predation study

ReviewHow Nature-Based TourismMight Increase PreyVulnerability to Predators[TD$FIRSTNAME]Benjamin [TD$FIRSTNAME.E] [TD$SURNAME]Geffroy [TD$SURNAME.E]Q1 ,1,2 [TD$FIRSTNAME]Diogo S.M. [TD$FIRSTNAME.E] [TD$SURNAME]Samia [TD$SURNAME.E],3 [TD$FIRSTNAME]Eduardo [TD$FIRSTNAME.E] [TD$SURNAME]Bessa[TD$SURNAME.E],4,5

and [TD$FIRSTNAME]Daniel T. [TD$FIRSTNAME.E] [TD$SURNAME]Blumstein [TD$SURNAME.E]6,*

Tourism can be deleterious for wildlife because it triggers behavioral changes inindividuals with cascading effects on populations and communities. Amongthese behavioral changes, animals around humans often reduce their fearful-ness and antipredator responses [4_TD$DIFF]towards humans. A straightforward predictionis that habituation to humans associated with tourism would negatively inu-ence reaction to predators. This could happen indirectly, where human pres-ence decreases the number of natural predators and thus prey become lesswary, or directly, where human-habituated individuals become bolder and thusmore vulnerable to predation. Building on ideas from the study of traits associ-ated with domestication and urbanization, we develop a framework to under-stand how behavioral changes associated with nature-based tourism canimpact individual tness, and thus [5_TD$DIFF] the demographic trajectory [6_TD$DIFF] of a population.

How Might Nature-Based Tourism Inuence 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 swimwith marinemammals, 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 sh[18_TD$DIFF]iQ2 .

However, these interactions between wildlife and humans, even when the welfare of animals isconsidered, often change[19_TD$DIFF] the behavior of wild animals. For example, it is well documented thatindividuals of many species that have benign interactions with humans undergo habituation-like processes leading to some degree of human tolerance [5,6]. Nonetheless, [20_TD$DIFF][21_TD$DIFF]althoughfrequent, tolerance is not a necessary outcome and the development of tolerance is inuencedby [22_TD$DIFF][23_TD$DIFF][24_TD$DIFF]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 avery popular leisure activity in the [7_TD$DIFF]pastyears and is a substantial conservationissue because it modies [8_TD$DIFF] the behavior [9_TD$DIFF]and community structure [10_TD$DIFF] of an animal.

Nature-based tourism might modifybehavior in ways similar to that seenin domestication and urbanization, aswell as modify [11_TD$DIFF] the population dynamics [12_TD$DIFF]of species.

Domestication and urbanization reducethe fearfulness and [13_TD$DIFF]antipredator beha-vior of animals around humans [14_TD$DIFF]attribu-table to both habituation [15_TD$DIFF]towardshumans anddisplacement of predators.

Nature-based tourism could negativelyinuence behavioral responses to pre-dators. This could happen indirectly,where human presence decreases thenumber of predators in a given area[16_TD$DIFF], andmore directly,where individuals becomebolder following habituation, resulting ina boldness syndrome that couldincrease vulnerability to predators.[17_TD$DIFF]

1Center of [1_TD$DIFF]Study of the [2_TD$DIFF]MeridionalAmazon, Federal University of MatoGrosso, Sinop, Brazil2INRA, UR1037 LPGP, FishPhysiology and Genomics, Campusde Beaulieu, 35000 Rennes, France3Laboratory of Theoretical Ecologyand Synthesis, Department ofEcology, Federal University of Gois,CP. 131, 74001-970 Goinia, Brazil4State University of Mato Grosso,Tangar da Serra, Mato Grosso, Brazil5Laboratory of Behavioral Ecology ofReproduction, State University ofPonta Grossa [3_TD$DIFF], Av. Gal. CarlosCavalcanti, 4748, 84030-900 PontaGrossa, Paran, Brazil

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events (e.g., [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 could alsomodify community structure by affecting species distribution,diversity [25_TD$DIFF], and richness [9].

The ultimate consequences of this increased tolerance to humans are diverse. Indeed, humanpresence has been shown to impair different tness-related traits such as reproduction [10] andoffspring provisioning [11]. To better understand how tolerance emerges and how it mayinuence tness, we need to step back and develop a more fundamental understanding ofhow 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 (e.g., 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 [26_TD$DIFF]spatiotemporal scales (i.e., local versus landscapes and evolu-tionary versus ephemeral), they all involve similar cognitive processes habituation or sensiti-zation leading to approach or avoidance [12] to the same [27_TD$DIFF]nonthreatening stimulus (humans).Importantly, the outcome of these interactions could then inuence the outcomes of predatorprey interactions. In this sense, habituation is often seen as synonymous with taming [1], as itwould increase [28_TD$DIFF] the ease of observation of animals by making them unnaturally tame toapproach by humans ([13], p. 35).[32_TD$DIFF]

We develop a framework that identies how antipredator behavior can be modied 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 (i.e., habituation) and longer [29_TD$DIFF] term (i.e., domestication)to those that occur [30_TD$DIFF] when animals interact with humans in both urban and more natural areas. [31_TD$DIFF] Ithighlights how selection for boldness, which might result from interacting with humans, canmake those individuals particularly susceptible to predation.

6Department of Ecology andEvolutionary Biology, University ofCalifornia, 621 Young Drive South,Los Angeles, CA 90095-1606, USA

*Correspondence:. [email protected](D.T. Blumstein).

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Box 1. What Governs Habituation-like Processes?

[146_TD$DIFF]We assume that most individuals will respond to their rst human encounter as an acutely stressful experience andtherefore interpret humans as potential predators [83]. It is worth noting that species seemingly vary in how they deal with [132_TD$DIFF]exposure [133_TD$DIFF] to a rst human (i.e., boldness at the species level [134_TD$DIFF] [84]). Following this initial encounter, if the response tohumans 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 [135_TD$DIFF] over time and lead [136_TD$DIFF] to differentdegrees of tolerance. Because tolerance ismeasured at a point in time, we can view it as a behavioral state (see [137_TD$DIFF][85] for asystematic review of the use and misuse of habituation, tolerance[138_TD$DIFF], and sensitization). While some species appear to gothrough habituation-like processes when facing chronic human exposure, other sensitize to increased human presence.This could happen, even in closely related species. For instance, jackass penguins (Spheniscus demersus) [86] andMagellanic penguins (Sphenicus magellanicus) [87] appear to habituate to human presence, while yellow-eyed penguins(Megadyptes antipodes) sensitize and thus are disturbed by humans [10]. Which variables drive habituation-likeprocesses? In the Magellanic penguins, for instance, the rate of habituation depends on the intensity of tourist visitation[88], a variable that also has been observed to drive habituation in other species (e.g., Mediterranean mouon [70]). Thetype of stressor (i.e., approach or capture [139_TD$DIFF] [89]) [140_TD$DIFF] and the type of tourism are also important factors that inuence the degreeof habituation (pedestrians, cars, bikes, horses [90]). [141_TD$DIFF]Spatiotemporal variables such as time of the day, season(inuencing reproduction, territoriality, migration) [142_TD$DIFF], and food availability have been identied as important as have[143_TD$DIFF] lifehistory traits [144_TD$DIFF] of a species such as the duration of parental investment and body size [12]. At the intraspecic level, sex,temperament [145_TD$DIFF], and previous experience with humans affect whether yellow-eyed penguins habituate or sensitize torepeated human visitation [91]. Calm individuals were more likely to habituate, as were females.

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Domestication and Antipredator BehaviorDomestication involves cognitive processes such as tameability and the reduction of aggression,fearfulness, and sensitivity to environmental variation [14]. These processes also occur whenanimals interact with humans in the wild. Domestication can lead to a progressive loss ofantipredator behavior (e.g., [15]). An iconic study of domestication comes from Belyaev'spioneering work on silver foxes (Vulpes vulpes). After almost 35 generations of captive handling,80% of the handled foxes were signicantly more docile and responded less fearfully to novelstimuli than [33_TD$DIFF]nonhandled control lines [16]. Importantly, these behavioral responses were trans-duced at the physiological level (there was a decrease of corticosteroid production) andaccompanied by important physical changes (loss of pigmentation, development of oppyears [34_TD$DIFF], and shorter tails) [16].

In salmonids, domestication also led to reduced physiological and behavioral responses topredators [17,18]. For instance, seventh generation juveniles of domestic Atlantic salmon (Salmosalar) had reduced heart rates and lower ight responses to simulated predator attacks than wildsalmon [17]. More importantly, when placed in [35_TD$DIFF]seminatural conditions, the rst and the secondgeneration of hatchery-reared juveniles from wild salmon had a signicantly reduced antipreda-tor response, compared [36_TD$DIFF]with their wild counterparts [18].

Similarly, a study recently reported that after only one generation of laboratory breeding,stickleback (Gasterosteus aculeatus) were much less responsive to simulated predatory attackwhen compared [37_TD$DIFF]with their wild counterparts [19]. Studies [38_TD$DIFF]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 (i.e., early in the domesticationprocess). Nonetheless, we also may have strongly directed responses that are associated with [39_TD$DIFF]the history [40_TD$DIFF] of a population [19], and that might persist under relaxed selection [20].

Parental rearing patterns, which sometimes change under domestication, can also inuenceantipredator behavior. For instance, when compared [41_TD$DIFF]with goose-raised geese, [42_TD$DIFF]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 density,handling [43_TD$DIFF], 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 modied how they copedwith stressful situations in adulthood [22].

Livestock depredation by wild mammalian predators (e.g., pumas Puma concolor, jaguars [44_TD$DIFF]Panthera onca, and wolves Canis lupus) has traditionally been associated with distance tothe forest edge, cattle density, and cattle age [23,24]. However, recent evidence also notedthat selection for docility impairs antipredator behavior when facing wolves [25]. It should benoted that this behavior was not assessed directly in this study, but rather indirectly throughthe facial hair whorl pattern [25], which is a phenotypic trait associated with vigilance incattle.

Hence, there is evidence that domestication directly selects for less wary and bolder individualsthat could then suffer higher predation in the wild [45_TD$DIFF] (Figure 1A [46_TD$DIFF], Key Figure). This could also haveconsequences for animal conservation since early experience (or lack of it) with humans ornatural predators can also inuence 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 inuence survival in released animals. Bold (including those that were bold [47_TD$DIFF]

GlossaryBehavioral spillover: a suite ofcovarying behaviors that is adaptivelyselected in one context butmaladaptive in another context [79].Behavioral syndrome: Q11a suite ofcorrelated behaviors across situations[80].Boldness: the way in which anindividual and/or 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 localpeople.Flight initiation distance (FID): thedistance between the predator orthreatening stimulus and prey whenthe prey begins to ee [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 inboth relatively wild and urban areas.Human-mediated behavioralspillover: when animals habituatedto humans benet by exhibitingbehaviors in close vicinity withtourists (either to acquire food orreceive passive protection frompredators), but these behaviorsbecome maladaptive when humansleave the area (e.g., the behaviorsmight increase predation risk).Individual behavioral reactionnorm: the set of behavioralphenotypes that a single individualproduces in a given set ofenvironments [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 ofnative predators decreases in urbanareas, reducing predation risk and,consequently, the antipredatorbehavior of their prey [46].

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towards humans) captive-bred swift foxes (Vulpes velox) suffered much higher mortality thantheir shyer conspecics upon release to a natural, [48_TD$DIFF]predator-rich environment [27].

To conclude, antipredator responses may be modied by experience and thus the specicresponse to predators could be lost [49_TD$DIFF] or modied by domestication [50_TD$DIFF] (Figure 1A [51_TD$DIFF]). Such changesmay happen quickly, within a single generation (this is also referred to as experienceadaptive development or experience adaptive programming; see [28]), and have tnessconsequences.

Urbanization and Antipredator BehaviorCharacteristics of Antipredator ResponsesNot all species successfully colonize urban habitats [29,30]. 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 ofcirculating corticosteroids [31,32]. Species often have reduced ight initiation distances(FID) in urban areas when compared [52_TD$DIFF]with rural areas [33], and the presence of articial feedingsites also can reduce FID [34]. Importantly, FID is one metric by which individuals (and species)can be compared with respect to their boldness [35].[61_TD$DIFF]

Urbanization: the process by whichanimals and plants modify theirbehavior and physiology to urbanenvironments, with the change fromancestral rural to recent urbanenvironments being the relevanttransition [53].

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Figure 1. Animals Respond to Human Presence along a Gradient from Domestication to Nature-BasedTourism. [167_TD$DIFF](A) During [168_TD$DIFF]domestication animals become tamed and remain close to humans. This involves a decrease offearfulness at both [169_TD$DIFF]behavioral and [170_TD$DIFF] physiological levels. Such animals are bold towards humans and can suffer enhancedpredation risk if released in natural areas. [171_TD$DIFF](B) During [172_TD$DIFF]urbanization (i) within the city, animals can either become bold, oralready bold animals are attracted to the city because of [173_TD$DIFF]the human shield and habituation to humans. These animals willsuffer high predation risk if predators enter the city, since they are less alert. A human shield also exists (ii) outside the city (e.g., in rural areas), such that the [174_TD$DIFF] antipredator vigilance [175_TD$DIFF]of a prey is attenuated and animals will suffer predation according totheir risk perception. [176_TD$DIFF] (C) When [177_TD$DIFF]tourists contact wild animals, they create a temporal shield and a boldness syndrome mainly [178_TD$DIFF]as a result of habituation (through presence alone and/or 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.


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When approached by humans, [53_TD$DIFF]the average FID [54_TD$DIFF] 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 [55_TD$DIFF]with rural areas [31], suggesting thatboldness is associated with urbanization. It is worth noting that some species inhabiting urbanenvironments have greater FIDs compared [56_TD$DIFF]with their rural counterparts, but these urbanpopulations suffer higher predation by sparrowhawks (Accipiter nisus) when compared [57_TD$DIFF]withrural populations [37]. If these species are preferentially targeted by sparrowhawks in towns,then this would explain their higher FIDs ([58_TD$DIFF]towards humans) in urban areas. Nevertheless, it isdifcult to disentangle causes from consequences since species with short FID (e.g., [59_TD$DIFF]towardshumans) could also suffer higher predation [60_TD$DIFF]resulting from their lower overall reduced fearfulness[38,39]. 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 [62_TD$DIFF]as a resultof rapid behavioral adjustments [40]. Using relative brain size as a proxy for behavioral exibility[41], one study found that brained species are highly variable in their FIDs and are alsomore likelyto become successful urban colonizers [42]. However, two recent studies did not conrm theeffect of relative brain size on urbanization either at the [63_TD$DIFF]intraspecic or [64_TD$DIFF]interspecic level [43,44].Regardless, living in urban areas is associated with a number of cognitive modications. Forexample, the structure of communication is modied [30], animals encounter new foragingopportunities [45], and animals reduce their FID in response to humans [3739].

Human Shields around Urban AreasPredators can avoid areas with human presence [65_TD$DIFF]as a result of the so-called human shieldeffect [46]. This human shield effect is part of the safe-habitat hypothesis [47] that describeshow predators are more likely to be absent in urban areas. Such safe habitats have a variety ofconsequences. For instance, nest predation is drastically decreased inside barns and shedswhere predators fear to go compared [66_TD$DIFF]with adjacent outdoor areas [48]. Human shields and safehabitats [67_TD$DIFF]effects are important because they can provide a relatively safe area for potential prey[49], making them less vigilant and more likely to allocate their time on tness-enhancingactivities, such as foraging [50]. Human shields can partially explain why prey could be saferin urban areas if urbanization reduces predator presence and diversity [51] and also providesrefuge [68_TD$DIFF] 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 tend tobe 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 betransferred to genuine predators [69_TD$DIFF] (Figure 1Bi). This question has been investigated in fox squirrelswhere individuals that were part of a population habituated to human presence (shown by adecreased FID) were also less responsive to different predator vocalizations, compared [70_TD$DIFF]withrural fox squirrels [36]. Although this result should be interpreted with caution ([71_TD$DIFF]as a result of [72_TD$DIFF]pseudoreplication, i.e., the statistical unit is block within one population), this is the rst, andpossibly the only, documented case of transfer of habituation between [73_TD$DIFF]humans and nativepredators for fox squirrels in a eld setting [36].

Mller and Ibez-lamo [53] also found that urban individuals of 15 bird species wriggled,pecked, and bit less when removed from mist nets than rural individuals, suggesting relaxedantipredator behavior in cities. The mechanisms underlying these responses are difcult to

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isolate. Is the relaxation of antipredator behavior (shorter FID) in urban areas [74_TD$DIFF]attributable tohuman shields [75_TD$DIFF](Figure 1Bi,[76_TD$DIFF]ii) and thus reduced predation risk? Or, is this change caused byhabituation to [77_TD$DIFF]nonthreatening stimuli? It is possible that both processes occur simultaneouslyand hence increase prey vulnerability to predators [78_TD$DIFF] (Figure 1B). Conducting experiments withpredators that are recolonizing urban areas (e.g., foxes in London [54]) might offer an opportunityto disentangle these mechanisms.

Tourist Exposure and Antipredator Behavior[83_TD$DIFF]Human presence might thus act in two [79_TD$DIFF]nonmutually exclusive ways: (i) indirectly, by creating ahuman shield that relaxes antipredator behavior of prey [80_TD$DIFF]; and (ii) directly, such that docility andboldness emerge from repeated interactions with [81_TD$DIFF]nonthreatening humans and these responsesare then transferred to other more-threatening sources (i.e., genuine predators or wildlifepoachers) [82_TD$DIFF]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 [84_TD$DIFF](Figure 1C). Nonetheless, extensive human visitation to a wild location could create a temporaryhuman shield. In this sense, human presence has been shown to reduce the probability ofencounters between vervet monkeys (Chlorocebus pygerythrus) and predatory leopards(Panthera pardus) [55]. In another, more recent example, tourist presence (using car trafcas a proxy) also sheltered both pronghorn (Antilocapra americana) and elk (Cervus elephus) frompredators in Grand Teton National Park [56]. This modied prey behavior: pronghorn and elkspent signicantly less time in alert postures, more time feeding [85_TD$DIFF], and were in smaller groups inthe areas with many tourists compared [86_TD$DIFF]with the areas with fewer tourists [56]. Human presencealso directly affects risk perception to terrestrial predators in samango monkeys (Cercopithecusmitis 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 thattemporarily live without predators have reduced antipredator defenses (Box 2). This might leadto increased predation when humans leave the place (e.g., at night or winter; the indirectpathway in Figure 2).

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Box 2. Permanent versus Temporary Human Shields[147_TD$DIFF]

[150_TD$DIFF]Tourist or other human presence can create a human shield (habitat free of predators) that can relax antipredatorbehavior during [148_TD$DIFF] the lifetime[149_TD$DIFF] of an individual. Antipredator behavior in predator-free environments is often lost [92] andcould occur relatively quickly (e.g., 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. Similarly,urbanization 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. [151_TD$DIFF]This has been seen duringperiodically shing closures where individuals decrease their wariness (as shown by shorter FIDs) and suffer highercapture rates when shing is reinstated [95], as well as when mammal poachers are temporarily absent. With respect tohuman shields linked to tourism, the core question is to determine whether the temporary presence of humans issufcient to either permanently reduce antipredator abilities [152_TD$DIFF] or reduce them for a sufciently long time so that thepopulation suffers. [153_TD$DIFF]

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 ofnature-based tourism usually changes according to the season, and predator presence can vary accordingly. Forinstance, animals might not encounter usual threats for some months (e.g., during spring and summer tourist seasons),while they would have to face high predation risk in other periods (e.g., during the fall and winter). Hence, the mainquestion is to understand how fast antipredator behavior can be lost, or reduced, under temporarily relaxed predationpressure.


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Increased Tolerance to Humans: A Direct PathwayAs shown by the urbanization examples described [87_TD$DIFF][88_TD$DIFF]earlier, the presence of humans can haveunanticipated effects on prey antipredator behavior, even in the wild. For instance, some animalshabituated to tourism presence and/or provisioning [89_TD$DIFF] become bolder and/or more aggressive[1,5,6]. Can boldness and aggressiveness be repeatable over time and/or across contexts? Thiskey question has been partly answered by studies that show repeatable behavioral traits [58,59]and by those showing that animals reduce exibility with experience [60,61]. If the developmentof personality is affected by early experiences, and animals then nd 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 [90_TD$DIFF]hypothalamic[91_TD$DIFF]pituitaryadrenal (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].

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Figure 2. The Link between Intensive Wildlife-Based Tourism and Natural Predation. Both indirect (throughdecreasing vigilance) and direct (through increased boldness) [179_TD$DIFF]pathways would enhance predation risk. The indirectpathway (salmon colored) assumes a process related to relaxed selection where individuals found in [180_TD$DIFF]predator-free habitatslose (previously learned or even evolved) defenses against predators temporally pushed away. The direct pathway (bluecolored) assumes that docility and boldness emerge from interaction with [181_TD$DIFF]nonthreatening humans and these are transferredwhen encountering more-threatening species. (A) Similar behavioral reaction norms for [182_TD$DIFF]animals unhabituated and habi-tuated to human presence as a function of different contexts (humans or predator types). (B) Different behavioral reactionnorms for animals unhabituated and habituated to human presence as a function of different contexts (humans or predatortypes). Note that habituated animals are bolder [183_TD$DIFF]towards potential threats, either genuine predators or wildlife poachers.


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While boldness could be the result of human habituation, and behavioral spillover could enhancepredation risk, the direct link between both is more difcult to establish, since it would mean thatanimals that become bold and aggressive [93_TD$DIFF]towards humans (e.g., through habituation) transfertheir habituation to real predators [94_TD$DIFF] (Figure 1C). This pathway may seem unlikely at rst glance,because it would mean that humans are classied into the same category as [95_TD$DIFF]nonhumanpredators and we know that many species are able to discriminate predators from [96_TD$DIFF]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 [50,67]. Nevertheless, neither of these studies formallyQ3 tested for atransfer of habituation, but rather capitalized on how individuals around humans were moretolerant of humans and then asked how the ability to discriminate between potential predatorsand [97_TD$DIFF]nonpredatory species was effected by human exposure. As with squirrels that were lessresponsive to predator vocalizations in urban areas [36], a transfer of habituation can also haveoccurred in blackbirds (Turdus merula) exposed to tourists in parks [68]. Blackbirds decreasedtheir FID with increased exposure to humans (consistent with [98_TD$DIFF]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 [99_TD$DIFF]pseudoreplication (i.e., 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 normQ4 .Specically, 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 2A,B) 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 whomight alsobenet from tourist-habituated wildlife. It is not currently clear whether or not animals are able to

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Box 3. A Human-Mediated Behavioral Spillover

[159_TD$DIFF]Both environmental [96] and early social experiences [97] can inuence how an individual typically behaves, including howthey respond to novel situations. Nave juveniles generally are more wary and have greater FIDs in response to humansthan adults [36], suggesting an habituation-like process where adult individuals became less wary after having multipleencounters with [154_TD$DIFF]nonthreatening stimuli, such that their reaction norm [155_TD$DIFF]decreases over time (e.g., [156_TD$DIFF]leads to a decrease ofcorticosteroids throughout ontogeny in response to tourism [157_TD$DIFF] [64,87]). This highlights the importance of early experiencesin shaping behavioral traits (experience adaptive development or experience adaptive programming for captiveindividuals [158_TD$DIFF] [28]) that become progressively xed with age (see [61] and references therein). [166_TD$DIFF]

Antipredator behavior, such as FID, could be considered a personality trait in some species since there can be a very hightemporal repeatability (e.g., R = 0.84 0.92 in burrowing owls Athene cunicularia [98]). The emergence of suchpersonality traits has been explained in the context of tness trade-offs, whereby a given behavior could be advantageousin [160_TD$DIFF]one situation while it would not be in another. In Namibian rock agamas (Agama planiceps), bolder males had greateraccess to food, but they also suffered increased tail loss when compared [161_TD$DIFF]with shyer individuals [99]. When a syndromehas adaptive consequences in one context but maladaptive consequences in another (e.g., with and without a predatorpresent), the term behavioral spillover is used. [164_TD$DIFF] North American shing spiders (Dolomedes triton) with high level ofvoracity in foraging (resulting in high tness) andmating contexts (resulting in low tness) were also bolder in a context of asimulated predatory attack (resulting in low tness) [79]. In [165_TD$DIFF]summary, if habituation to humans leads to a general decreasein fearfulness, this habituation might also lead to inappropriate (perhaps fatal) behavior in other contexts, such as beingbold in the presence of predators, resulting in a human-mediated behavioral spillover.


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distinguish 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)are able to distinguish hunters (Maasai men) from [100_TD$DIFF]nonhunters (Maasai women and children)based on their voices [69]. Mouon (Ovis gmelini musimon) readily identify noisy hunting withhounds [70], while more silent speargunsmight not be well detected by sh [71]. Regardless, wecould view wildlife poaching as a form of cheating in cases where a population has habituatedto benign human presence and then individuals are caught off guard by a poacher. Viewed thisway, a small degree of very successful poaching can be tolerated before individuals in apopulation learn to associate humans with enhanced risk resulting in higher capture rates[72,73]. For instance, gorillas (Gorilla gorilla graueri) habituated to tourist presence ed moreslowly and did not readily attack or hide, when a poacher approached, when compared [101_TD$DIFF]withnonhabituated [102_TD$DIFF]gorillas [72]. This has also been observed for wild Barbary macaques (Macacasylvanus),which are extremely habituated tohumans, andwhichare easy targets for poachers [73].

Concluding Remarks[108_TD$DIFF]We know that humans are able to drive rapid phenotypic change in other species [74]. Ifindividuals selectively habituate to humans particularly tourists and if invasive tourismpractices enhance this habituation, we might be selecting for or creating traits or syndromesthat have unintended consequences, such as increased predation risk (Figure 2). Even a smallhuman-induced perturbation could affect the behavior or population biology of a species andinuence the [103_TD$DIFF] function[104_TD$DIFF] of the species in its community [75]. Such cryptic function loss and theassociated reduction in functional diversity are considered to be among the most signicantconcerns for ecosystem stability [75]. Exposure to humans can also reduce phenotypic variationand behavioral plasticity. Since behavioral plasticity might mirror genetic diversity, ecotourismcould also drive the loss of genetic diversity. The effect might even be greater if human-linkedperturbations affect keystone species or individuals [76,77]. Owing to the plethora of impactsnature-based tourism has on wildlife, it could well be added to the list of drivers of human-induced rapid environmental change (HIREC), which already includes habitat change, pollution,exotic species, human harvesting[105_TD$DIFF], and climate change [78]. Our review highlights numerousunanswered questions ([106_TD$DIFF]see Outstanding [107_TD$DIFF]Questions) that could be tested with the ultimate goalof better understanding whether and how habituation to human presence creates deleteriouseffects to wildlife.

Uncited referencesQ6[8082].

AcknowledgmentsEarly discussions with Michael Clinchy and Liana Zanette helped us clarify our argument. In addition, we thank Oded

Tal-Berger and three anonymous reviewers who provided extensive feedback that signicantly improved this manuscript.

Amine Bouchareb helped in drafting the gures. B.G. is supported by a CAPES-Cincia Sem Fronteiras, grant A045_2013.

D.S.M.S [114_TD$DIFF]. is supported by CAPES. E. [115_TD$DIFF]B. was funded by FAPEMAT (Process 002.191/2007). D.T.B. is supported by the US [116_TD$DIFF]

National Science Foundation (NSF [117_TD$DIFF]Q7 ).

Resourcesi www.turismo.gov.br/turismo/noticias/todas_noticias/20131112.html

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How often does habituation explaintolerance?

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Which intrinsic factors explain variationbetween species in human-orientedboldness? In other words, why dosome species acclimate well to humanpresence while others avoid humans? [112_TD$DIFF]

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What are the evolutionary responses ofanimals to nature-based tourism?


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How Nature-Based Tourism Might Increase Prey Vulnerability to PredatorsHow Might Nature-Based Tourism Influence Wildlife Behavior?How do Animals Respond to Humans?Domestication and Antipredator BehaviorUrbanization and Antipredator BehaviorCharacteristics of Antipredator ResponsesHuman Shields around Urban AreasEcological Consequences: Two Causes, One Possible Outcome

Tourist Exposure and Antipredator BehaviorHuman Shields in the Wild: An Indirect PathwayIncreased Tolerance to Humans: A Direct Pathway

Concluding RemarksUncited referencesAcknowledgmentsResourcesReferences

predation study

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