound indirect effects on community interactions through altering individualbehaviour particularly foraging through either fear arousal or a stress response(Frid amp Dill 2002 Werner amp Peacor 2003)

The ability of wildlife to cope with urban environments can occur through either plasticor evolved shifts in behaviour foraging food preferences or predator avoidance andin shifts in the timing of breeding (Ditchkoff Saalfeld amp Gibson 2006 Moslashller 2009Shochat Lerman amp Fernaacutendez-Juricic 2010 Rodriguez Hausberger amp Clergeau 2010Alberti 2015McDonnell amp Hahs 2015Otto 2018 Santini et al 2019) It is most commonfor urban-occupying species to plastically adjust to human imposed stressors (Donihue ampLambert 2015) with some ultimately evolving tolerance to urban environmentsHuman activity can therefore impose pressures that are strong enough to influencechanges in behaviour and in physiologymdashendocrinology in particular (Bonier 2012 Snell-Rood amp Wick 2013 Otto 2018) Bolder individuals are most likely to exploit novelopportunities and have reduced stress responses to human activity (Atwell et al 2012)Animals that routinely encounter human activity typically provide parental care and arecapable of reproducing multiple times across their life span may produce offspring thatare acclimated to human activity and accordingly show lower fearstress responses


(Schell et al 2018) Habituation of groups of animals to human activity is beingincreasingly observed often as a result of bold individuals spending significant amounts oftime around human-disturbed areas and displaying reduced fear responses (Stillfried et al2017) This counters the idea that human activity always imposes landscapes of fearbut may reflect the combination of reduced resource availability and bold personalities thatallow for urban habituation (Lowry Lill amp Wong 2013) In some instances this may beproblematic for humans if increased interactions with habituated animals increasevehicle accidents andor transfer of zoonotic diseases this highlights the potential need tomanage some mammalian prey species in urban areas (Honda et al 2018)

Fear and acutechronic stress may be constant hurdles faced by wildlife but adding theeffects of anthropogenic disturbance could result in the elevation of acute stress responsesto prolonged and widespread chronic stress and upscale the possible impacts fromindividuals to populations (Rehnus Wehrle amp Palme 2014) As we have outlined humanactivity can both indirectly and directly create landscapes of fear influencing andamplifying existing landscapes of fear through interactive effects Predator presence andhuman activity can also interact to alter ecosystem structure and modify the predationrisk perceived by prey species with either positive or negative impacts dependent uponthe circumstances The combination of stress resulting from the pressures of alteredpredatorndashprey interactions and human activities is yet to be investigated extensivelyUnderstanding the cumulative effects that both may impose is critical for effectiveconservation of wildlife in an increasingly human-influenced world

ALLEVIATING FEAR AND STRESS FOR WILDLIFECONSERVATIONAs we have illustrated fear can produce stress and simultaneous multiple stressors canhave chronic effects that negatively influence both predator and prey species populations(Allan et al 2013) To synthesize these impacts we note that in modern urban situationsboth habitat stressors and introduced stressors now collide (Fig 1) Habitat stressorsresult from naturally occurring environmental factors such as native predator presence(especially for prey) social and reproductive pressures limited access to refugesnestsandor food and water and disease and parasite prevalence all of which produce predictivehomeostasis responses by prey species (Fig 1) Introduced stressors by contrast areadditional stressors that are imposed by human actions that result in reactive homeostasisresponses These introduced anthropogenic stressors include structural developments thatchange landscapes human recreational activities in natural habitats (including use ofvehicles) introduced pollutants and toxins that alter landscapes and resource quality andintroduced predators and altered predatorndashprey interactions (Fig 1) The combination ofimpacts from both naturally occurring and introduced anthropogenic stressors has thepotential to cause a cumulative stress response that can result in homeostatic overload orfailure as defined by Romero Dickens amp Cyr (2009) and may result in population collapsesdue to increased susceptibility of individuals to the additional stressors (as we havedemonstrated above and Fig 1) Cumulative stress may be additive or synergistic and is


likely to be particularly detrimental for prey species For example if prey species facemultiple stressors they may take greater foraging risks or be less able to allocate energy tovigilance or flight behaviours and thus become more susceptible to predation or additionalstressors In the case of population-impacting stressors the local population may beimpacted to a high degree such that it becomes threatened (Sweitzer 1996 Doherty et al2015) As such conservation action in areas where simultaneous introduced stressorsoccur in addition to natural ecosystem pressures like in urban and peri-urban habitatsmay be urgently needed

The most direct way to alleviate stress in wildlife is to remove or reduce the keystressors This may be difficult if the stressors are anthropogenic as the needs of theexpanding human population often usurp those of wildlife alternative solutions then needto be considered A suite of activities related to managing vegetation structure densityandor heterogeneity may well provide such an alternative solution These activities resultin increased availability of potential refuge sites and may be readily achieved throughongoing habitat engineering that for example supports the growth of structurally complexplants or adds logsrock piles to reduce areas of open space In order to mitigate introducedfear and stress effects it is important that future studies investigate whether vegetationmanagement and other habitat components can alleviate some of the pressures associatedwith multiple introduced stressors for target species

Figure 1 A Venn diagram showing two main categories of stressor On the left are stressors that occurnaturally in ecosystems such as native predators social and breeding interactions availability of refugeand burrowden microhabitats diseaseparasite prevalence and availability of food and water On theright are introduced stressors primarily those arising from anthropogenic disturbances such as urbandevelopments human activity introduced toxins and introduced predators Where both categories ofstressor occur together simultaneously as in many urban environments cumulative stress impacts canresult in homeostatic overload or failure (as defined by Romero Dickens amp Cyr (2009)) In these situationspopulations may be at particular risk of collapse and conservation action will be most urgent

Full-size DOI 107717peerj9104fig-1


MANAGING HABITAT TO ALLEVIATE WILDLIFE FEARAND STRESSThe impact of predators (or human activity) can be mitigated by changing the configurationof risky areas within a habitat (Hopcraft Sinclair amp Packer 2005 Lone et al 2014)Food availability often drives habitat selection (Sherman 1984 Johnson amp Sherry 2001) butpredation risk and human activity affect a suite of correlated factors such as movementdecisions (Turcotte amp Desrochers 2003) foraging patterns (Gil Zill amp Ponciano 2017) socialorganisation (Rodriacuteguez Andreacuten amp Jansson 2001) and reproductive success (Zanette et al2011) Supplementation of essential resources including refuges nests or roosts food andwater to wildlife is a growing conservation method due to its ease of implementationimmediate results and favourable portrayal in the media One example of positive resultsincludes increased parasite resistance in nestling birds after supplementation withhigh-quality food during the stressful young-rearing stage (Knutie 2020) Another exampleis the reduction in impact from introduced predators on small desert mammals following theaddition of artificial refuge structures (Bleicher amp Dickman 2020) Despite these successesnegative impacts can also ensue following supplementation Built-up refuges may beprimarily investigated by invasive species such as the black rat (Rattus rattus) which couldpotentially deter commensal native species and support the population growth of invasivespecies (Price amp Banks 2018) Artificial nests or roosts can support increased predation ratesowing to the structure supporting a sit-and-wait predator at the exit (McComb et al 2019)Food and water subsidies can increase pathogen transmission reduce movement andmigratory behaviours increase predatorndashprey interaction rates and competitor aggressioninteractions (Murray et al 2016) However owing to the benefits of supplementationespecially during times of stress it may be used as a tool to mitigate the negative impacts ofstress on wildlife if conducted in a targeted monitored and well-considered manner(Freeman et al 2020)

Considering the existing knowledge base on food and water supplementationmeta-analyses have suggested that the associated disease risk may be managed byfocusing on specific natural food sources and pathogen groups subject to the targetecosystem and by increasing the spatial extent of feeding stations across potential linkedhabitats which also limits microparasite host aggregations (Becker Streicker amp Altizer2015 Becker et al 2018) In considering the specific needs of target animals andecosystems chainsaw-carved cavities have more favourable thermodynamic propertiesfor small mammals and birds than do artificial next boxes (Griffiths et al 2018)As they mimic natural hollows they are also less likely to increase rates ofpredation Supplementation projects are therefore moving forward using this growingknowledge base to adaptively tailor methods to specific conditions and to orchestratepre- and post-monitoring that ensures successful stress mitigation (Civitello et al2018)

Survivorship of prey in the face of predation stressors is often positively correlated withincreased structural complexity of the habitat (Hopcraft Sinclair amp Packer 2005 Loneet al 2014 Leahy et al 2016) This has been demonstrated in many studies to be a


consequence of the increased opportunities for prey to escape and hide thereby mediatingpredatorndashprey dynamics by reducing encounter rates as only a proportion of the total preypopulation remains available to predators (Holt 1984 Kotler amp Brown 1988 BianchiSchellhorn amp Van der Werf 2009 Rieucau Vickery amp Doucet 2009 Klecka amp Boukal 2014Laundreacute et al 2014) The extensive research on the benefits to prey of habitat structuralcomplexity builds on the lsquohabitat heterogeneity hypothesisrsquo which postulates thatstructurally complex habitats support increased species diversity by offering a wide rangeof niches and diverse ways of exploiting resources (Bazzaz 1975) Habitat complexityby extension has been generalized to be a primary driver of biodiversity (Pianka 2011)The landscape of fear concept accepts this principle too in that a wide range ofmicrohabitat types offers multiple foraging and shelter conditions with varied predationrisks for species For example northern quolls (Dasyurus hallucatus) of the semi-aridPilbara region in Western Australia utilise complex rocky habitats in preference toopen grasslands where the threat of predation from feral cats (Felis catus) is greater(Hernandez-Santin Goldizen amp Fisher 2016)

Animals in habitats with high predation pressure may display foraging preferencesfor microhabitats or times that they perceive to be safe (Brown 2000 LaundreacuteHernaacutendez amp Altendorf 2001 Laundreacute Hernaacutendez amp Ripple 2010) Some smallmammals seek structurally complex vegetation owing to the reduced risk of predation andincreased reward of foraging they find there (Lima amp Dill 1990 Andruskiw et al 2008)Others such as the Australian hopping mouse (Notomys alexis) that exhibit bursts ofspeed in open habitat are less adept at moving through complex vegetation (SpencerCrowther amp Dickman 2014) No matter the species in landscapes of fear a preyspeciesrsquo use of the topography refuges and escape substrates can indicate its perceivedrisk of predation (Brown amp Kotler 2004 Van Der Merwe amp Brown 2008 Shrader et al2008) and the associated fear and stress that may arise or be alleviated due tohabitat structure The same principle should be relevant to reducing stress in proximity tohuman activity considering that prey responses to human activity and predators aresimilar

Human activity and disturbance can quickly reduce habitat complexity (Western 2001)However enhancing habitat complexity and heterogeneity is being incorporatedincreasingly into restoration and management efforts with some success (Brown 2003Bernhardt amp Palmer 2007 Palmer Menninger amp Bernhardt 2010) To balance the needsof people and biodiversity local planning procedures are at times now incorporatinggreen spaces and greening initiatives into urban areas As habitat complexity and diversityare of particular importance in supporting biodiversity and population sustainability it isimportant that habitat structure underpins the engineering of wildlife habitats in urbanand urban-adjacent areas (Threlfall et al 2016) The effectiveness of any managementregime depends on recognising the direct and indirect impacts that occur acrosssustainable ecosystems Consequently habitat complexity as a management objectiverequires that urban landscapes are approached on a case by case basis with full assessmentbefore the habitat is ecologically engineered (Tews et al 2004)


MANAGEMENT TOOLS TO OBSERVE AND ALLEVIATEFEAR AND STRESS FOR WILDLIFE CONSERVATIONCumulative stress maps of human activity and stressors that occur naturally in ecosystemshave allowed returns on restoration investments to be maximized by indicating keyareas that will or do need intervention to mitigate the effects of severe stress on wildlifeas opposed to unsuccessful piecemeal management that focuses on one or two stressorsbroadly (Allan et al 2013) Physiological and behavioural stress in wildlife may becost-effectively and straightforwardly observed by comparing the outcomes ofsimultaneous measurements taken across a disturbance gradient where multiple stressorsare both abundant and low using several well-established methods Specifically assays offaecalurinefurfeather glucocorticoid metabolites can provide insight into the level ofphysiological stress an animal is experiencing under comparative circumstances (Cook2012 Cooke et al 2013 Sheriff et al 2011 Palme 2019) Pairing such results for eachlocation with those of giving-up density surveys (Brown 1988) that can also be filmed byinfrared motion sensor cameras to observe foraging behavioural responses (Leo Reading ampLetnic 2015) yields an understanding of both physiological stress responses andforaging responses Comparing these results may further indicate if behavioural responsesare changing to moderate physiological stress impacts (Carlstead Brown amp Seidensticker1993 Carlstead Brown amp Strawn 1993) Simultaneous measurements of habitatquality that include vegetation cover refuges distance to foodwater source anddistance to disturbances (eg human activity or predator sighting based on spotlightingor in-field camera traps) will build a dataset for spatial correlation analyses that cangeographically map the landscape of fear Such measurements should also identify whatfactors influence the landscape such as by use of behavioural data (Willems amp Hill 2009)andor giving-up density data (Van Der Merwe amp Brown 2008)

Spatial mapping of the physiological stress response based on the collection locations ofsamples could be overlaid and compared to these results also Such spatially mappedresults may clarify important areas that are in need of protection or the habitat types thatcould be extended to mitigate stress impacts It is worth noting that several authorshave emphasized that these methods need to be used correctly to ensure that stress andhabitat factors are linked (eg McMahon et al 2018 Bleicher 2017 Bedoya-Perez et al2013 MacDougall-Shackleton et al 2019) For example collection of fresh faecalsamples of a target species along a gradient of high to low human activity would allowglucocorticoid metabolites to be assayed providing insight into potential stress inducedby human activity along the gradient (Rehnus Wehrle amp Palme 2014) A similar approachcould be used to assay stress perceived by prey species in areas of high and low predatoractivity and sex hormones also could be assayed to explore sex-related effects of stressBy allowing pathways of fear and stress to be mapped including sites where stressorsfrom predators and human activity occur simultaneously such methods should allowmanagers to reliably identify where best to intervene to preserve at-risk populations andmaintain community stability We consider potential interventions in more detail below


If cumulative stressors occur and are suspected to have detrimental effects on targetwildlife populations or communities we suggest that a potentially powerful mitigationapproach could be developed based on Cumulative Effects Assessments (CEA) Devised inthe 1990s amid growing concerns that Environmental Impact Assessments (EIA) did notconsider all the effects of urban and peri-urban developments (Smit amp Spaling 1995)CEAs have been advocated as an effective tool for use by on-ground practitioners (Duinkeret al 2013) Numerous countries have mandated that CEAs be incorporated into EIAsnamely the United States of America Canada Europe New Zealand and Australia eachadvocate some level of CEAs (Therivel amp Ross 2007) Despite this legal requirementand the CEA concept being widely known in scientific literature it is rarely applied inpractice (Ma Becker amp Kilgore 2009 Foley et al 2017)

We propose further that the principles of the lsquoreactive scope modelrsquo be used to developCEAs to identify where cumulative stressors occur and thus better inform conservationmanagement initiatives in areas where wildlife is subject to homeostasis overload orfailure (Fig 2) The results from the above mentioned methods andor other applicableestablished methods may be used to answer our suggested CEA questions The reactivescope model (Romero Dickens amp Cyr 2009) provides useful insight into the range ofphysiological mediators available in response to a stressor It maps the homeostasis rangeof a given species in four stages (1) predictivemdashchange occurs in response to routineenvironmental change such as seasons or day to night (2) reactivemdashchange occurs inresponse to an unpredictable change allowing survival via classic stress responses

Figure 2 A conservation management approach that outlines the key steps for assessing ifcumulative stress impacts are occurring between stressors that occur naturally in ecosystems andthose that are introduced The circled areas indicate where conservation management initiatives maybe used to mitigate these effects through management of vegetation complexity or supplementationmaterials such as water stations or carved lsquotree-hollowrsquo cavities



(3) overloadmdashconsistent changes occur in response to a stressor and chronic stressimpacts start to occur and (4) failuremdashthe species shows inability to sustain homeostasisand is very susceptible to additional stressors and death (Romero Dickens amp Cyr 2009)If our proposed CEA approach (Fig 2) based on the reactive scope model wereapplied to small mammals in urban urban adjacent and peri-urban ecosystems forexample then areas of conservation concern could be identified where the additive orsynergistic impacts of human disturbance and introduced predators combine withstressors that occur naturally Appropriate management such as increasing habitatcomplexity or reducing human activity in conservation areas (Bleicher amp Dickman 2020)could then be implemented to alleviate these stressors

FEAR AND STRESSING IN SMALL MAMMAL ECOLOGYIN AUSTRALIA THE NEED TO CONSIDER THE TWINSTRESSORS OF INTRODUCED PREDATORS AND PEOPLEIN WILDLIFE MANAGEMENTSmall mammals are often somewhat resilient to threatening processes owing to their highpopulation growth rates (Cardillo et al 2005 2006) However in Australia small mammalpopulations are declining quickly and due to causes dissimilar to those driving globaldeclines (Woinarski Burbidge amp Harrison 2015) Declines in Australia have beenattributed to a wide range of habitat stressors habitat loss altered fire regimes diseaseincreasing temperatures decreasing water availability depleted soil quality and salinity(Woinarski Burbidge amp Harrison 2015) However mammals within a lsquocritical weightrangersquo (CWR 35ndash5550 g) are particularly vulnerable (Chisholm amp Taylor 2007Woinarski Burbidge ampHarrison 2015) owing to the effects of predation by two introducedcarnivores the red fox (Vulpes vulpes) and domestic house cat (Felis catus) that arrived inAustralia over 150 years ago (Johnson 2006) If predators are introduced their impactson prey are likely to be exacerbated owing to prey naiumlveteacute (Doherty et al 2016) Suchimpacts have been particularly acute on wildlife in Australia where eutherian carnivoresare recent arrivals (Salo et al 2007) However the question of Australian native animalstress responses and the extent of their naiveteacute to these introduced eutherian predatorsis debatable (Banks amp Dickman 2007 Carthey amp Banks 2016) Although CWR mammalsare of high conservation concern predation from introduced predators poses a threat alsoto all native predators by reducing their food resources which in turn may increasepredation and predation-associated stress on alternative food sources such as smaller(lt35 g) or larger (gt5550 g) mammal species For example a study examining the dietof a nocturnal avian predator the sooty owl (Tyto tenebricosa) before and after red foxintroduction revealed a dietary shift post introduction with owls consuming morearboreal than terrestrial prey species after fox arrival (Bilney Cooke amp White 2006)This shift to consuming arboreal prey increased dietary overlap with the sympatricpowerful owl (Ninox strenua) providing disproportionate predation pressure on prey inthe ecosystems of East Gippsland Victoria

Predation by red foxes and cats is prevalent not only in natural habitats but also inagricultural and urban habitats (Dickman 1996 Morgan et al 2009 Bino et al 2010)


The paths and roads that fragment urban and agricultural habitats are used frequently bythese predators which exacerbates their predation pressure on prey species by combiningwith impacts imposed by human activities (Latham et al 2011 Červinka et al 2013)Consequently this can result in increased abundances of red foxes and cats inhuman-modified landscapes that border or include natural habitats (Towerton et al 2011Graham Maron amp McAlpine 2012) Urban and agricultural habitats present many threatsto wildlife but they may also offer food and shelter opportunities (Pickett et al 2001Gaston et al 2005 Hobbs Higgs amp Harris 2009) As reported by Ives et al (2016)46 percent of threatened Australian animals occur in or near Australian cities Thus thefate of many species could depend on accommodating their needs in urban andagricultural habitats (Ives et al 2016) A recent assessment of data collected at the WildlifeRehabilitation Centre in Queensland Zoo Australia revealed that pet cat or dog attack carstrike and entanglement in human-placed objects represented 564 of the causes ofsubmission of injured wildlife mortality rates associated with these traumas were alsohigh with 613 of admitted animals dying from their injuries (Taylor-Brown et al 2019)These threats may contribute to landscapes of fear through fear arousal altered foragingbehaviour post-traumatic stress reactions and cumulative stress exposures resulting inchronic stress responses

Despite growing knowledge of anthropogenic impacts on threatened species Australianconservation planning continues to exclude urban and agricultural habitats fromconsideration (Dales 2011) There is recognition of the scope of this issue in Australia(Hill Carbery amp Deane 2007 Carthey amp Banks 2012 Threlfall Law amp Banks 2012McCauley Jenkins amp Quintana-Ascencio 2013 Banks amp Smith 2015 Ives et al 2016)but few studies have explored the interactive effects of introduced predators and humanactivity on the survival of prey species Despite the development of glucocorticoid analysistechniques to determine stress in animals dating to the 1960s (Jones et al 1964) onlysix of the 60 extant small mammals of conservation concern in Australia have been subjectto studies seeking to better understand their glucocorticoid response to stressors(Hing et al 2014) such as predation by introduced species or human activity

There is a need for alternative management regimes to mitigate the additional stressorsof human-imposed impacts on wildlife and the situation we have outlined in Australiaunderlines the urgency of this need As there are difficulties with the current control ofintroduced predators in Australia (Glen amp Dickman 2005 Rayner et al 2007 Bergstromet al 2009 Norton 2009Warburton amp Norton 2009 Carroll 2011 Newsome et al 2017)there is also an urgent need for alternative management regimes to mitigate the additionalstressors of introduced predator-imposed impacts As we have argued throughout thisreview it is logical that biodiversity conservation managers consider stress from thecombined impacts of introduced predators altered predator interactions human activityand stressors that occur naturally in ecosystems Using the example methods toconduct our proposed CEA based on the reactive scope model to draft appropriatemanagement plans such as increasing habitat complexity or reducing human interactionin areas would be a progressive response towards preserving many species of Australiansmall mammals and their constituent communities


CONCLUSIONConsidering ongoing global urbanization and the acknowledged importance of urbanareas to biodiversity conservation there is a great need for increased focus on themanagement of urban biodiversity Management decisions require information aboutfear and stress impacts on wildlife including impacts from both human activities andpredators especially if they are novel or introduced Understanding the impacts of humanactivities is a research priority for modern science There are many gaps in our currentunderstanding of fear and stress impacts on wildlife and of associated impacts of alteredpredation pressures and the persistence of target populations To sustain biodiversity inurban and urban-adjacent green space habitats reserves and conservation areas it is vitalthat we establish better understanding and management of the multiple stressors thatoperate in these systems

ADDITIONAL INFORMATION AND DECLARATIONS

FundingThis work was supported by a Holsworth Wildlife Research Endowment The funders hadno role in study design data collection and analysis decision to publish or preparation ofthe manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsHolsworth Wildlife Research Endowment

Competing InterestsThe authors declare that they have no competing interests

Author Contributions Loren L Fardell conceived and designed the experiments performed the experimentsanalyzed the data prepared figures andor tables authored or reviewed drafts of thepaper and approved the final draft

Chris R Pavey conceived and designed the experiments authored or reviewed drafts ofthe paper and approved the final draft

Christopher R Dickman conceived and designed the experiments authored or revieweddrafts of the paper and approved the final draft

Data AvailabilityThe following information was supplied regarding data availability

This is a literature review article and did not generate raw data

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National Park Wildlife Society Bulletin 19(3)339ndash349


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Brown JS Kotler BP 2004Hazardous duty pay and the foraging cost of predation Ecology Letters7(10)999ndash1014 DOI 101111j1461-0248200400661x

Cannon WB 1932 The wisdom of the body New York WW Norton and Company 177ndash201

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Cardillo M Mace GM Gittleman JL Purvis A 2006 Latent extinction risk and the futurebattlegrounds of mammal conservation Proceedings of the National Academy of Sciences of theUnited States of America 103(11)4157ndash4161 DOI 101073pnas0510541103

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Carthey AJ Banks PB 2012 When does an alien become a native species A vulnerable nativemammal recognises and responds to its long-term alien predator PLOS ONE 7(2)e31804DOI 101371journalpone0031804

Carthey AJR Banks PB 2016 Naiveteacute is not forever responses of a vulnerable native rodent to itslong term alien predators Oikos 125(7)918ndash926 DOI 101111oik02723

Carthey AJR Blumstein DT 2018 Predicting predator recognition in a changing world Trends inEcology amp Evolution 33(2)106ndash115 DOI 101016jtree201710009

Červinka J Šaacutelek M Padyšaacutekovaacute E Šmilauer P 2013 The effects of local and landscape-scalehabitat characteristics and prey availability on corridor use by carnivores a comparison of twocontrasting farmlands Journal for Nature Conservation 21(2)105ndash113DOI 101016jjnc201211004

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Ciuti S Northrup JM Muhly TB Simi S Musiani M Pitt JA Boyce MS 2012 Effects of humanson behaviour of wildlife exceed those of natural predators in a landscape of fear PLOS ONE7(11)e50611 DOI 101371journalpone0050611


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Clinchy M Zanette L Boonstra R Wingfield JC Smith JNM 2004 Balancing food and predatorpressure induces chronic stress in songbirds Proceedings of the Royal Society of London Series BBiological Sciences 271(1556)2473ndash2479 DOI 101098rspb20042913

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Clinchy M Zanette LY Roberts D Suraci JP Buesching CD Newman C Macdonald DW2016 Fear of the human super predator far exceeds the fear of large carnivores in a modelmesocarnivore Behavioral Ecology 27(6)1826ndash1832

Cook NJ 2012 Minimally invasive sampling media and the measurement of corticosteroids asbiomarkers of stress in animals Canadian Journal of Animal Science 92(3)227ndash259DOI 104141cjas2012-045

Cooke SJ Sack L Franklin CE Farrell AP Beardall J Wikelski M Chown SL 2013 What isconservation physiology Perspectives on an increasingly integrated and essential scienceConservation Physiology 1(1)cot001 DOI 101093conphyscot001

Cocircteacute IM Darling ES Brown CJ 2016 Interactions among ecosystem stressors and theirimportance in conservation Proceedings of the Royal Society B Biological Sciences283(1824)20152592 DOI 101098rspb20152592

Crain CM Kroeker K Halpern BS 2008 Interactive and cumulative effects of multiple humanstressors in marine systems Ecology Letters 11(12)1304ndash1315DOI 101111j1461-0248200801253x

Cremona T Crowther MS Webb JK 2014 Variation of prey responses to cues from amesopredator and an apex predator Austral Ecology 39(7)749ndash754 DOI 101111aec12138

Crocker DE Khudyakov JI Champagne CD 2016 Oxidative stress in northern elephant sealsIntegration of omics approaches with ecological and experimental studies ComparativeBiochemistry and Physiology Part A Molecular amp Integrative Physiology 20094ndash103DOI 101016jcbpa201602011

Crooks KR Souleacute ME 1999 Mesopredator release and avifaunal extinctions in a fragmentedsystem Nature 400(6744)563ndash566 DOI 10103823028

Dales JT 2011Death by a thousand cuts incorporating cumulative effects in Australiarsquos EnvironmentProtection and Biodiversity Conservation Act Pacific Rim Law amp Policy Journal 20149ndash178

Dantzer B Fletcher QE Boonstra R Sheriff MJ 2014 Measures of physiological stress atransparent or opaque window into the status management and conservation of speciesConservation Physiology 2(1)cou023 DOI 101093conphyscou023

Darimont CT Fox CH Bryan HM Reimchen TE 2015 The unique ecology of human predatorsScience 349(6250)858ndash860 DOI 101126scienceaac4249

Davis M 1992 The role of the amygdala in fear and anxiety Annual Review of Neuroscience15(1)353ndash375 DOI 101146annurevne15030192002033

Davis MWhalen PJ 2001 The amygdala vigilance and emotionMolecular Psychiatry 6(1)13ndash34DOI 101038sjmp4000812

Dhabhar FS McEwen BS 1999 Enhancing versus suppressive effects of stress hormones on skinimmune function Proceedings of the National Academy of Sciences USA 96(3)1059ndash1064DOI 101073pnas9631059


Dickens MJ Romero LM 2013 A consensus endocrine profile for chronically stressed wildanimals does not exist General and Comparative Endocrinology 191177ndash189DOI 101016jygcen201306014

Dickman CR 1996 Impact of exotic generalist predators on the native fauna of AustraliaWildlife Biology 2(1)185ndash195 DOI 102981wlb1996018

Ditchkoff SS Saalfeld ST Gibson CJ 2006 Animal behavior in urban ecosystems modificationsdue to human-induced stress Urban Ecosystems 9(1)5ndash12 DOI 101007s11252-006-3262-3

Doherty TS Dickman CR Nimmo DG Ritchie EG 2015 Multiple threats or multiplying thethreats Interactions between invasive predators and other ecological disturbancesBiological Conservation 19060ndash68 DOI 101016jbiocon201505013

Doherty TS Glen AS Nimmo DG Ritchie EG Dickman CR 2016 Invasive predators and globalbiodiversity loss Proceedings of the National Academy of Sciences USA 113(40)11261ndash11265DOI 101073pnas1602480113

Doherty TS Dickman CR Glen AS Newsome TM Nimmo DG Ritchie EG Vanak ATWirsing AJ 2017 The global impacts of domestic dogs on threatened vertebratesBiological Conservation 21056ndash59 DOI 101016jbiocon201704007

Donihue CM Lambert MR 2015 Adaptive evolution in urban ecosystems AMBIO44(3)194ndash203 DOI 101007s13280-014-0547-2

Duinker PN Burbidge EL Boardley SR Greig LA 2013 Scientific dimensions of cumulativeeffects assessment toward improvements in guidance for practice Environmental Reviews21(1)40ndash52 DOI 101139er-2012-0035

Estes JA Terborgh J Brashares JS Power ME Berger J Bond WJ Carpenter SR Essington TEHolt RD Jackson JBC Marquis RJ Oksanen L Oksanen T Paine RT Pikitch EKRipple WJ Sandin SA Scheffer M Schoener TW Shurin JB Sinclair ARE Souleacute MEVirtanen R Wardle DA 2011 Trophic downgrading of planet Earth Science333(6040)301ndash306 DOI 101126science1205106

Epstein S 1972 The nature of anxiety with emphasis upon its relationship to expectancyIn Spielberger CD ed Anxiety Current Trends in Theory and Research Vol 2 New YorkAcademic Press 291ndash337

Fanselow MS Poulos AM 2005 The neuroscience of mammalian associative learningAnnual Review of Psychology 56(1)207ndash234 DOI 101146annurevpsych56091103070213

Feng S-F Shi T-Y Yang F WangW-N Chen Y-C Tan Q-R 2012 Long-lasting effects of chronicrTMS to treat chronic rodent model of depression Behavioural Brain Research 232(1)245ndash251DOI 101016jbbr201204019

Fischer JD Cleeton SH Lyons TP Miller JR 2012 Urbanization and the predation paradox therole of trophic dynamics in structuring vertebrate communities BioScience 62(9)809ndash818DOI 101525bio20126296

Fleming PA Bateman PW 2018 Novel predation opportunities in anthropogenic landscapesAnimal Behaviour 138145ndash155 DOI 101016janbehav201802011

Fogaca MV Lisboa SF Aguiar DC Moreira FA Gomes FV Casarotto PC Guimaraes FS 2012Fine-tuning of defensive behaviors in the dorsal periaqueductal gray by atypicalneurotransmitters Brazilian Journal of Medical and Biological Research 45(4)357ndash365DOI 101590S0100-879X2012007500029

Foley MM Mease LA Martone RG Prahler EE Morrison TH Murray CC Wojcik D 2017The challenges and opportunities in cumulative effects assessment Environmental ImpactAssessment Review 62122ndash134 DOI 101016jeiar201606008


Freeman NE Norris DR Sutton AO Newman AEM 2020 Raising young with limited resourcessupplementation improves body condition and advances fledging of Canada jays Ecology101(1)e02909 DOI 101002ecy2909

Frid A Dill LM 2002 Human-caused disturbance stimuli as a form of predation riskConservation Ecology 6(1)11 DOI 105751ES-00404-060111

Gaston KJ Warren PH Thompson K Smith RM 2005 Urban domestic gardens (IV) the extentof the resource and its associated features Biodiversity and Conservation 14(14)3327ndash3349DOI 101007s10531-004-9513-9

Gaynor KM Hojnowski CE Carter NH Brashares JS 2018 The influence of human disturbanceon wildlife nocturnality Science 360(6394)1232ndash1235 DOI 101126scienceaar7121

Gaynor KM Brown JS Middleton AD Power ME Brashares JS 2019 Landscapes of fear spatialpatterns of risk perception and response Trends in Ecology amp Evolution 34(4)355ndash368DOI 101016jtree201901004

Geary WL Nimmo DG Doherty TS Ritchie EG Tulloch AI 2019 Threat webs reframing theco-occurrence and interactions of threats to biodiversity Journal of Applied Ecology561992ndash1997

Gil MA Zill J Ponciano JM 2017 Context-dependent landscape of fear algal density elicits riskyherbivory in a coral reef Ecology 98(2)534ndash544 DOI 101002ecy1668

Gill JA Sutherland WJ Watkinson AR 1996 A method to quantify the effects of humandisturbance on animal populations Journal of Applied Ecology 33(4)786ndash792DOI 1023072404948

Glen AS Dickman CR 2005 Complex interactions among mammalian carnivores in Australiaand their implications for wildlife management Biological Reviews 80(3)387ndash401DOI 101017S1464793105006718

Graham CA Maron M McAlpine CA 2012 Influence of landscape structure on invasivepredators feral cats and red foxes in the brigalow landscapes Queensland Australia WildlifeResearch 39(8)661ndash676 DOI 101071WR12008

Griffiths SR Lentini PE Semmens K Watson SJ Lumsden LF Robert KA 2018Chainsaw-carved cavities better mimic the thermal properties of natural tree hollows than nestboxes and log hollows Forests 9(5)235 DOI 103390f9050235

Guiden PW Bartel SL Byer NW Shipley AA Orrock JL 2019 Predatorndashprey interactions in theAnthropocene reconciling multiple aspects of novelty Trends in Ecology amp Evolution34(7)616ndash627 DOI 101016jtree201902017

Gunderson AR Armstrong EJ Stillman JH 2016 Multiple stressors in a changing world theneed for an improved perspective on physiological responses to the dynamic marineenvironment Annual Review of Marine Science 8(1)357ndash378DOI 101146annurev-marine-122414-033953

Hammerschlag N Broderick AC Coker JW Coyne MS Dodd M Frick MG Godfrey MHGodley BJ Griffin DBB Hartog K Murphy SR Murphy TM Nelson ER Williams KLWitt MJ Hawkes LA 2015 Evaluating the landscape of fear between apex predatory sharks andmobile sea turtles across a large dynamic seascape Ecology 96(8)2117ndash2126DOI 10189014-21131

Hawlena D Schmitz OJ 2010 Physiological stress as a fundamental mechanism linking predationto ecosystem functioning American Naturalist 176(5)537ndash556 DOI 101086656495

Hawlena D Strickland MS Bradford MA Schmitz OJ 2012 Fear of predation slows litterdecomposition Science 336(6087)1434ndash1438 DOI 101126science1220097


Hayes RA Nahrung HF Wilson JC 2006 The response of native Australian rodents to predatorodours varies seasonally a by-product of life history variation Animal Behaviour71(6)1307ndash1314 DOI 101016janbehav200508017

Hernandez-Santin L Goldizen AW Fisher DO 2016 Introduced predators and habitat structureinfluence range contraction of an endangered native predator the northern quollBiological Conservation 203160ndash167

Hill NJ Carbery KA Deane EM 2007 Humanndashpossum conflict in urban Sydney Australiapublic perceptions and implications for species management Human Dimensions of Wildlife12(2)101ndash113 DOI 10108010871200701195928

Hing S Narayan E Thompson RCA Godfrey S 2014 A review of factors influencing the stressresponse in Australian marsupials Conservation Physiology 2(1)cou027DOI 101093conphyscou027

Hobbs RJ Higgs E Harris JA 2009 Novel ecosystems implications for conservation andrestoration Trends in Ecology amp Evolution 24(11)599ndash605 DOI 101016jtree200905012

Hofer H East ML 1998 Biological conservation and stress Advances in the Study of Behavior27405ndash525

Hoffman CR Sitvarin MI Rypstra AL 2016 Information from familiar and related conspecificsaffects foraging in a solitary wolf spider Oecologia 181(2)359ndash367DOI 101007s00442-015-3460-x

Holt RD 1984 Spatial heterogeneity indirect interactions and the coexistence of prey speciesAmerican Naturalist 124(3)377ndash406 DOI 101086284280

Honda T Iijima H Tsuboi J Uchida K 2018 A review of urban wildlife management from theanimal personality perspective the case of urban deer Science of the Total Environment644576ndash582 DOI 101016jscitotenv201806335

Hopcraft JGC Sinclair ARE Packer C 2005 Planning for success serengeti lions seek preyaccessibility rather than abundance Journal of Animal Ecology 74(3)559ndash566DOI 101111j1365-2656200500955x

Iossa G Soulsbury CD Baker PJ Harris S 2010 A taxonomic analysis of urban carnivoreecology In Gehrt SD Riley SPD Cypher BL eds Urban Carnivores Ecology Conflict andConservation Baltimore Johns Hopkins University Press 173ndash180

Iribarren C Kotler BP 2012 Foraging patterns of habitat use reveal landscape of fear of Nubianibex Capra nubiana Wildlife Biology 18(2)194ndash202 DOI 10298111-041

Ives CD Lentini PE Threlfall CG Ikin K Shanahan DF Garrard GE Bekessy SA Fuller RAMumaw L Rayner L Rowe R Valentine LE Kendal D 2016 Cities are hotspots forthreatened species Global Ecology and Biogeography 25(1)117ndash126 DOI 101111geb12404

Jaatinen K Seltmann MW Oumlst M 2014 Context-dependent stress responses and theirconnections to fitness in a landscape of fear Journal of Zoology 294(3)147ndash153DOI 101111jzo12169

Jackson MC Loewen CJG Vinebrooke RD Chimimba CT 2016Net effects of multiple stressorsin freshwater ecosystems a meta-analysis Global Change Biology 22(1)180ndash189DOI 101111gcb13028

Johnson MD Sherry TW 2001 Effects of food availability on the distribution of migratorywarblers among habitats in Jamaica Journal of Animal Ecology 70(4)546ndash560DOI 101046j1365-2656200100522x

Johnson C 2006 Australiarsquos mammal extinctions a 50000-year history Cambridge CambridgeUniversity Press


Johnstone CP Lill A Reina RD 2012 Does habitat fragmentation cause stress in the agileantechinus A haematological approach Journal of Comparative Physiology B 182(1)139ndash155DOI 101007s00360-011-0598-7

Jokimaumlki J Kaisanlahti-Jokimaumlki ML Suhonen J Clergeau P Pautasso M Fernaacutendez-Juricic E2011 Merging wildlife community ecology with animal behavioral ecology for a betterurban landscape planning Landscape and Urban Planning 100(4)383ndash385DOI 101016jlandurbplan201102001

Jones IC Vinson GP Jarrett IG Sharman GB 1964 Steroid components in the adrenal venousblood of Trichosurus vulpecula (Kerr) Journal of Endocrinology 30(1)149ndash150DOI 101677joe00300149

Jones ME Apfelbach R Banks PB Cameron EZ Dickman CR Frank A McLean SMcGregor IS Muumlller-Schwarze D Parsons MH Sparrow E Blumstein DT 2016 A nose fordeath integrating trophic and informational networks for conservation and managementFrontiers in Ecology and Evolution 4124 DOI 103389fevo201600124

Kauffman MJ Brodie JF Jules ES 2010 Are wolves saving Yellowstonersquos aspen Alandscape-level test of a behaviorally mediated trophic cascade Ecology 91(9)2742ndash2755DOI 10189009-19491

King JM Bradshaw SD 2010 Stress in an island kangaroo The Barrow Island euro Macropusrobustus isabellinus General and Comparative Endocrinology 167(1)60ndash67DOI 101016jygcen201002018

Klecka J Boukal DS 2014 The effect of habitat structure on prey mortality dependson predator and prey microhabitat use Oecologia 176(1)183ndash191DOI 101007s00442-014-3007-6

Kloppers EL St Clair CC Hurd TE 2005 Predator-resembling aversive conditioning formanaging habituated wildlife Ecology and Society 10(1)31 DOI 105751ES-01293-100131

Knutie SA 2020 Food supplementation affects gut microbiota and immunological resistance toparasites in a wild bird species bioRxiv DOI 1011111365-266413567

Kohl MT Stahler DR Metz MC Forester JD Kauffman MJ Varley N White PJ Smith DWMacNulty DR 2018 Diel predator activity drives a dynamic landscape of fear EcologicalMonographs 88(4)638ndash652 DOI 101002ecm1313

Kotler BP Brown JS 1988 Environmental heterogeneity and the coexistence of desert rodentsAnnual Review of Ecology and Systematics 19(1)281ndash307DOI 101146annureves19110188001433

Kuijper DP Bubnicki JW Churski M Mols B Van Hooft P 2015 Context dependence of riskeffects wolves and tree logs create patches of fear in an old-growth forest Behavioral Ecology26(6)1558ndash1568 DOI 101093behecoarv107

Labar KS Ledoux JE 2011 Coping with danger the neural basis of defensive behavior and fearfulfeelings Comprehensive Physiology 8139ndash154

Latham ADM Latham MC Boyce MS Boutin S 2011 Movement responses by wolves toindustrial linear features and their effect on woodland caribou in northeastern AlbertaEcological Applications 21(8)2854ndash2865 DOI 10189011-06661

Laundreacute JW Hernaacutendez L Altendorf KB 2001 Wolves elk and bison reestablishing theldquolandscape of fearrdquo in Yellowstone National Park USA Canadian Journal of Zoology79(8)1401ndash1409 DOI 101139z01-094

Laundreacute JW Hernaacutendez L Ripple WJ 2010 The landscape of fear ecological implications ofbeing afraid Open Ecology Journal 31ndash7


Laundreacute JW Hernaacutendez L Medina PL Campanella A Loacutepez-Portillo J Gonzaacutelez-Romero AGrajales-TamKM Burke AM Gronemeyer P Browning DM 2014 The landscape of fear themissing link to understand top-down and bottom-up controls of prey abundance Ecology95(5)1141ndash1152 DOI 10189013-10831

Laws AN 2017 Climate change effects on predatorndashprey interactions Current Opinion in InsectScience 2328ndash34 DOI 101016jcois201706010

Leahy L Legge SM Tuft K McGregor HW Barmuta LA Jones ME Johnson CN 2016Amplified predation after fire suppresses rodent populations in Australiarsquos tropical savannasWildlife Research 42(8)705ndash716 DOI 101071WR15011

LeDoux JE 1996 The emotional brain New York Simon and Schuster

LeDoux JE 2003 The emotional brain fear and the amygdala Cellular and MolecularNeurobiology 23(45)727ndash738 DOI 101023A1025048802629

Legge S Smith JG James A Tuft KD Webb T Woinarski JC 2019 Interactions among threatsaffect conservation management outcomes Livestock grazing removes the benefits of firemanagement for small mammals in Australian tropical savannas Conservation Science andPractice 1(7)e52 DOI 101111csp252

Leighton PA Horrocks JA Kramer DL 2010 Conservation and the scarecrow effect can humanactivity benefit threatened species by displacing predators Biological Conservation143(9)2156ndash2163 DOI 101016jbiocon201005028

Leo V Reading RP Letnic M 2015 Interference competition odours of an apex predator andconspecifics influence resource acquisition by red foxes Oecologia 179(4)1033ndash1040DOI 101007s00442-015-3423-2

Lima SL Dill LM 1990 Behavioral decisions made under the risk of predation a review andprospectus Canadian Journal of Zoology 68(4)619ndash640 DOI 101139z90-092

Lima SL 1998 Stress and decision making under the risk of predation recent developments frombehavioral reproductive and ecological perspectives Advances in the Study of Behavior27215ndash290

Lima SL Bednekoff PA 1999 Temporal variation in danger drives antipredator behavior thepredation risk allocation hypothesis American Naturalist 153(6)649ndash659 DOI 101086303202

Lone K Loe LE Gobakken T Linnell JD Odden J Remmen J Mysterud A 2014 Living anddying in a multi-predator landscape of fear roe deer are squeezed by contrasting pattern ofpredation risk imposed by lynx and humans Oikos 123(6)641ndash651DOI 101111j1600-0706201300938x

Lowry H Lill A Wong BBM 2013 Behavioural responses of wildlife to urban environmentsBiological Reviews 88(3)537ndash549 DOI 101111brv12012

Lyons J Mastromonaco G Edwards DB Schulte-Hostedde AI 2017 Fat and happy in the cityEastern chipmunks in urban environments Behavioral Ecology 28(6)1464ndash1471DOI 101093behecoarx109

Ma Z Becker DR Kilgore MA 2009 Assessing cumulative impacts within state environmentalreview frameworks in the United States Environmental Impact Assessment Review29(6)390ndash398 DOI 101016jeiar200903004

MacDougall-Shackleton SA Bonier F Romero LM Moore IT 2019 Glucocorticoids andldquostressrdquo are not synonymous Integrative Organismal Biology 1(1)obz017DOI 101093iobobz017

Madsen B Carroll N Moore Brands K 2010 State of biodiversity markets report offset andcompensation programs worldwide Available at httpwwwecosystemmarketplacecomdocumentsacrobatsbdmrpdf


Malcolm KD McShea WJ Garshelis DL Luo SJ Van Deelen TR Liu F Li S Miao L Wang DBrown JL 2014 Increased stress in Asiatic black bears relates to food limitation crop raidingand foraging beyond nature reserve boundaries in China Global Ecology and Conservation2267ndash276 DOI 101016jgecco201409010

Manuck SB Kaplan JR Adams MR Clarkson TB 1988 Studies of psychosocial influences oncoronary artery atherogenesis in cynomolgus monkeys Health Psychology 7(2)113ndash124DOI 1010370278-613372113

Maren S 2001 Neurobiology of Pavlovian fear conditioning Annual Review of Neuroscience24(1)897ndash931 DOI 101146annurevneuro241897

Mason JW 1971 A re-evaluation of the concept of lsquonon-specificityrsquo in stress theoryJournal of Psychiatric Research 8(3ndash4)323ndash333 DOI 1010160022-3956(71)90028-8

McCauley LA Jenkins DG Quintana-Ascencio PF 2013 Isolated wetland loss and degredationover two decades in an increasingly urbanised landscape Wetlands 33(1)117ndash127DOI 101007s13157-012-0357-x

McClennen NAWigglesworth RR Anderson SHWachob DG 2001 The effect of suburban andagricultural development on the activity patterns of coyotes (Canis latrans) American MidlandNaturalist 146(1)27ndash37 DOI 1016740003-0031(2001)146[0027TEOSAA]20CO2

McComb LB Lentini PE Harley DK Lumsden LF Antrobus JS Eyre AC Briscoe NJ 2019Feral cat predation on Leadbeaterrsquos possum (Gymnobelideus leadbeateri) and observationsof arboreal hunting at nest boxes Australian Mammalogy 41(2)262ndash265DOI 101071AM18010

McDonnell MJ Hahs AK 2015 Adaptation and adaptedness of organisms to urbanenvironments Annual Review of Ecology Evolution and Systematics 46(1)261ndash280DOI 101146annurev-ecolsys-112414-054258

McEwen BS Stellar E 1993 Stress and the individual mechanisms leading to disease Archives ofInternal Medicine 153(18)2093ndash2101 DOI 101001archinte199300410180039004

McEwen BS Wingfield JC 2003 The concept of allostasis in biology and biomedicine Hormonesand Behavior 43(1)2ndash15 DOI 101016S0018-506X(02)00024-7

McEwen BS 2004 Protection and damage from acute and chronic stress allostasis and allostaticoverload and relevance to the pathophysiology of psychiatric disorders Annals of the New YorkAcademy of Sciences 1032(1)1ndash7 DOI 101196annals1314001

McKinney ML 2006 Urbanization as a major cause of biotic homogenizationBiological Conservation 127(3)247ndash260 DOI 101016jbiocon200509005

McMahon JD Lashley MA Brooks CP Barton BT 2018 Covariance between predation risk andnutritional preferences confounds interpretations of giving-up density experiments Ecology99(7)1517ndash1522 DOI 101002ecy2365

Mella VSA Banks PB McArthur C 2014 Negotiating multiple cues of predation risk in alandscape of fear what scares free-ranging brushtail possums Journal of Zoology 294(1)22ndash30DOI 101111jzo12146

Mineka S 1979 The role of fear in theories of avoidance learning flooding and extinctionPsychological Bulletin 86(5)985ndash1010 DOI 1010370033-2909865985

Mineur YS Belzung C Crusio WE 2006 Effects of unpredictable chronic mild stress on anxietyand depression-like behavior in mice Behavioural Brain Research 175(1)43ndash50DOI 101016jbbr200607029

Moslashller AP 2009 Successful city dwellers a comparative study of the ecological characteristicsof urban birds in the Western Palearctic Oecologia 159(4)849ndash858DOI 101007s00442-008-1259-8


Morgan SA Hansen CM Ross JG Hickling GJ Ogilvie SC Paterson AM 2009 Urban cat (Feliscatus) movement and predation activity associated with a wetland reserve in New ZealandWildlife Research 36(7)574ndash580 DOI 101071WR09023

Murray MH Becker DJ Hall RJ Herandez SM 2016 Wildlife health and supplemental feedinga review and management recommendations Biological Conservation 204163ndash174DOI 101016jbiocon201610034

Navara KJ Nelson RJ 2007 The dark side of light at night physiological epidemiological andecological consequences Journal of Pineal Research 43(3)215ndash224DOI 101111j1600-079X200700473x

Newsome TM Ballard GA Fleming PJ Van de Ven R Story GL Dickman CR 2014 Human-resource subsidies alter the dietary preferences of a mammalian top predator Oecologia175(1)139ndash150 DOI 101007s00442-014-2889-7

Newsome TM Dellinger JA Pavey CR Ripple WJ Shores CR Wirsing AJ Dickman CR 2015The ecological effects of providing resource subsidies to predators Global Ecology andBiogeography 24(1)1ndash11 DOI 101111geb12236

Newsome T Van Eeden L Lazenby B Dickman C 2017Does culling work Australasian Science38(1)28ndash30

Nersesian CL Banks PB McArthur C 2012 Behavioural responses to indirect and directpredator cues by a mammalian herbivore the common brushtail possum Behavioral Ecologyand Sociobiology 66(1)47ndash55 DOI 101007s00265-011-1250-y

Norton DA 2009 Species invasions and the limits to restoration learning from the New Zealandexperience Science 325(5940)569ndash571 DOI 101126science1172978

Oumlhman A 2000 Fear In Fink G ed Encyclopedia of Stress Vol 2 111ndash116

Otto SP 2018Adaptation speciation and extinction in the Anthropocene Proceedings of the RoyalSociety B Biological Sciences 285(1891)20182047 DOI 101098rspb20182047

Palme R 2019 Non-invasive measurement of glucocorticoids advances and problemsPhysiology amp Behaviour 199229ndash243 DOI 101016jphysbeh201811021

Palmer MA Menninger HL Bernhardt E 2010 River restoration habitat heterogeneity andbiodiversity a failure of theory or practice Freshwater Biology 55205ndash222DOI 101111j1365-2427200902372x

Parsons MH Blumstein DT 2010 Familiarity breeds contempt kangaroos persistently avoidareas with experimentally deployed dingo scents PLOS ONE 5(5)5e10403

Parsons MH Apfelbach R Banks PB Cameron EZ Dickman CR Frank AS Jones MEMcGregor IS McLean S Muumlller-Schwarze D Sparrow EE Blumstein DT 2017 Biologicallymeaningful scents a framework for understanding predatorndashprey research across disciplinesBiological Reviews 93(1)98ndash114 DOI 101111brv12334

Parris KM 2016 Ecology of urban environments New Jersey John Wiley and Sons

Patten MA Burger JC 2018 Reserves as double-edged sword avoidance behavior in anurban-adjacent wildland Biological Conservation 218233ndash239 DOI 101016jbiocon201712033

Pianka ER 2011 Evolutionary ecology Siskiyou County Eric R Pianka

Pickett ST Cadenasso ML Grove JM Nilon CH Pouyat RV Zipperer WC Costanza R 2001Urban ecological systems linking terrestrial ecological physical and socioeconomiccomponents of metropolitan areas Annual Review of Ecology and Systematics 32(1)127ndash157DOI 101146annurevecolsys32081501114012

Pitkanen A 2000 Connectivity of the rat amygdaloid complex The amygdala a functional analysisOxford Oxford University Press 31ndash115


Polis GA Barnes JD Seely MK Henschel JR Enders MM 1998 Predation as a major cost ofreproduction in Namib Desert tenebrionid beetles Ecology 79(7)2560ndash2566DOI 1018900012-9658(1998)079[2560PAAMCO]20CO2

Price CJ Banks PB 2018 Habitat augmentation for introduced urban wildlife the use of piles ofrailway sleepers as refuge for introduced black rats Rattus rattus Australian Zoologist39(3)513ndash519 DOI 107882AZ2017029

Prugh LR Stoner CJ Epps CW BeanWT Ripple WJ Laliberte AS Brashares JS 2009 The riseof the mesopredator BioScience 59(9)779ndash791 DOI 101525bio20095999

Rayner MJ Hauber ME Imber MJ Stamp RK Clout MN 2007 Spatial heterogeneity ofmesopredator release within an oceanic island system Proceedings of the National Academy ofSciences USA 104(52)20862ndash20865 DOI 101073pnas0707414105

Rehnus M Wehrle M Palme R 2014 Mountain hares Lepus timidus and tourism stress eventsand reactions Journal of Applied Ecology 51(1)6ndash12 DOI 1011111365-266412174

Rescorla RA Solomon RL 1967 Two-process learning theory relationships between Pavlovianconditioning and instrumental learning Psychological Review 74(3)151ndash182DOI 101037h0024475

Rieucau G Vickery WL Doucet GJ 2009 A patch use model to separate effects of foraging costson giving-up densities an experiment with white-tailed deer (Odocoileus virginianus)Behavioral Ecology and Sociobiology 63(6)891ndash897 DOI 101007s00265-009-0732-7

Riley SP Sauvajot RM Fuller TK York EC Kamradt DA Bromley C Wayne RK 2003 Effectsof urbanization and habitat fragmentation on bobcats and coyotes in southern CaliforniaConservation Biology 17(2)566ndash576 DOI 101046j1523-1739200301458x

Riley S Brown J Sikich J Schoonmaker C Boydston E 2014Wildlife friendly roads the impactsof roads on wildlife in urban areas and potential remedies In McCleery R Moorman CPeterson M eds Urban Wildlife Conservation Boston Springer 323ndash360

Ripple WJ Estes JA Beschta RL Wilmers CC Ritchie EG Hebblewhite M Berger JElmhagen B Letnic M Nelson MP Schmitz OJ Smith DW Wallach AD Wirsing AJ 2014Status and ecological effects of the worldrsquos largest carnivores Science 343(6167)1241484DOI 101126science1241484

Ritchie EG Johnson CN 2009 Predator interactions mesopredator release and biodiversityconservation Ecology Letters 12(9)982ndash998 DOI 101111j1461-0248200901347x

Rodriacuteguez A Andreacuten H Jansson G 2001 Habitat-mediated predation risk and decisionmaking of small birds at forest edges Oikos 95(3)383ndash396DOI 101034j1600-07062001950303x

Rodrigues SM LeDoux JE Sapolsky RM 2009 The influence of stress hormones on fear circuitryAnnual Review of Neuroscience 32(1)289ndash313 DOI 101146annurevneuro051508135620

Rodriguez A Hausberger M Clergeau P 2010 Flexibility in European starlingsrsquo use of socialinformation experiments with decoys in different populations Animal Behaviour80(6)965ndash973 DOI 101016janbehav201008010

Romero LM 2004 Physiological stress in ecology lessons from biomedical research Trends inEcology amp Evolution 19(5)249ndash255 DOI 101016jtree200403008

Romero LM Dickens MJ Cyr NE 2009 The reactive scope modelmdasha new model integratinghomeostasis allostasis and stress Hormones and Behavior 55(3)375ndash389DOI 101016jyhbeh200812009

Roozendaal B 2000 Glucocorticoids and the regulation of memory consolidationPsychoneuroendocrinology 25(3)213ndash238 DOI 101016S0306-4530(99)00058-X


Rosen JB Schulkin J 1998 From normal fear to pathological anxiety Psychological Review105(2)325ndash350 DOI 1010370033-295X1052325

Rosen JB 2004 The neurobiology of conditioned and unconditioned fear a neurobehavioralsystem analysis of the amygdala Behavioral and Cognitive Neuroscience Reviews 3(1)23ndash41DOI 1011771534582304265945

Rosen JB Schulkin J 2004 Adaptive fear allostasis and the pathology of anxiety anddepression In Schulkin J ed Allostasis Homeostasis and the Costs of Physiological Adaptation164ndash227

Santini L Gonzaacutelez-Suaacuterez M Russo D Gonzalez-Voyer A Von Hardenberg A Ancillotto L2019 One strategy does not fit all determinants of urban adaptation in mammals EcologyLetters 22(2)365ndash376 DOI 101111ele13199

Santos X Mateos E Bros V Brotons L De Mas E Herraiz JA Herrando S Miňo AgraveOlmo-Vidal JM Quesada J Ribes J Sabateacute S Sauras-Yera T Serra A Vallejo VR Viňolas A2014 Is response to fire influenced by dietary specialization and mobility A comparativestudy with multiple animal assemblages PLOS ONE 9(2)e88224DOI 101371journalpone0088224

Salo P Korpimaumlki E Banks PB Nordstroumlm M Dickman CR 2007 Alien predators are moredangerous than native predators to prey populations Proceedings of the Royal Society BBiological Sciences 274(1615)1237ndash1243 DOI 101098rspb20060444

Sapolsky RM Romero LM Munck AU 2000 How do glucocorticoids influence stress responsesIntegrating permissive suppressive stimulatory and preparative actions Endocrine Reviews21(1)55ndash89

Say-Sallaz E Chamailleacute-Jammes S Fritz H Valeix M 2019 Non-consumptive effects ofpredation in large terrestrial mammals Mapping our knowledge and revealing the tip of theiceberg Biological Conservation 23536ndash52 DOI 101016jbiocon201903044

Schell CJ Young JK Lonsdorf EV Santymire RM Mateo JM 2018 Parental habituation tohuman disturbance over time reduces fear of humans in coyote offspring Ecology and Evolution8(24)12965ndash12980

Schmidt K Kuijper DPJ 2015 A ldquodeath traprdquo in the landscape of fear Mammal Research60(4)275ndash284 DOI 101007s13364-015-0229-x

Schmitz OJ Beckerman AP OrsquoBrien KM 1997 Behaviorally mediated trophic cascades effects ofpredation risk on food web interactions Ecology 78(5)1388ndash1399DOI 1018900012-9658(1997)078[1388BMTCEO]20CO2

Schmitz OJ Krivan V Ovadia O 2004 Trophic cascades the primacy of trait-mediated indirectinteractions Ecology Letters 7(2)153ndash163 DOI 101111j1461-0248200300560x

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Smith JA Suraci JP Clinchy M Crawford A Roberts D Zanette LY Wilmers CC 2017 Fear ofthe human lsquosuper predatorrsquo reduces feeding time in large carnivores Proceedings of the RoyalSociety B Biological Sciences 284(1857)20170433 DOI 101098rspb20170433

Smith JA Donadio E Pauli JN Sheriff MJ Middleton AD 2019 Integrating temporal refugiainto landscapes of fear prey exploit predator downtimes to forage in risky places Oecologia189(4)883ndash890 DOI 101007s00442-019-04381-5

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Suraci JP Clinchy M Zanette LY Wilmers CC 2019 Fear of humans as apex predators haslandscape-scale impacts from mountain lions to mice Ecology Letters 22(10)1578ndash1586DOI 101111ele13344

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Fear and stressing in predator--prey ecology considering the twin stressors of predators and people on mammals

Introduction

Review method

Mammalian physiological responses to fear and stress

Mammalian behavioural responses to fear and stress the landscape of fear concept

Human activity as a fear-inducing stressor

Alleviating fear and stress for wildlife conservation

Managing habitat to alleviate wildlife fear and stress

Management tools to observe and alleviate fear and stress for wildlife conservation

Fear and stressing in small mammal ecology in Australia the need to consider the twin stressors of introduced predators and people in wildlife management

Conclusion

References

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50 and later) gtgt Namespace [ (Adobe) (Common) (10) ] OtherNamespaces [ ltlt AsReaderSpreads false CropImagesToFrames true ErrorControl WarnAndContinue FlattenerIgnoreSpreadOverrides false IncludeGuidesGrids false IncludeNonPrinting false IncludeSlug false Namespace [ (Adobe) (InDesign) (40) ] OmitPlacedBitmaps false OmitPlacedEPS false OmitPlacedPDF false SimulateOverprint Legacy gtgt ltlt AddBleedMarks false AddColorBars false AddCropMarks false AddPageInfo false AddRegMarks false ConvertColors NoConversion DestinationProfileName () DestinationProfileSelector NA Downsample16BitImages true FlattenerPreset ltlt PresetSelector MediumResolution gtgt FormElements false GenerateStructure true IncludeBookmarks false IncludeHyperlinks false IncludeInteractive false IncludeLayers false IncludeProfiles true MultimediaHandling UseObjectSettings Namespace [ (Adobe) (CreativeSuite) (20) ] PDFXOutputIntentProfileSelector NA PreserveEditing true UntaggedCMYKHandling LeaveUntagged UntaggedRGBHandling LeaveUntagged UseDocumentBleed false gtgt ]gtgt setdistillerparamsltlt HWResolution [2400 2400] PageSize [612000 792000]gtgt setpagedevice

and the way they interact with the environment (Brown amp Kotler 2004 Clinchy et al 2004Romero 2004) For example the fear response of an individual of a prey species to apredator may be to change the locations or times in which they forage which can havepositive impacts on the structure of the environment (Laundreacute Hernaacutendez amp Ripple2010) Such fear responses can in turn influence ecosystem function (Schmitz Krivan ampOvadia 2004 Schmitz Beckerman amp OrsquoBrien 1997 Hawlena et al 2012) These effectsarise due to the lsquolandscape of fearrsquo that prey individuals perceivemdashthat is the spatialdistribution of perceived predation risk that influences prey movement and behaviour asprey individuals attempt to mitigate risk and obtain essential resources (LaundreacuteHernaacutendez amp Altendorf 2001 Laundreacute Hernaacutendez amp Ripple 2010)

Recent studies suggest that the effects of predators are being altered and oftenamplified by human activities For example the demise of top predators in many parts ofthe world has lsquoreleasedrsquo populations of smaller predators or mesopredators that have sincebecome overabundant and now exert strong pressure on smaller species (Prugh et al2009) Predators that have been introduced to new areas also exert much stronger pressureon prey populations than do native predators (Salo et al 2007) Climate change andassociated shifts in primary productivity can also have bottom-up impacts onpredatorndashprey interactions (Laws 2017) Such novel alterations to predatorndashpreydynamics can depress prey populations and disrupt community structure and as suchrequire novel approaches to recognize and manage their effects (Carthey amp Blumstein2018 Fleming amp Bateman 2018 Guiden et al 2019)

Altered predatorndashprey interactions may contribute to declines in biodiversity but aprimary cause of biodiversity loss is the rapid global increase in human populationsdriving agricultural industrial and urban expansions that change or destroy naturalhabitats (Madsen Carroll amp Moore Brands 2010) Such expansions are resulting in novelhumanndashwildlife interactions and secondary impacts that arise from human activities inclose proximity to natural environments and thus increasingly are becoming an additionalstressor that influences ecosystem function Pressures exerted both directly and indirectlyby human activities have been likened to the pressures exerted by the presence of atop predator on prey (Frid amp Dill 2002 Rehnus Wehrle amp Palme 2014 Patten amp Burger2018) Natural predation pressures coupled with human-imposed predation-like pressuresandor additional exogenous stressors such as pollution arising from anthropogenicactivities are likely to negatively affect prey species by increasing their levels or frequencyof stress Current research is developing a more nuanced understanding of the effectsof human activity and predator presence on the stress of prey (Arlettaz et al 2015Jaatinen Seltmann amp Oumlst 2014 respectively) However few studies in terrestrialecosystems have considered both of these pressures simultaneously or have linkedbehavioural responses with endocrinological evidence of stress In one instructive recentstudy human activity was shown to be positively correlated with physiological stress inungulates whilst in areas occupied by large predators stress was found to be lower and lessvariable (Zbyryt et al 2017)

Conservation management and associated scientific research is often viewed from theperspective of a single discipline However ecological changes arising from anthropogenic













































































































































































































































































































































































Introduction

Review method








Conclusion

References

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PDFXCompliantPDFOnly false PDFXNoTrimBoxError true PDFXTrimBoxToMediaBoxOffset [ 000000 000000 000000 000000 ] PDFXSetBleedBoxToMediaBox true PDFXBleedBoxToTrimBoxOffset [ 000000 000000 000000 000000 ] PDFXOutputIntentProfile (None) PDFXOutputConditionIdentifier () PDFXOutputCondition () PDFXRegistryName () PDFXTrapped False CreateJDFFile false Description ltlt CHS ltFEFF4f7f75288fd94e9b8bbe5b9a521b5efa7684002000500044004600206587686353ef901a8fc7684c976262535370673a548c002000700072006f006f00660065007200208fdb884c9ad88d2891cf62535370300260a853ef4ee54f7f75280020004100630072006f0062006100740020548c002000410064006f00620065002000520065006100640065007200200035002e003000204ee553ca66f49ad87248672c676562535f00521b5efa768400200050004400460020658768633002gt CHT ltFEFF4f7f752890194e9b8a2d7f6e5efa7acb7684002000410064006f006200650020005000440046002065874ef653ef5728684c9762537088686a5f548c002000700072006f006f00660065007200204e0a73725f979ad854c18cea7684521753706548679c300260a853ef4ee54f7f75280020004100630072006f0062006100740020548c002000410064006f00620065002000520065006100640065007200200035002e003000204ee553ca66f49ad87248672c4f86958b555f5df25efa7acb76840020005000440046002065874ef63002gt DAN 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 DEU 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 ESP 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 FRA ltFEFF005500740069006c006900730065007a00200063006500730020006f007000740069006f006e00730020006100660069006e00200064006500200063007200e900650072002000640065007300200064006f00630075006d0065006e00740073002000410064006f00620065002000500044004600200070006f007500720020006400650073002000e90070007200650075007600650073002000650074002000640065007300200069006d007000720065007300730069006f006e00730020006400650020006800610075007400650020007100750061006c0069007400e90020007300750072002000640065007300200069006d007000720069006d0061006e0074006500730020006400650020006200750072006500610075002e0020004c0065007300200064006f00630075006d0065006e00740073002000500044004600200063007200e900e90073002000700065007500760065006e0074002000ea0074007200650020006f007500760065007200740073002000640061006e00730020004100630072006f006200610074002c002000610069006e00730069002000710075002700410064006f00620065002000520065006100640065007200200035002e0030002000650074002000760065007200730069006f006e007300200075006c007400e90072006900650075007200650073002egt ITA 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 JPN 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 KOR ltFEFFc7740020c124c815c7440020c0acc6a9d558c5ec0020b370c2a4d06cd0d10020d504b9b0d1300020bc0f0020ad50c815ae30c5d0c11c0020ace0d488c9c8b85c0020c778c1c4d560002000410064006f0062006500200050004400460020bb38c11cb97c0020c791c131d569b2c8b2e4002e0020c774b807ac8c0020c791c131b41c00200050004400460020bb38c11cb2940020004100630072006f0062006100740020bc0f002000410064006f00620065002000520065006100640065007200200035002e00300020c774c0c1c5d0c11c0020c5f40020c2180020c788c2b5b2c8b2e4002egt NLD (Gebruik deze instellingen om Adobe PDF-documenten te maken voor kwaliteitsafdrukken op desktopprinters en proofers De gemaakte PDF-documenten kunnen worden geopend met Acrobat en Adobe Reader 50 en hoger) NOR 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 SUO 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 SVE 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 ENU (Use these settings to create Adobe PDF documents for quality printing on desktop printers and proofers Created PDF documents can be opened with Acrobat and Adobe Reader 50 and later) gtgt Namespace [ (Adobe) (Common) (10) ] OtherNamespaces [ ltlt AsReaderSpreads false CropImagesToFrames true ErrorControl WarnAndContinue FlattenerIgnoreSpreadOverrides false IncludeGuidesGrids false IncludeNonPrinting false IncludeSlug false Namespace [ (Adobe) (InDesign) (40) ] OmitPlacedBitmaps false OmitPlacedEPS false OmitPlacedPDF false SimulateOverprint Legacy gtgt ltlt AddBleedMarks false AddColorBars false AddCropMarks false AddPageInfo false AddRegMarks false ConvertColors NoConversion DestinationProfileName () DestinationProfileSelector NA Downsample16BitImages true FlattenerPreset ltlt PresetSelector MediumResolution gtgt FormElements false GenerateStructure true IncludeBookmarks false IncludeHyperlinks false IncludeInteractive false IncludeLayers false IncludeProfiles true MultimediaHandling UseObjectSettings Namespace [ (Adobe) (CreativeSuite) (20) ] PDFXOutputIntentProfileSelector NA PreserveEditing true UntaggedCMYKHandling LeaveUntagged UntaggedRGBHandling LeaveUntagged UseDocumentBleed false gtgt ]gtgt setdistillerparamsltlt HWResolution [2400 2400] PageSize [612000 792000]gtgt setpagedevice












































































































































































































































































































































































Introduction

Review method








Conclusion

References


fear and stressing in predator--prey ecology: considering ... · fear and stressing in...

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