Como o turismo de natureza pode prejudicar animais

8/20/2019 Como o turismo de natureza pode prejudicar animais

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Review

How Nature-Based TourismMight Increase Prey

Vulnerability to PredatorsBenjamin Geffroy,1,2 Diogo S.M. Samia,3 Eduardo Bessa,4,5

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 inu-

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 tness, and thus the demographic trajectory 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 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 shi.

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 [5,6]. Nonetheless, althoughfrequent, tolerance is not a necessary outcome and the development of tolerance is inuencedby 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 modies 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 negativelyinuence behavioral responses to pre-dators. This could happen indirectly,where 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 Goiás,

CP. 131, 74001-970 Goiânia, Brazil4State University of Mato Grosso,

Tangará 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 & Evolution, Month Year, Vol. xx, No. yy http://dx.doi.org/10.1016/j.tree.2015.09.010 1© 2015 Elsevier Ltd. All rights reserved.

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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 couldalso modify community structure by affecting species distribution,diversity, 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] and

offspring provisioning [11]. To better understand how tolerance emerges and how it mayinuence tness, 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 (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 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 nonthreatening stimulus (humans).Importantly, the outcome of these interactions could then inuence the outcomes of predator–

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

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 term (i.e., 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, Paraná, Brazil6Department of Ecology and

Evolutionary Biology, University of

California, 621 Young Drive South,

Los Angeles, CA 90095-1606, USA

*Correspondence: [email protected]

(D.T. Blumstein).

Box 1. What Governs Habituation-like Processes?

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 dealwith exposure to a rst human (i.e., 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 ‘state’ (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 (Spheniscusdemersus) [86] and Magellanic penguins (Sphenicus magellanicus) [87] appear to habituate to human presence,while 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(e.g., Mediterranean mouon [70]). The type of stressor (i.e., approach or capture [89]) and the type of tourism arealso important factors that inuence the degree of habituation (pedestrians, cars, bikes, horses [90]). Spatiotemporalvariables such as time of the day, season (inuencing reproduction, territoriality, migration), and food availability havebeen identied as important as have life history traits of a species such as the duration of parental investment andbody size [12]. At the intraspecic 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 & Evolution, Month Year, Vol. xx, No. yy

mailto:[email protected]:[email protected]


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Domestication and Antipredator Behavior

Domestication involves cognitive processessuchas tameability and the reduction of aggression,fearfulness, 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 (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 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, and shorter tails) [16].

In salmonids, domestication also led to reduced physiological and behavioral responses topredators [17,18]. For instance, seventh generation juvenilesof domestic Atlantic salmon (Salmo

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

generation of hatchery-reared juveniles from wild salmon had a signicantly reduced antipreda-tor response, compared 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 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 (i.e., 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 inuence

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 density,handling, 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 , jaguarsPanthera 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

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 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

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 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 in

both 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 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 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, predator-rich environment [27].

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

consequences.

Urbanization and Antipredator Behavior

Characteristics 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 of circulating corticosteroids [31,32]. Species often have reduced ight initiation distances(FID) in urban areas when compared 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].

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

Transfer of habituaon

and inexperience with

nave predators

Process:

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


predaon risk once

tourists leave the place

(e.g., at night or winter)

Transfer of habituaonInexperience with nave

predators

Border of the shield not

well defined: depends on

prey’s 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 bold,or already bold animals are attracted to the city because of the human shield and habituation to humans. These animalswill sufferhigh predationrisk if predators enter thecity,since they areless alert. A human shieldalso exists(ii) outsidethe city(e.g.,in 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 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, 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 towns,then this would explain their higher FIDs (towards humans) in urban areas. Nevertheless, it isdif cult to disentangle causes from consequences since species with short FID (e.g., towardshumans) could also suffer higher predation 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 as a result

of 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 also more likelyto become successful urban colonizers [42]. However, two recent studies did not conrm theeffect of relative brain size on urbanization either at the intraspecic or 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 [37–39].

Human Shields around Urban AreasPredators can avoid areas with human presence as a result of the so-called ‘human shield’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 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 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, i.e., the statistical unit is ‘block ’ within one population), this is the rst, andpossibly the only, documented case of transfer of habituation between humans and nativepredators for fox squirrels in a eld setting [36].

Møller and Ibáñez-Álamo [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 dif cult to



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isolate. Is the relaxation of antipredator behavior (shorter FID) in urban areas attributable tohuman shields (Figure 1Bi,ii) 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 (e.g., 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 (i.e., 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 c asa proxy) also sheltered both pronghorn ( Antilocapra americana) and elk (Cervus elephus) frompredators in Grand Teton National Park [56]. This modied prey behavior: pronghorn and elk spent signicantly 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 (e.g., 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 (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. 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 issuf cient to either permanently reduce antipredator abilities or reduce them for a suf ciently 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 (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 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 and/or provisioning become bolder and/or more aggressive[1,5,6]. Can boldness and aggressiveness be repeatable over time and/or acrosscontexts? 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 hypothalamic–pituitary–adrenal (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

Humans Predator 1 Predator 2

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.



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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 dif cult to establish, since it would mean thatanimals that become bold and aggressive towards humans (e.g., through habituation) transfertheir habituation to real predators (Figure 1C). This pathway may seem unlikely at rst glance,because it would mean that humans are classied 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 [50,67]. 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 (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 norm.

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 2 A,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 who might alsobenet 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] caninuencehow an individual typically behaves, including howthey respond to novel situations. Naïve 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 (e.g., leads to a decrease of corticosteroids throughout ontogeny in response to tourism [64,87]). This highlights the importance of early experiencesin shaping behavioral traits (‘experience adaptive development’ or ‘experience adaptive programming’ for captiveindividuals [28]) that become progressively xed 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 (e.g., R = 0.84 – 0.92 in burrowing owls Athene cunicularia [98]). The emergence of suchpersonality traits hasbeenexplained in thecontext of tnesstrade-offs,whereby 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 behavioralsyndrome has adaptive consequences in one context but maladaptive consequences in another (e.g., with and withouta predator present), the term ‘behavioral spillover’ is used. North American shing spiders (Dolomedes triton) with highlevel of voracity in foraging (resulting in high tness) and mating contexts (resulting in low tness) were also bolder in acontext of a simulated predatory attack (resulting in low 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 ‘human-mediated behavioral spillover’.



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

could 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 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 – particularly tourists – 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 andinuence 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 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, 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 argument.In addition, wethankOdedBerger-

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

Boucharebhelpedin drafting the gures.B.G. is supportedby a CAPES-Ciência SemFronteiras, grant A045_2013. D.S.M.

S. is supportedby CAPES.E.B. wasfunded by FAPEMAT (Process 002.191/2007). D.T.B.is supportedby theUS National

Science Foundation (NSF).

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

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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 behavioralspillover, inuencing antipredatorbehavior, affected by predator origin(i.e., native or alien species)?

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

Given temporal variation in risk, howfast can antipredator behavior be lost,or 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?


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