how nature-based tourism might increase prey vulnerability to predators

8202019 How Nature-Based Tourism Might Increase Prey Vulnerability to Predators

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Review

How Nature-Based TourismMight Increase Prey

Vulnerability to PredatorsBenjamin Geffroy12 Diogo SM Samia3 Eduardo Bessa45

and Daniel T Blumstein6

Tourism can be deleterious for wildlife because it triggers behavioral changes in

individuals with cascading effects on populations and communities Among

these behavioral changes animals around humans often reduce their fearful-ness and antipredator responses towards humans A straightforward prediction

is that habituation to humans associated with tourism would negatively in1047298u-

ence reaction to predators This could happen indirectly where human pres-

ence decreases the number of natural predators and thus prey become less

wary or directly where human-habituated individuals become bolder and thus

more vulnerable to predation Building on ideas from the study of traits associ-

ated with domestication and urbanization we develop a framework to under-

stand how behavioral changes associated with nature-based tourism can

impact individual 1047297tness and thus the demographic trajectory of a population

How Might Nature-Based Tourism In1047298uence Wildlife Behavior

Nature-based tourism (see Glossary) and ecotourism have both become very popularleisure activities that constitute a business worth millions of dollars annually [1] Terrestrialprotected areas around the world receive approximately 8 billion visitors per year [2] a numberthat is greater than each human on earth visiting a protected area once a year Marine and inlandwaters also attract millions of tourists annually [3] More invasive wildlife tourism such as that inwhich visitors closely observe or swim with marine mammals increased 30 between 1998 and2008 involving 13 million people annually [4] Inland waters also attract tourists with forinstance 242 000 people that in 2012 swam along a riverine trail in Bonito (Center-WestBrazil) to observe 1047297shi

However these interactions between wildlife and humans even when the welfare of animals isconsidered often change the behavior of wild animals For example it is well documented that

individuals of many species that have benign interactions with humans undergo habituation-like processes leading to some degree of human tolerance [56] Nonetheless althoughfrequent tolerance is not a necessary outcome and the development of tolerance is in1047298uencedby various factors (Box 1)

Reserve managers or ecotourist providers may explicitly habituate animals so as to ensure clientsatisfaction For instance Ugandan park rangers habituated chimpanzees through daily visits inKibale National Park so as to improve the quality of chimpanzee-watching ecotourists [7]

Food provisioning by tourist operators and guides has also led to documented changes inbehavior For instance previous studies have shown that individuals learn to anticipate feeding

TrendsNature-based tourism has become a

very popular leisure activity in the pastyears and is a substantial conservationissue because it modi1047297es the behaviorand community structure of animals

Nature-based tourism might modifybehavior in ways similar to that seenin domestication and urbanization aswell as modifythe population dynamicsof species

Domestication and urbanization reducethe fearfulness and antipredator beha-vior of animals around humans attribu-table to both habituation towardshumans anddisplacementof predators

Nature-based tourism could negativelyin1047298uence behavioral responses to pre-dators This could happen indirectlywhere human presence decreases thenumberof predatorsin a givenarea andmoredirectly whereindividualsbecomebolder following habituation resultingin a boldness syndrome that couldincrease vulnerability to predators

1Center of Study of the Meridional

Amazon Federal University of Mato

Grosso Sinop Brazil2INRA UR1037 LPGP Fish

Physiology and Genomics Campus

de Beaulieu 35000 Rennes France3Laboratory of Theoretical Ecology

and Synthesis Department of

Ecology Federal University of Goiaacutes

CP 131 74001-970 Goiacircnia Brazil4State University of Mato Grosso

Tangaraacute da Serra Mato Grosso Brazil5Laboratory of Behavioral Ecology of

Reproduction State University of

Ponta Grossa Av Gal Carlos

Cavalcanti 4748 84030-900 Ponta

TREE 2005 No of Pages 11

Trends in Ecology amp Evolution Month Year Vol xx No yy httpdxdoiorg101016jtree201509010 1copy 2015 Elsevier Ltd All rights reserved




events (eg [8]) and that provisioning food might increase aggression within and betweenspecies resulting in wounding [1] In addition to the short-term behavioral changes aggregationfollowing feeding events couldalso modify community structure by affecting species distributiondiversity and richness [9]

The ultimate consequences of this increased tolerance to humans are diverse Indeed humanpresence has been shown to impair different 1047297tness-related traits such as reproduction [10] and

offspring provisioning [11] To better understand how tolerance emerges and how it mayin1047298uence 1047297tness we need to step back and develop a more fundamental understanding of how animals respond to humans

How do Animals Respond to Humans

Animals can interact with humans in three main ways (i) they can be forced to interact through ataming process that ultimately may lead to domestication (ii) they can move to or remain in alocation where humans are settled (eg by urbanization) or (iii) they can passively interact withhumans as a consequence of ecotourism or nature-based tourism Although these three typesof interactions act at different spatiotemporal scales (ie local versus landscapes and evolu-tionary versus ephemeral) they all involve similar cognitive processes ndash habituation or sensiti-zation leading to approach or avoidance [12] ndash to the same nonthreatening stimulus (humans)Importantly the outcome of these interactions could then in1047298uence the outcomes of predatorndash

prey interactions In this sense habituation is often seen as synonymous with taming [1] as itwould lsquoincrease the ease of observation of animals by making them unnaturally tame toapproach by humansrsquo ([13] p 35)

We develop a framework that identi1047297es how antipredator behavior can be modi1047297ed followinghuman exposure in different contexts and how that might be deleterious for wild animals whenfacing natural predators or when humans hunt or illegally poach them This framework linksprocesses that occur over the short term (ie habituation) and longer term (ie domestication)to those that occur when animals interact with humans in both urban and more natural areas Ithighlights how selection for boldness which might result from interacting with humans canmake those individuals particularly susceptible to predation

Grossa Paranaacute Brazil6Department of Ecology and

Evolutionary Biology University of

California 621 Young Drive South

Los Angeles CA 90095-1606 USA

Correspondence marmotsuclaedu

(DT Blumstein)

Box 1 What Governs Habituation-like Processes

We assume that most individuals will respond to their 1047297rst human encounter as an acutely stressful experience andtherefore interpret humans as potential predators [83] It is worth noting that species seemingly vary in how they dealwith exposure to a 1047297rst human (ie boldness at the species level [84]) Following this initial encounter if the response

to humans declines over repeated exposures then the animal may accurately be described as having habituated tohumans By contrast if the responsiveness is enhanced with repeated human exposure then the animal could bedescribed as having sensitized to humans Both habituation and sensitization occur over time and lead to differentdegrees of tolerance Because tolerance is measured at a point in time we can view it as a behavioral lsquostatersquo (see [85]for a systematic review of the use and misuse of habituation tolerance and sensitization) While some speciesappear to go through habituation-like processes when facing chronic human exposure other sensitize to increasedhuman presence This could happen even in closely related species For instance jackass penguins (Spheniscus

demersus) [86] and Magellanic penguins (Sphenicus magellanicus) [87] appear to habituate to human presencewhile yellow-eyed penguins (Megadyptes antipodes) sensitize and thus are disturbed by humans [10] Whichvariables drive habituation-like processes In the Magellanic penguins for instance the rate of habituation dependson the intensity of tourist visitation [88] a variable that also has been observed to drive habituation in other species(eg Mediterranean mou1047298on [70]) The type of stressor (ie approach or capture [89]) and the type of tourism arealso important factors that in1047298uence the degree of habituation (pedestrians cars bikes horses [90]) Spatiotemporalvariables such as time of the day season (in1047298uencing reproduction territoriality migration) and food availability havebeen identi1047297ed as important as have life history traits of a species such as the duration of parental investment andbody size [12] At the intraspeci1047297c level sex temperament and previous experience with humans affect whether

yellow-eyed penguins habituate or sensitize to repeated human visitation [91] Calm individuals were more likely tohabituate as were females

2 Trends in Ecology amp Evolution Month Year Vol xx No yy




Domestication and Antipredator Behavior

Domestication involves cognitive processessuchas tameability and the reduction of aggressionfearfulness and sensitivity to environmental variation [14] These processes also occur when

animals interact with humans in the wild Domestication can lead to a progressive loss of antipredator behavior (eg [15]) An iconic study of domestication comes from Belyaevspioneering work on silver foxes (Vulpes vulpes) After almost 35 generations of captive handling80 of the handled foxes were signi1047297cantly more docile and responded less fearfully to novelstimuli than nonhandled control lines [16] Importantly these behavioral responses were trans-duced at the physiological level (there was a decrease of corticosteroid production) andaccompanied by important physical changes (loss of pigmentation development of 1047298oppyears and shorter tails) [16]

In salmonids domestication also led to reduced physiological and behavioral responses topredators [1718] For instance seventh generation juvenilesof domestic Atlantic salmon (Salmo

salar ) had reduced heart rates andlower 1047298ight responsesto simulated predator attacks than wildsalmon [17] More importantly when placed in seminatural conditions the 1047297rst and the second

generation of hatchery-reared juveniles from wild salmon had a signi1047297cantly reduced antipreda-tor response compared with their wild counterparts [18]

Similarly a study recently reported that after only one generation of laboratory breedingstickleback (Gasterosteus aculeatus) were much less responsive to simulated predatory attack when compared with their wild counterparts [19] Studies such as these highlight the essentialrole of experience in shaping antipredator responses and that these antipredator responsescould be strongly altered within the lifetime of an individual (ie early in the domesticationprocess) Nonetheless we also may have strongly directed responses that are associated withthe history of a population [19] and that might persist under relaxed selection [20]

Parental rearing patterns which sometimes change under domestication can also in1047298uence

antipredator behavior For instance when compared with goose-raised geese hand-raisedgreylag geese ( Anser anser ) suffered higher mortality when exposed to predators and had lowerglucocorticoid metabolites (a proxy for physiological stress) in response to social densityhandling and predator stress [21] In addition geese were less vigilant and selected less safenest boxes in which to lay their eggs (J Hemetsberger PhD thesis University of Vienna 2002)Moreover a number of studies have shown that rats (Rattus norvegicus) that had earlyexperiences with human handling had decreased fearfulness and modi1047297ed how they copedwith stressful situations in adulthood [22]

Livestock depredation by wild mammalian predators (eg pumas Puma concolor jaguarsPanthera onca and wolves Canis lupus) has traditionally been associated with distance tothe forest edge cattle density and cattle age [2324] However recent evidence also notedthat selection for docility impairs antipredator behavior when facing wolves [25] It should

be noted that this behavior was not assessed directly in this study but rather indirectlythrough the facial hair whorl pattern [25] which is a phenotypic trait associated with vigilancein cattle

Hence there is evidence that domestication directly selects for less wary and bolder individualsthat could then suffer higher predation in the wild (Figure 1 A Key Figure) This could also haveconsequences for animal conservation since early experience (or lack of it) with humans ornatural predators can also in1047298uence reintroduction success [26] Although there are to the bestof our knowledge no studies directly linking human-mediated boldness resulting from domesti-cation to increased predation risk in a reintroduction context studies have shown that variationin temperament can in1047298uence survival in released animals Bold (including those that were bold

GlossaryBehavioral spillover a suite of covarying behaviors that is adaptivelyselected in one context butmaladaptive in another context [79]Behavioral syndrome a suite of correlated behaviors across situations[80]Boldness the way in which anindividual andor population respondsto threatening situations Bolderindividuals take more risks [32]Domestication the process bywhich a wild species becomesadapted to humans in captiveenvironments by means of geneticchanges and developmental orbehavioral changes reinforced everygeneration [14]Ecotourism travel to natural areasin ways that are designed toconserve the environment andimprove the well-being of localpeopleFlight initiation distance (FID) thedistance between the predator orthreatening stimulus and prey whenthe prey begins to 1047298ee [35]Habituation decreasedresponsiveness of individuals causedby repeated exposure to a stimulus[81]Human shield prey species usehumans as shield from naturalpredation [61] This could happen in

both relatively wild and urban areasHuman-mediated behavioral

spillover when animals habituatedto humans bene1047297t by exhibitingbehaviors in close vicinity withtourists (either to acquire food orreceive passive protection frompredators) but these behaviorsbecome maladaptive when humansleave the area (eg the behaviorsmight increase predation risk)Individual behavioral reaction

norm the set of behavioralphenotypes that a single individualproduces in a given set of environments [82]

Nature-based tourism travelling innatural places although notnecessarily in a responsible way (seeecotourism)Personality consistent individualdifferences in behavior over time and or context [59]Safe-habitat hypothesis

hypothesizes that abundance of native predators decreases in urbanareas reducing predation risk andconsequently the antipredatorbehavior of their prey [46]

Trends in Ecology amp Evolution Month Year Vol xx No yy 3




towards humans) captive-bred swift foxes (Vulpes velox ) suffered much higher mortality thantheir shyer conspeci1047297cs upon release to a natural predator-rich environment [27]

To conclude antipredator responses may be modi1047297ed by experience and thus the speci1047297cresponse to predators could be lost or modi1047297ed by domestication (Figure 1 A) Such changesmay happen quickly within a single generation (this is also referred to as lsquoexperienceadaptive developmentrsquo or lsquoexperience adaptive programmingrsquo see [28]) and have 1047297tness

consequences

Urbanization and Antipredator Behavior

Characteristics of Antipredator ResponsesNot all species successfully colonize urban habitats [2930] Yet urbanization shares similarfeatures with taming processes in terms of the cognitive and physiological traits favored byselection such as reduced fearfulness increased aggressiveness and reduced levels of circulating corticosteroids [3132] Species often have reduced 1047298ight initiation distances

(FID) in urban areas when compared with rural areas [33] and the presence of arti1047297cial feedingsites also can reduce FID [34] Importantly FID is one metric by which individuals (and species)can be compared with respect to their boldness [35]

Urbanization the process by whichanimals and plants modify theirbehavior and physiology to urbanenvironments with the change from

ancestral rural to recent urbanenvironments being the relevanttransition [53]

(A) Domescaon (B) Urbanizaon (C) Tourism

Prey

Prey will suffer high

predaon risk once

released in the wild

Transfer of habituaon

and inexperience with

predators



nave predators

Process

(i) Within the city (ii) Outside the city


predaon risk once

tourists leave the place

(eg at night or winter)

Transfer of habituaonInexperience with nave

predators

Border of the shield not

well defined depends on

preyrsquos percepon and

migraon


predaon risk if genuine

predators enter

Predators

Predators surrounding gradient

Shield

Response

Human contact gradient

Vigilance

Boldness

Vigilance

Boldness

Vigilance

Boldness

Vigilance

BoldnessFID FID FID

Figure 1 Animals Respond to Human Presence along a Gradient from Domestication to Nature-Based Tourism (A) During domestication animals become tamed and remain close to humans This involves a decrease of fearfulness at both behavioral and physiological levels Such animals are bold towards humans and can suffer enhancedpredation risk if released in natural areas (B) During urbanization (i) within the city animals can either become boldor already bold animals are attracted to the city because of the human shield and habituation to humans These animalswill sufferhigh predationrisk if predators enter thecitysince they areless alert A human shieldalso exists(ii) outsidethe city(egin rural areas) such that theantipredator vigilanceof a prey is attenuated andanimals will sufferpredationaccording to

their risk perception (C) When tourists contact wild animals they create a temporal shield and a boldness syndrome mainlyas a result of habituation (through presence alone andor by food provisioning) mimicking what happens during domes-tication and with urbanization This can create individuals more susceptible to predation when tourists leave (see Figure 2)

Abbreviation FID Flight initiation distance





When approached by humans the average FID of fox squirrels (Sciurus niger ) was almost seventimes smaller in urban areas than in rural areas [36] For 48 European bird species FID was onaverage two times smaller in urban areas when compared with rural areas [31] suggesting that

boldness is associated with urbanization It is worth noting that some species inhabiting urbanenvironments have greater FIDs compared with their rural counterparts but these urbanpopulations suffer higher predation by sparrowhawks ( Accipiter nisus) when compared withrural populations [37] If these species are preferentially targeted by sparrowhawks in townsthen this would explain their higher FIDs (towards humans) in urban areas Nevertheless it isdif 1047297cult to disentangle causes from consequences since species with short FID (eg towardshumans) could also suffer higher predation resulting from their lower overall reduced fearfulness[3839] Hence it is likely that both predation pressure (which increases FID) and acclimation tourban area (which decreases FID) shapes the FID response of different species towards humanswithin towns

Currently it is not known whether only bold individuals from different species are able tosuccessfully colonize urban areas or if individuals that settled in cities become bold as a result

of rapid behavioral adjustments [40] Using relative brain size as a proxy for behavioral 1047298exibility[41] one study found that brained species are highly variable in their FIDs and are also more likelyto become successful urban colonizers [42] However two recent studies did not con1047297rm theeffect of relative brain size on urbanization either at the intraspeci1047297c or interspeci1047297c level [4344]Regardless living in urban areas is associated with a number of cognitive modi1047297cations Forexample the structure of communication is modi1047297ed [30] animals encounter new foragingopportunities [45] and animals reduce their FID in response to humans [37ndash39]

Human Shields around Urban AreasPredators can avoid areas with human presence as a result of the so-called lsquohuman shieldrsquo

effect [46] This human shield effect is part of the safe-habitat hypothesis [47] that describeshow predators are more likely to be absent in urban areas Such safe habitats have a variety of

consequences For instance nest predation is drastically decreased inside barns and shedswhere predators fear to go compared with adjacent outdoor areas [48] Human shields and safehabitats effects are important because they can provide a relatively safe area for potential prey[49] making them less vigilant and more likely to allocate their time on 1047297tness-enhancingactivities such as foraging [50] Human shields can partially explain why prey could be saferin urban areas if urbanization reduces predator presence and diversity [51] and also providesrefuge from predators [52] However the safe-habitat hypothesis should be treated with cautionbecause some generalist predators such as cats do extremely well around humans and tendto be abundant in urban areas [38]

Ecological Consequences Two Causes One Possible OutcomeBecause habituation-like processes are a widespread mechanism driving human tolerance inmany species (but see Box 1) this raises the question of whether habituation to humans can be

transferred to genuine predators (Figure 1Bi) This question hasbeen investigated in fox squirrelswhere individuals that were part of a population habituated to human presence (shown by adecreased FID) were also less responsive to different predator vocalizations compared withrural fox squirrels [36] Although this result should be interpreted with caution (as a result of pseudoreplication ie the statistical unit is lsquoblock rsquo within one population) this is the 1047297rst andpossibly the only documented case of transfer of habituation between humans and nativepredators for fox squirrels in a 1047297eld setting [36]

Moslashller and Ibaacutentildeez-Aacutelamo [53] also found that urban individuals of 15 bird species wriggledpecked and bit less when removed from mist nets than rural individuals suggesting relaxedantipredator behavior in cities The mechanisms underlying these responses are dif 1047297cult to





isolate Is the relaxation of antipredator behavior (shorter FID) in urban areas attributable tohuman shields (Figure 1Biii) and thus reduced predation risk Or is this change caused byhabituation to nonthreatening stimuli It is possible that both processes occur simultaneously

and hence increase prey vulnerability to predators (Figure 1B) Conducting experiments withpredators that arerecolonizing urban areas (eg foxes in London [54]) might offer an opportunityto disentangle these mechanisms

Tourist Exposure and Antipredator Behavior

Human presence might thus act in two nonmutually exclusive ways (i) indirectly by creating ahuman shield that relaxes antipredator behavior of prey and (ii) directly such that docility andboldness emerge from repeated interactions with nonthreatening humans and these responsesare then transferred to other more-threatening sources (ie genuine predators or wildlifepoachers) resulting from a behavioral spillover

Human Shields in the Wild An Indirect PathwayIn contrast to domestication and urbanization where exposure to predators is likely reduced

nature-based tourism occurs in the wild often in relatively intact predator communities(Figure 1C) Nonetheless extensive human visitation to a wild location could create a temporaryhuman shield In this sense human presence has been shown to reduce the probabilityof encounters between vervet monkeys (Chlorocebus pygerythrus) and predatory leopards(Panthera pardus) [55] In another more recent example tourist presence (using car traf 1047297c asa proxy) also sheltered both pronghorn ( Antilocapra americana) and elk (Cervus elephus) frompredators in Grand Teton National Park [56] This modi1047297ed prey behavior pronghorn and elk spent signi1047297cantly less time in alert postures more time feeding and were in smaller groups inthe areas with many tourists compared with the areas with fewer tourists [56] Human presencealso directly affects risk perception to terrestrial predators in samango monkeys (Cercopithecus

mitis erythrarcus) who usually spend more time foraging on the ground around humans [57] The indirect pathway assumes a process that is similar to relaxed selection where individuals that

temporarily live without predators have reduced antipredator defenses (Box 2) This might leadto increased predation when humans leave the place (eg at night or winter the indirectpathway in Figure 2)

Box 2 Permanent versus Temporary Human Shields

Tourist or other human presence can create a human shield (habitat free of predators) that can relax antipredatorbehavior during the lifetime of an individual Antipredator behavior in predator-free environments is often lost [92] andcould occur relatively quickly (eg less than 130 years in tammar wallabies Macropus eugenii [93]) We note that thetaming process relaxes antipredator vigilance [94] but this selection process occurs over several generations Similarlyurbanization relaxes antipredator vigilance (and more general wariness) because individuals assess reduced risk whenprotected by human presence Both domestication and urbanization can create more lasting human shields whilenature-based tourism can create a temporary although effective [57] shield

In the case of hunting animals might have relaxed antipredator behavior when not hunted This has been seen duringperiodically 1047297shing closures where individuals decrease their wariness (as shown by shorter FIDs) and suffer highercapture rates when 1047297shing is reinstated [95] as well as when mammal poachers are temporarily absent With respect tohuman shields linked to tourism the core question is to determine whether the temporary presence of humans issuf 1047297cient to either permanently reduce antipredator abilities or reduce them for a suf 1047297ciently long time so that thepopulation suffers

Although this has never been formally tested it is conceivable that animals living around substantial and invasive tourismcan indeed modify their perceptions so that human presence is associated with safety Nevertheless the intensity of nature-based tourism usually changes according to the season and predator presence can vary accordingly Forinstance animals might not encounter usual threats for some months (eg during spring and summer tourist seasons)while they would have to face high predation risk in other periods (eg during the fall and winter) Hence the mainquestion is to understand how fast antipredator behavior can be lost or reduced under temporarily relaxed predationpressure





Increased Tolerance to Humans A Direct Pathway As shown by the urbanization examples described earlier the presence of humans can haveunanticipated effects on prey antipredator behavior even in the wild For instance some animalshabituated to tourism presence andor provisioning become bolder andor more aggressive[156] Can boldness and aggressiveness be repeatable over time andor acrosscontexts Thiskey question has been partly answered by studies that show repeatable behavioral traits [5859]

and by those showing that animals reduce 1047298exibility with experience [6061] If the developmentof personality is affected by early experiences and animals then 1047297nd themselves in a relativelydirected trajectory based on those early experiences exposure to benign humans can createpotentially maladaptive traits or syndromes (Box 3)

At the physiological level there are proximate processes acting through the hypothalamicndash

pituitaryndashadrenal (HPA) axis that might reduce overall responsiveness to humans over time andwe know that early experiences modify HPA sensitivity over longer periods [62] Exposure totourism reduces stress-induced corticosteroid production in some species [63] and couldincrease it in others [10] Nevertheless the process of habituation to human presence fromtourism decreases corticosteroid production over time [64]

PresenceFeeding

Decreased vigilance

Human shield(Indirect pathway)

Fewer predators

Increased predaon

Habituaon(Direct pathway)

Increased

aggressiveness

Bolder individuals

Decreased

fearfulness

Humans Predator 1 Predator 2

(A)

B o l d n e s s

Habituated

Unhabituated

(B)

B o l d n e s s

Habituated

Unhabituated

Human-mediated behavioral spillover

i


Figure 2 The Link between Intensive Wildlife-Based Tourism and Natural Predation Both indirect (throughdecreasing vigilance) and direct (through increased boldness) pathways would enhance predation risk The indirectpathway (salmon colored) assumes a process related to relaxed selection where individuals found in predator-freehabitats lose (previously learned or even evolved) defenses against predators temporally pushed away The direct

pathway (blue colored) assumes that docility and boldness emerge from interaction with nonthreatening humans andthese are transferred when encountering more-threatening species (A) Similar behavioral reaction norms for animalsunhabituated and habituated to human presence as a function of different contexts (humans or predator types) (B)Different behavioral reaction norms for animals unhabituated and habituated to human presence as a function of different contexts (humans or predator types) Note that habituated animals are bolder towards potential threats eithergenuine predators or wildlife poachers





While boldness could be the result of human habituation and behavioral spillover could enhancepredation risk the direct link between both is more dif 1047297cult to establish since it would mean thatanimals that become bold and aggressive towards humans (eg through habituation) transfertheir habituation to real predators (Figure 1C) This pathway may seem unlikely at 1047297rst glancebecause it would mean that humans are classi1047297ed into the same category as nonhumanpredators and we know that many species are able to discriminate predators from nonpredators[65] as well as to discriminate among different predators based on their level of threat [66]Moreover we also know of at least two studies that found that human habituation enhancedpredator discrimination [5067] Nevertheless neither of these studies formally tested for atransfer of habituation but rather capitalized on how individuals around humans were more

tolerant of humans and then asked how the ability to discriminate between potential predatorsand nonpredatory species was effected by human exposure As with squirrels that were lessresponsive to predator vocalizations in urban areas [36] a transfer of habituation can also haveoccurred in blackbirds (Turdus merula) exposed to tourists in parks [68] Blackbirds decreasedtheir FID with increased exposure to humans (consistent with an habituation-like process) Inaddition blackbirds from high visitation areas had shorter FIDs in response to a novel threat-ening stimulus (cars) [68] Nevertheless a possible caveat to this study relies on the fact that theauthors did not take into account pseudoreplication (ie subsamples within parks and individ-uals that could have been sampled more than once) in their statistical analysis Regardless aswe summarize in Figure 2 individuals might differentiate predators but have an overall reducedresponse to them following human habituation

Hence the main question focuses on the nature of the individual behavioral reaction norm

Speci1047297cally how do bolder animals respond to humans and to predators Indeed indepen-dently of the underlying process involved in the presence of bolder individuals in areas withpeople (including tourists) if individuals become more tolerant to predators (Figure 2 AB) theirvulnerability will be enhanced This is an empirical question worthy of study which could betested by designing experiments similar to those used in the blackbird study [68] and the squirrelstudy [36] but in wild areas with real predators

Apart from natural predators another important issue concerns wildlife poachers who might alsobene1047297t from tourist-habituated wildlife It is not currently clear whether or not animals are able todistinguish legal hunters from tourists This distinction might be tightly associated with cognitivecapacities of the species and the type of hunting For instance elephants (Loxodonta africana)

Box 3 A Human-Mediated Behavioral Spillover

Both environmental [96] and earlysocial experiences[97] canin1047298uencehow an individual typically behaves including howthey respond to novel situations Naiumlve juveniles generally are more wary and have greater FIDs in response to humansthan adults [36] suggesting an habituation-like process where adult individuals became less wary after having multiple

encounters with nonthreatening stimuli such that their reaction norm decreases over time (eg leads to a decrease of corticosteroids throughout ontogeny in response to tourism [6487]) This highlights the importance of early experiencesin shaping behavioral traits (lsquoexperience adaptive developmentrsquo or lsquoexperience adaptive programmingrsquo for captiveindividuals [28]) that become progressively 1047297xed with age (see [61] and references therein)

Antipredator behavior such as FID could be considered a personality trait in some species since there can be a very hightemporal repeatability (eg R = 084 ndash 092 in burrowing owls Athene cunicularia [98]) The emergence of suchpersonality traits hasbeenexplained in thecontext of 1047297tnesstrade-offswhereby a givenbehavior couldbe advantageousin one situation while it would not be in another In Namibian rock agamas ( Agama planiceps) bolder males had greateraccess to food but they also suffered increased tail loss when compared with shyer individuals [99]Whena behavioral

syndrome has adaptive consequences in one context but maladaptive consequences in another (eg with and withouta predator present) the term lsquobehavioral spilloverrsquo is used North American 1047297shing spiders (Dolomedes triton) with highlevel of voracity in foraging (resulting in high 1047297tness) and mating contexts (resulting in low 1047297tness) were also bolder in acontext of a simulated predatory attack (resulting in low 1047297 tness) [79] In summary if habituation to humans leads toa general decrease in fearfulness this habituation might also lead to inappropriate (perhaps fatal) behavior in othercontexts such as being bold in the presence of predators resulting in a lsquohuman-mediated behavioral spilloverrsquo





are able to distinguish hunters (Maasai men) from nonhunters (Maasai women and children)based on their voices [69] Mou1047298on (Ovis gmelini musimon) readily identify noisy hunting withhounds [70] while more silent spearguns might not be well detected by 1047297sh [71] Regardless we

could view wildlife poaching as a form of lsquo

cheatingrsquo

in cases where a population has habituatedto benign human presence and then individuals are caught off guard by a poacher Viewed thisway a small degree of very successful poaching can be tolerated before individuals in apopulation learn to associate humans with enhanced risk resulting in higher capture rates[7273] For instance gorillas (Gorilla gorilla graueri ) habituated to tourist presence 1047298ed moreslowly and did not readily attack or hide when a poacher approached when compared withnonhabituated gorillas [72] This has also been observed for wild Barbary macaques ( Macaca

sylvanus) which are extremely habituated to humans and which are easy targets for poachers[73]

Concluding Remarks

We know that humans are able to drive rapid phenotypic change in other species [74] If individuals selectively habituate to humans ndash particularly tourists ndash and if invasive tourism

practices enhance this habituation we might be selecting for or creating traits or syndromesthat have unintended consequences such as increased predation risk (Figure 2) Even a smallhuman-induced perturbation could affect the behavior or population biology of a species andin1047298uence the function of the species in its community [75] Such cryptic function loss and theassociated reduction in functional diversity are considered to be among the most signi1047297cantconcerns for ecosystem stability [75] Exposure to humans can also reduce phenotypic variationand behavioral plasticity Since behavioral plasticity might mirror genetic diversity ecotourismcould also drive the loss of genetic diversity The effect might even be greater if human-linkedperturbations affect keystone species or individuals [7677] Owing to the plethora of impactsnature-based tourism has on wildlife it could well be added to the list of drivers of human-induced rapid environmental change (HIREC) which already includes habitat change pollutionexotic species human harvesting and climate change [78] Our review highlights numerous

unanswered questions (see Outstanding Questions) that could be tested with the ultimate goalof better understanding whether and how habituation to human presence creates deleteriouseffects to wildlife

Acknowledgments

Early discussions with Michael Clinchy andLianaZanettehelped us clarifyour argumentIn addition wethankOdedBerger-

Tal and three anonymous reviewers who provided extensive feedback that signi1047297cantly improved this manuscript Amine

Boucharebhelpedin drafting the 1047297guresBG is supportedby a CAPES-Ciecircncia SemFronteiras grant A045_2013 DSM

S is supportedby CAPESEB wasfunded by FAPEMAT (Process 0021912007) DTBis supportedby theUS National

Science Foundation (NSF)

Resourcesi wwwturismogovbrturismonoticiastodas_noticias20131112html

References1 Knight J (2009) Making wildlife viewable habituation and attrac-

tion Soc Anim 17 167ndash184

2 Balmford A et al (2015) Walk on the wild side estimating theglobal magnitude of visits to protected areas PLoS Biol 13e1002074

3 Prideaux B and Cooper M (2009) River Tourism CABIPublishing

4 OrsquoConnor S et al (2009) Whale Watching Worldwide Tourism

Numbers Expenditures and Expanding Economic Bene1047297 ts A

Special Report from the International Fund for Animal Welfare

International Fund for Animal Welfare

5 Ikuta LAand BlumsteinDT (2003) Do fences protect birdsfromhuman disturbance Biol Conserv 112 447ndash452

6 Webb NV and Blumstein DT (2005) Variation in human distur-bance differentially affects predation risk assessment in WesternGulls The Condor 107 178ndash181

7 Lloyd J and Ajarova L (2005) Chimpanzee habituation for tour-ism In World Atlas of Great Apes and their Conservation (Calde-cott J and Miles L eds) pp 76ndash77 University of California Press

8 Gaspar C et al (2008) Feeding sites frequentation by the pink whipray Himantura fai in Moorea (French Polynesia) as determinedby acoustic telemetry Cybium 32 153ndash164

9 Albuquerque T et al (2014) In situ effects of human disturbanceson coral reef-1047297sh assemblage structure temporary and persistingchanges arere1047298ectedas a result of intensivetourism MarFreshw

Res 66 23ndash32

Outstanding Questions Are humans always initially perceivedas predators

How often does habituation explaintolerance

How do bolder animals respond tohumans and to predators

Under what conditions do animalstransfer habituation from humans toreal predators

Which intrinsic factors explain variationbetween species in human-orientedboldness In other words why dosome species acclimate well to humanpresence while others avoid humans

Is the human-mediated behavioral

spillover in1047298uencing antipredatorbehavior affected by predator origin(ie native or alien species)

With respect to human shields linkedtotourism the core question is to deter-mine whether the temporary presenceof humans is suf 1047297cient to either perma-nently reduce antipredator abilities orreduce them for a suf 1047297ciently long timeto drive population decline

Given temporal variation in risk howfast can antipredator behavior be lostor reduced under temporary relaxedpredation pressure

How often does human presencereduce vigilance by distracting preyand diverting their attention

What are the evolutionary responses of animals to nature-based tourism





10 Ellenberg U et al (2007) Elevated hormonal stress response andreduced reproductive output in yellow-eyed penguins exposed tounregulated tourism Gen Comp Endocrinol 152 54ndash63

11 McClungMR etal (2004) Nature-based tourism impacts yellow-eyed penguins Megadyptes antipodes does unregulated visitor

access affect 1047298edging weight and juvenile survival Biol Conserv119 279ndash285

12 Higham JES and Shelton EJ (2011) Tourism and wildlifehabituation reduced population 1047297 tness or cessation of impactTourism Manage 32 1290ndash1298

13 Reynolds PC and Braithwaite D (2001) Towards a conceptualframework for wildlife tourism Tourism Manage 22 31ndash42

14 Price EO (ed) (2002) Animal Domestication and Behavior CABIPublishing

15 Kohane MJ and Parsons PA (1989) Domestication evolution-ary change under stress Evol Biol 23 31ndash48

16 Trut LN (1999) Early canid domestication the farm-fox experi-ment Am Sci 24 124ndash129

17 Johnsson JI et al (2001) Behavioural and heart rate responsesto predation riskin wildand domesticated Atlantic salmon Can J

Fish Aquat Sci 58 788ndash794

18 Jackson CD and Brown GE (2011) Differences in antipredator

behaviour between wild and hatchery-reared juvenile Atlanticsalmon (Salmo salar ) under seminatural conditions Can J Fish

Aquat Sci 58 2157ndash2165

19 Wund MA et al (2015) The evolution of antipredator behaviourfollowing relaxed and reversed selection in Alaskan threespinestickleback 1047297sh Anim Behav 106 181ndash189

20 Blumstein DT (2006) The multi-predator hypothesis and theevolutionary persistence of antipredator behavior Ethology 112209ndash217

21 Hemetsberger J et al (2010) In1047298uence of socially involved hand-raising on life history and stress responses in greylag geeseInteract Stud 11 380ndash395

22 Macrigrave S and Wuumlrbel H (2006) Developmental plasticity of HPA and fear responses in rats a critical review of the maternal media-tion hypothesis Horm Behav 50 667ndash680

23 Palmeira FB et al (2008) Cattle depredation by puma (Puma

concolor ) and jaguar (Panthera onca) in central-western BrazilBiol Conserv 141 118ndash125

24 CarvalhoEA (2015) Modeling the riskof livestockdepredation by jaguar along the Transamazon highway Brazil Basic Appl Ecol

16 413ndash419

25 Floumlrcke Cand Grandin T (2013) Lossof anti-predator behaviorsin cattle and the increased predation losses by wolves in thenorthern rocky mountains Open J Anim Sci 3 248ndash253

26 McPhee E (2004) Generations in captivity increases behavioralvariance considerations for captive breeding and reintroductionprograms Biol Conserv 115 71ndash77

27 Bremner-Harrison S et al (2004) Behavioural traitassessment asa release criterion boldness predicts early death in a reintroduc-tion programme of captive-bred swift fox (Vulpes velox ) Anim

Conserv 7 313ndash320

28 Mason G et al (2013) Plastic animals in cages behavioural1047298exibility and responses to captivity Anim Behav 85 1113ndash1126

29 Phillips BL and Suarez AV (2012) The role of behaviouralvariation in the invasion of new areas In Behavioural Responses

to a Changing World Mechanisms and Consequences (CandolinU and Wong BBM eds) pp 190ndash200 Oxford University Press

30 Slabbekoorn H (2013) Songs of the city noise-dependent spec-tral plasticity in the acoustic phenotype of urban birds Anim

Behav 85 1089ndash1099

31 MoslashllerAP (2010) Interspeci1047297c variationin fearresponses predictsurbanization in birds Behav Ecol 21 365ndash371

32 Lowry H et al (2013) Behavioural responses of wildlife to urbanenvironments Biol Rev 88 537ndash549

33 Magle S et al (2005) Behavioral responses to repeated humanintrusion by black-tailed prairie dogs (Cynomys ludovicianus) J Mammal 86 524ndash530

34 Moslashller AP et al (2015) Urban habitats and feeders both contrib-ute to 1047298ight initiation distance reduction in birds Behav Ecol 6 8

35 Cooper WE Blumstein DT eds (2015) Escaping from

Predators An Integrative View of Escape Decisions CambridgeUniversity Press

36 Mccleery RA (2009) Changes in fox squirrel anti-predator behav-iors acrossthe urbanndashrural gradient LandscapeEcol 24 483ndash493

37 Moslashller AP (2008) Flight distance of urban birds predation andselection for urban life Behav Ecol Sociobiol 63 63ndash75

38 Moslashller AP etal (2008) Risktaking by singing males Behav Ecol

19 41ndash53

39 Moslashller AP (2014) Life history predation and 1047298 ight initiation dis-tance in a migratory bird J Evol Biol 27 1105ndash1113

40 Sol D et al (2013) Behavioural adjustments for a life in the city Anim Behav 85 1101ndash1112

41 Sol D etal (2005) Brainsize innovativepropensity and migratorybehaviour in temperate Palaearctic birds Proc R Soc B Biol

Sci 272 1433ndash1441

42 CarreteM andTella JL(2011)Inter-individual variabilityin fearof humans and relative brain size of the species are related tocontemporary urban invasion in birds PLoS ONE 6 e18859

43 Dale S et al (2015) Commonness and ecology but not biggerbrains predict urban living in birds BMC Ecol 15 12

44 Moslashller AP and Erritzoslashe J (2015) Brain size and urbanization in

birds Avian Res 6 1ndash745 Sol D et al (2012) Unraveling the life history of successful

invaders Science 337 580ndash583

46 Berger J (2007) Fearhuman shields andthe redistributionof preyand predators in protected areas Biol Lett 3 620ndash623

47 Valcarcel A and Fernaacutendez-Juricic E (2009) Antipredator strat-egies of house 1047297nches are urban habitats safe spots from pred-ators even when humans are around Behav Ecol Sociobiol 63673ndash685

48 Moslashller AP (2010) The 1047297tness bene1047297t of association withhumans elevated success of birds breeding indoors Behav

Ecol 21 913ndash918

49 Waser NM et al (2014) Coyotes deer and wild1047298owers diverseevidence points to a trophic cascade Naturwissenschaften 101427ndash436

50 Coleman A et al (2008) Does habituation to humans in1047298uencepredator discrimination in Gunthers dik-diks (Madoqua guen-

theri ) Biol Lett 4 250ndash

25251 Shochat E et al (2006) From patterns to emerging processes in

mechanistic urban ecology Trends Ecol Evol 21 186ndash191

52 Moslashller AP (2012) Urban areas as refuges from predators and1047298ight distance of prey Behav Ecol 23 1030ndash1035

53 Moslashller AP and Ibaacutentildeez-Aacutelamo JD (2012) Escape behaviour of birds provides evidence of predation being involved in urbaniza-tion Anim Behav 84 341ndash348

54 Bateman PW and Fleming PA (2012) Big city life carnivores inurban environments J Zool 287 1ndash23

55 Isbell LA and Young TP (1993) Human presence reducespredation in a free-ranging vervet monkey population in Kenya Anim Behav 45 1233ndash1235

56 Shannon G et al (2014) Behavioral responses associated with ahuman-mediated predator shelter PLoS ONE 9 e94630

57 Nowak K et al (2014) Human observers impact habituatedsamango monkeysrsquo perceived landscape of fear Behav Ecol

25 1199ndash

120458 Dall SRX et al (2004) The behavioural ecology of personality

consistent individual differences from an adaptive perspectiveEcol Lett 7 734ndash739

59 Fuumlrtbauer I et al (2015) Personality plasticity and predationlinking endocrine and behavioural reaction norms in stickleback 1047297sh Funct Ecol httpdxdoiorg1011111365-243512400

60 Bergmuumlller R and Taborsky M (2010) Animal personality due tosocial niche specialisation Trends Ecol Evol 25 504ndash511

61 Groothuis TGG and Trillmich F (2011) Unfolding personalitiesthe importance of studying ontogeny Dev Psychobiol 53641ndash655

62 Mirescu C et al (2004) Early life experience alters response of adult neurogenesis to stress Nat Neurosci 7 841ndash846





63 Romero LM and Wikelski M (2002) Exposure to tourismreduces stress-inducedcorticosteronelevelsin Galapagosmarineiguanas Biol Conserv 108 371ndash374

64 Shutt K et al (2014) Effects of habituation research and eco-tourism on faecal glucocorticoid metabolites in wild western low-

land gorillas implications for conservation management BiolConserv 172 72ndash79

65 Belton LE et al (2007) Do Cape ground squirrels ( Xerus inauris)discriminate between olfactory cues in the faeces of predatorsversus non-predators Afric Zool 42 135ndash138

66 Liesenjohann T and Eccard JA (2008) Foraging under uniformrisk from different types of predators BMC Ecol 8 19

67 Carrasco MF and Blumstein DT (2012) Mule deer (Odocoileus

hemionus) respond to yellow-belliedmarmot( Marmota 1047298 aviventris)alarm calls Ethology 118 243ndash250

68 Rodriguez-Prieto I etal (2009)Antipredator behaviorin blackbirdshabituationcomplements risk allocation Behav Ecol 20 371ndash377

69 McComb K et al (2014) Elephants can determine ethnicitygender and age from acoustic cues in human voices Proc Natl

Acad Sci USA 111 5433ndash5438

70 Marchand P et al (2014) Impacts of tourism and hunting on alargeherbivores spatio-temporalbehaviorin and around a French

protected area Biol Conserv 177 1ndash

1171 Januchowski-Hartley FA et al (2012) In1047298uence of spear guns

dive gear and observers on estimating 1047297sh 1047298ight initiation distanceon coral reefs Mar Ecol Prog Ser 469 113ndash119

72 Kasereka B et al (2006) Vulnerability of habituated Grauersgorilla to poachingin the Kahuzi-Biega NationalPark DRC African

Stud Monogr 27 15ndash26

73 Meacutenard N et al (2014) How tourism and pastoralism in1047298uencepopulation demographic changes in a threatened large mammalspecies Anim Conserv 17 115ndash124

74 HendryAP etal (2008) Humanin1047298uences on ratesof phenotypicchange in wild animal populations Mol Ecol 17 20ndash29

75 McConkey KR and OrsquoFarrill G (2015) Cryptic function loss inanimal populations Trends Ecol Evol 30 182ndash189

76 Bond WJ (1994) Keystone species In Biodiversity and Ecosys-

tem Function (Schulze ED and Mooney HA eds) pp 237ndash

253 Springer

77 Modlmeier AP et al (2014) The keystone individual concept anecological and evolutionary overview Anim Behav 89 53ndash62

78 Sih A (2013) Understanding variationin behavioural responsestohuman-induced rapid environmental change a conceptual over-view Anim Behav 85 1077ndash1088

79 Johnson JC and Sih A (2005) Precopulatory sexual cannibal-ism in 1047297shing spiders (Dolomedes triton) a role for behavioralsyndromes Behav Ecol Sociobiol 58 390ndash396

80 Sih A et al (2004) Behavioral syndromes an ecological andevolutionary overview Trends Ecol Evol 19 372ndash378

81 McFarland D (1993) Animal Behaviour Psychobiology Ecology

and Evolution (2nd edn) Longman Scienti1047297c and Technical

82 Dingemanse NJ et al (2010) Behavioural reaction norms animalpersonality meets individual plasticity Trends Ecol Evol 2581ndash89

83 FridA and DillLM (2002) Human-caused disturbance stimuli asa form of predation risk Conserv Ecol 6 11

84 Holmes ND (2007) Comparing king gentoo and royal penguinresponses to pedestrian visitation J Wildl Manag 712575ndash2582

85 Bejder L et al (2009) Impact assessment research use andmisuse of habituation sensitisation and tolerance in describingwildlife responses to anthropogenic stimuli Mar Ecol Prog Ser

395 177ndash185

86 van Heezik Y and Seddon PJ (1990) Effect of human distur-banceon beachgroupsof jackasspenguinsSAfric JWildl Res

20 89ndash93

87 WalkerBG etal (2006) Habituationof adultMagellanic penguinsto human visitation as expressed through behavior and cortico-sterone secretion Conserv Biol 20 146ndash154

88 Fowler GS(1999) Behavioraland hormonal responsesof Magel-lanic penguins (Spheniscus magellanicus) to tourism and nest sitevisitation Biol Conserv 90 143ndash149

89 Viblanc VA et al (2012) Coping with continuous human distur-bance in the wild insights from penguin heart rate response to

various stressors BMC Ecol 12 1090 Li C et al (2011) Quantifying human disturbance on antipredator

behavior and 1047298ush initiation distance in yellow-bellied marmots Appl Anim Behav Sci 129 146ndash152

91 Ellenberg U et al (2009) Habituation potential of yellow-eyedpenguins depends on sex character and previous experiencewith humans Anim Behav 77 289ndash296

92 Lahti DC et al (2009) Relaxed selection in the wild Trends Ecol

Evol 24 487ndash496

93 Blumstein DT et al (2004) A test of the multi-predator hypothe-sis rapid loss of antipredator behavior after 130 years of isolationEthology 110 919ndash934

94 Beauchamp G (2015) Animal Vigilance Elsevier

95 Januchowski-Hartley FA et al (2014) Fishery bene1047297ts frombehavioural modi1047297cation of 1047297shes in periodically harvested1047297sheries closures Aquatic Conserv Mar Freshw Ecosyst

24 777ndash790

96 Hensley NM et al (2012) Personality and habitat segregation ingiantsea anemones (Condylactis gigantea) J Exp Mar Biol Ecol

426ndash427 1ndash4

97 Geffroy B et al (2014) The link between social network densityand rank-order consistency of aggressiveness in juvenile eelsBehav Ecol Sociobiol 68 1073ndash1083

98 Carrete M and Tella JL (2010) Individual consistency in 1047298 ightinitiation distances in burrowing owls a new hypothesis on dis-turbance-induced habitat selection Biol Lett 6 167ndash170

99 Carter AJ et al (2010) Agamas exhibit behavioral syndromesbolder males baskand feedmore but may suffer higher predationBehav Ecol 21 655ndash661





events (eg [8]) and that provisioning food might increase aggression within and betweenspecies resulting in wounding [1] In addition to the short-term behavioral changes aggregationfollowing feeding events couldalso modify community structure by affecting species distributiondiversity and richness [9]

The ultimate consequences of this increased tolerance to humans are diverse Indeed humanpresence has been shown to impair different 1047297tness-related traits such as reproduction [10] and

offspring provisioning [11] To better understand how tolerance emerges and how it mayin1047298uence 1047297tness we need to step back and develop a more fundamental understanding of how animals respond to humans

How do Animals Respond to Humans

Animals can interact with humans in three main ways (i) they can be forced to interact through ataming process that ultimately may lead to domestication (ii) they can move to or remain in alocation where humans are settled (eg by urbanization) or (iii) they can passively interact withhumans as a consequence of ecotourism or nature-based tourism Although these three typesof interactions act at different spatiotemporal scales (ie local versus landscapes and evolu-tionary versus ephemeral) they all involve similar cognitive processes ndash habituation or sensiti-zation leading to approach or avoidance [12] ndash to the same nonthreatening stimulus (humans)Importantly the outcome of these interactions could then in1047298uence the outcomes of predatorndash

prey interactions In this sense habituation is often seen as synonymous with taming [1] as itwould lsquoincrease the ease of observation of animals by making them unnaturally tame toapproach by humansrsquo ([13] p 35)

We develop a framework that identi1047297es how antipredator behavior can be modi1047297ed followinghuman exposure in different contexts and how that might be deleterious for wild animals whenfacing natural predators or when humans hunt or illegally poach them This framework linksprocesses that occur over the short term (ie habituation) and longer term (ie domestication)to those that occur when animals interact with humans in both urban and more natural areas Ithighlights how selection for boldness which might result from interacting with humans canmake those individuals particularly susceptible to predation

Grossa Paranaacute Brazil6Department of Ecology and

Evolutionary Biology University of

California 621 Young Drive South

Los Angeles CA 90095-1606 USA

Correspondence marmotsuclaedu

(DT Blumstein)

Box 1 What Governs Habituation-like Processes

We assume that most individuals will respond to their 1047297rst human encounter as an acutely stressful experience andtherefore interpret humans as potential predators [83] It is worth noting that species seemingly vary in how they dealwith exposure to a 1047297rst human (ie boldness at the species level [84]) Following this initial encounter if the response

to humans declines over repeated exposures then the animal may accurately be described as having habituated tohumans By contrast if the responsiveness is enhanced with repeated human exposure then the animal could bedescribed as having sensitized to humans Both habituation and sensitization occur over time and lead to differentdegrees of tolerance Because tolerance is measured at a point in time we can view it as a behavioral lsquostatersquo (see [85]for a systematic review of the use and misuse of habituation tolerance and sensitization) While some speciesappear to go through habituation-like processes when facing chronic human exposure other sensitize to increasedhuman presence This could happen even in closely related species For instance jackass penguins (Spheniscus

demersus) [86] and Magellanic penguins (Sphenicus magellanicus) [87] appear to habituate to human presencewhile yellow-eyed penguins (Megadyptes antipodes) sensitize and thus are disturbed by humans [10] Whichvariables drive habituation-like processes In the Magellanic penguins for instance the rate of habituation dependson the intensity of tourist visitation [88] a variable that also has been observed to drive habituation in other species(eg Mediterranean mou1047298on [70]) The type of stressor (ie approach or capture [89]) and the type of tourism arealso important factors that in1047298uence the degree of habituation (pedestrians cars bikes horses [90]) Spatiotemporalvariables such as time of the day season (in1047298uencing reproduction territoriality migration) and food availability havebeen identi1047297ed as important as have life history traits of a species such as the duration of parental investment andbody size [12] At the intraspeci1047297c level sex temperament and previous experience with humans affect whether

yellow-eyed penguins habituate or sensitize to repeated human visitation [91] Calm individuals were more likely tohabituate as were females





























consequences







Prey


predaon risk once




predators



nave predators

Process



predaon risk once




predators




migraon



predators enter

Predators


Shield

Response


Vigilance

Boldness

Vigilance

Boldness

Vigilance

Boldness

Vigilance

BoldnessFID FID FID










































PresenceFeeding

Decreased vigilance


Fewer predators

Increased predaon


Increased

aggressiveness

Bolder individuals

Decreased

fearfulness


(A)

B o l d n e s s

Habituated

Unhabituated

(B)

B o l d n e s s

Habituated

Unhabituated


i
























cheatingrsquo



Concluding Remarks




Acknowledgments




















Res 66 23ndash32




































16 413ndash419



















19 41ndash53




Sci 272 1433ndash1441









Ecol 21 913ndash918












25 1199ndash
































253 Springer











395 177ndash185


20 89ndash93








Evol 24 487ndash496




24 777ndash790


426ndash427 1ndash4
































consequences







Prey


predaon risk once




predators



nave predators

Process



predaon risk once




predators




migraon



predators enter

Predators


Shield

Response


Vigilance

Boldness

Vigilance

Boldness

Vigilance

Boldness

Vigilance

BoldnessFID FID FID










































PresenceFeeding

Decreased vigilance


Fewer predators

Increased predaon


Increased

aggressiveness

Bolder individuals

Decreased

fearfulness


(A)

B o l d n e s s

Habituated

Unhabituated

(B)

B o l d n e s s

Habituated

Unhabituated


i
























cheatingrsquo



Concluding Remarks




Acknowledgments




















Res 66 23ndash32




































16 413ndash419



















19 41ndash53




Sci 272 1433ndash1441









Ecol 21 913ndash918












25 1199ndash
































253 Springer











395 177ndash185


20 89ndash93








Evol 24 487ndash496




24 777ndash790


426ndash427 1ndash4










































PresenceFeeding

Decreased vigilance


Fewer predators

Increased predaon


Increased

aggressiveness

Bolder individuals

Decreased

fearfulness


(A)

B o l d n e s s

Habituated

Unhabituated

(B)

B o l d n e s s

Habituated

Unhabituated


i
























cheatingrsquo



Concluding Remarks




Acknowledgments




















Res 66 23ndash32




































16 413ndash419



















19 41ndash53




Sci 272 1433ndash1441









Ecol 21 913ndash918












25 1199ndash
































253 Springer











395 177ndash185


20 89ndash93








Evol 24 487ndash496




24 777ndash790


426ndash427 1ndash4
























cheatingrsquo



Concluding Remarks




Acknowledgments




















Res 66 23ndash32




































16 413ndash419



















19 41ndash53




Sci 272 1433ndash1441









Ecol 21 913ndash918












25 1199ndash
































253 Springer











395 177ndash185


20 89ndash93








Evol 24 487ndash496




24 777ndash790


426ndash427 1ndash4




























16 413ndash419



















19 41ndash53




Sci 272 1433ndash1441









Ecol 21 913ndash918












25 1199ndash
































253 Springer











395 177ndash185


20 89ndash93








Evol 24 487ndash496




24 777ndash790


426ndash427 1ndash4





























253 Springer











395 177ndash185


20 89ndash93








Evol 24 487ndash496




24 777ndash790


426ndash427 1ndash4





how nature-based tourism might increase prey vulnerability to predators

Documents