Species-Specific Responses to Tourist Interactionsby White-Faced Capuchins (Cebus imitator)andMantled Howlers (Alouatta palliata) in a CostaRican Wildlife Refuge

Tracie McKinney

Received: 18 July 2013 /Accepted: 28 December 2013 /Published online: 15 March 2014# Springer Science+Business Media New York 2014

Abstract Ecotourism shows great potential for primate conservation, but furtherinvestigation through an ethnoprimatological lens is vital to understanding species-specific variation in human–nonhuman primate interactions at ecotourism sites. Thisstudy measured the rates and types of human–monkey interactions, the participantsin these encounters, and the association between tourist numbers and interaction rateswith white-faced capuchin monkeys (Cebus imitator) and mantled howlers (Alouattapalliata) at the Curú Wildlife Refuge in western Costa Rica. I collected data through15-min all-occurrence samples for human–monkey interactions between January2006 and December 2007. I recorded and analyzed a total of 1949 discrete interac-tions, representing one tourist group and one non-tourist group for each species. Forboth species, tourist groups showed more varied and more intense—but not morefrequent—human–monkey interactions than the non-tourist groups. White-facedcapuchins differed from mantled howlers in their greater frequency and more vari-able forms of human–monkey interactions. White-faced capuchins also showed amore gregarious pattern of interactions than mantled howlers, with most capuchininteractions being initiated by the monkeys and involving multiple actors. Althoughmantled howler human interaction rates correlated positively with levels of humantraffic, white-faced capuchins did not show this relationship. These findings dem-onstrate that the differences in human–monkey interactions across species are animportant consideration for the management of primate tourism sites. This studysuggests that species-specific guidelines for ecotourism would reduce visitor impacton nonhuman primates.

Keywords Alouatta .Cebus . Conservation . Ecotourism . Ethnoprimatology

Int J Primatol (2014) 35:573–589DOI 10.1007/s10764-014-9769-1

T. McKinney (*)Sixth Form Academy, City of Bristol College, St. Stephen’s Road, Soundwell, Bristol BS16 4RL, UKe-mail: Tracie.Mckinney@cityofbristol.ac.uk

Introduction

Ethnoprimatology is an emerging area of focus for biological anthropologists. Asoriginally conceived by Sponsel (1997), ethnoprimatology centers on human–nonhu-man primate relationships. Though this interface has been within the field primatolo-gists’ attention for many years, human–nonhuman primate interactions have beenconsidered primarily in terms of conflict paradigms, such as crop-raiding (Hill 2005;Strum 2010), bushmeat (Chapman and Peres 2001; Cowlishaw and Dunbar 2000), andpublic health risk (Singla et al. 1997). Ethnoprimatology today has broadened its scope,as all living nonhuman primate populations have been or are currently influenced insome way by human actions (Fuentes 2012; Struhsaker 1999). Instead of viewinghuman–nonhuman primate interactions as a reflection of some “disturbed” or “imbal-anced” state, ethnoprimatology recognizes humans as an integral part of the ecosystemand an influential factor in most nonhuman primate habitats (Fuentes and Hockings2010; Pavelka 2002).

An ethnoprimatological approach is particularly beneficial when considering theconservation and management of wild primate populations. Habitat change and thegrowth of ecotourism affect primates living within protected areas, as well as thosepopulations in more disturbed landscapes. In many cases, sustainable primate conser-vation programs depend on reaching a delicate compromise concerning the primates’dietary and spatial needs, human economic priorities, and complex use of sharedlandscapes (Lee 2010; Singh and Rao 2004). A broader understanding of these realitiesof primate ecology will reduce conflict at the human–nonhuman primate interface andwill improve the efficacy and sustainability of primate management efforts.

One of the key components of primate management in habitat countries, and animportant arena for ethnoprimatology, is ecotourism. The term is loosely defined, butecotourism generally refers to any nature-based tourism that incorporates an educa-tional or environmentally sustainable mission (Horton 2009; Krüger 2005). Visitoraccess to wild primates can provide public education about wildlife conservation aswell as an economic incentive for the local community to maintain the native habitat;both are key tools for conservation efforts. However, the effects of ecotourism onprimates remain poorly understood, and researchers report a discrepancy between theintended goals of ecotourism and its consequences for wildlife (Krüger 2005; López-Espinosa de los Monteros 2002; Treves and Carlson 2012). For example, researchsuggests that close interaction with humans affects substrate and home range use(Altmann and Muruthi 1988; De la Torre et al. 2000; Grossberg et al. 2003;Hoffman and O’Riain 2011), alters diet and foraging behaviors (McKinney 2011;Riley 2007; Saj et al. 1999; Unwin and Smith, 2010), elevates stress hormone levels(Behie et al. 2010; Maréchal et al. 2011), and increases the risk of monkey bites anddisease transmission (Brennan et al. 1985; Chapman et al 2005; Fuentes and Gamerl2005; Muehlenbein et al. 2010). The cumulative effects of interactions associated withprimate tourism are difficult to quantify, but we must consider this impact if we hope toconduct ethical, sustainable wildlife tourism.

Though there has been little formal investigation into the effects of tourism acrossspecies, sympatric primates in other anthropogenic landscapes show species-specificresponses to disturbance. Both rhesus macaques (Macaca mulatta) and Hanumanlangurs (Presbytis entellus), for example, are found within anthropogenic landscapes

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in India, but the Hanuman langur appears to be more heavily affected by the distur-bance, resulting in decreased population density (Ross et al. 1993). In Costa Rica,mantled howlers (Alouatta palliata) and white-faced capuchins (Cebus imitator) areboth commonly found in agricultural and tourist areas, yet squirrel monkeys (Saimirioerstedii) and black-handed spider monkeys (Ateles geoffroyi) are restricted to largeunbroken forests (Zaldívar et al. 2004). The robust literature concerning primates inagroecosystems and other anthropogenic habitats is outside the scope of this article, butthe ability of primate taxa to persist in such environments is heavily dependent on theirlocomotor, activity, and dietary patterns (Cowlishaw and Dunbar 2000; Estrada et al.2012; Michalski and Peres 2005; Singh and Rao 2004; Sorensen and Fedigan 2000).

Understanding which individuals within a group are most likely to participate ininteractions, and whether those interactions are initiated by the animals or by humans,is another important component to species-appropriate management of primate tourism.Studies involving Cebus and Macaca in primate tourism sites note that human–nonhuman primate interactions are usually initiated by visitors (Hsu et al. 2009;McCarthy et al. 2009; Sabbatini et al. 2006). Other studies report observations of paidnature guides clapping, “howling,” and making other noises to elicit a response fromthe monkeys (Grossberg et al. 2003; Treves and Brandon 2005). These actions validatevisitors’ attempts to interact with the wildlife and can lead to further problematicbehaviors by tourists. Few studies have examined age-class interactions, but it hasbeen noted that tourists are particularly attracted to young animals (O’Leary and Fa1993). Young animals living in close proximity to human disturbance are exposed topeople from birth. The acceptance by the adult members of their group of closeassociations with people aids in the habituation of the infants (Jack et al. 2008),increasing the likelihood of future cross-species interactions for these young animals.

Many sites provide basic measures, such as instructional brochures or signage, toreduce the impact of visitors (Cowlishaw and Dunbar, 2000; Fuentes et al. 2007;Muehlenbein et al. 2010). Some sites also manage visitors by limiting the times of dayin which primate tourism is permitted, maintaining a maximum number of viewings perday, or limiting tour group size (Berman et al. 2007; Klailova et al. 2010; Muehlenbeinet al. 2010; Nakamura andNishida 2009). It is reasonable to expect that animals withmoreopportunities for interaction will engage with humans at higher frequencies. However,many primates alter ranging patterns to avoid humans (De la Torre et al. 1999; Grossberget al. 2003; Treves and Brandon 2005), so it is plausible that primates will withdraw frominteractions if they feel threatened and this expected relationship will be absent. If thenumber or frequency of human visitors correlates directly with the frequency and type ofhuman–monkey interactions, it may be possible to define a baseline level of visitorpresence that triggers avoidance behaviors, mild interactions, or interspecies conflict.

To explore the types, intensity, and potential effects of interactions in an ecotourismcontext, I studied the interactions between tourists and two species of neotropicalmonkeys living within a small Costa Rican wildlife refuge. White-faced capuchins(Cebus imitator) and mantled howlers (Alouatta palliata) are commonly encounteredspecies in wildlife tourism areas throughout Central America. Neither species is endan-gered, but both face pressures associated with increasing human encroachment (Arroyo-Rodríguez and Mandujano 2006; Fragaszy et al. 2004). Human–nonhuman primateinteraction studies to date have been dominated by Macaca (Fuentes and Gamerl 2005;Hsu et al. 2009; Maréchal et al. 2011; Riley 2007; Unwin and Smith 2010), Papio

White-Faced Capuchin and Mantled Howler Responses to Ecotourism 575

(Altmann and Muruthi 1988; Hoffman and O’Riain 2011; Strum 2010) andChlorocebus(Brennan et al. 1985; Saj et al. 1999) – all genera that share withCebus variable diets andterrestrial locomotor patterns. Research on human–nonhuman primate interactions intaxa without these key characteristics—such as Alouatta—is therefore necessary forunderstanding the range of responses to human pressure across the primate order.

The literature suggests that the more omnivorous diet, smaller body size, and moreterrestrial patterns of white-faced capuchins, as compared to mantled howlers, maypromote a greater acceptance of tourist disturbance (Cowlishaw and Dunbar 2000;Estrada et al. 2012; Sorensen and Fedigan 2000). Based on this literature, and on theresults of a short pilot study, I predicted that:

& White-faced capuchins will engage in more frequent interactions with touriststhan will mantled howlers, owing to their more active daily pattern and explor-atory foraging style (Fragaszy et al. 2004;Milton 1980; Pavelka andKnopff 2004;Rose 1998).

& Most interactions between tourists and the monkeys will be initiated by people.During a brief pilot study, I observed that the majority of interactions betweentourists and the monkeys appeared to be initiated by humans. I also witnessedguides attempting to interact with the monkeys during their tours.

& Juvenile individuals will participate in interactions more often than adults, be-cause juvenile monkeys tend to be more playful and explorative than adults(Bezanson 2009).

& The frequency of interactions will be directly related to human presence. Whengreater numbers of tourists are present, either simultaneously or throughout the day,there will be more opportunities for human–nonhuman primate interactions.

Methods

Study Site and Population

Curú Wildlife Refuge (9°47’43.69”N, 84°55’15.01”W) is a small, privately ownedhacienda and wildlife refuge on the southern tip of the Nicoya Peninsula in westernCosta Rica. Approximately one-third of the 1492-ha property is devoted to cattlepasture and small plantations of mango (Mangifera indica), banana (Musa acuminata),soursop (Annona muricata), guava (Psidium guajava), and African oil palm (Elaeisguineensis). The remaining two-thirds of the property retain its natural vegetation. Thearea is characterized by rare dry/transitional moist tropical forest (Herzog and Vaughan1998; Timm et al. 2009), and encompasses microhabitats such as mangrove swamp,primary and secondary tropical forest, and beach/marine ecosystems. Despite its smallsize, the varied microhabitats within Curú yield high biological diversity, with some500 plant, 230 birds, and 79 mammal species identified to date (Baker and Schutt2005). The refuge ranges from sea level to an elevation of ca. 155 m, and has twodistinct annual seasons: rainy season from May to October, and dry season fromNovember to April. Temperatures range from 20 to 35 °C, with an annual mean of28 °C. Rainfall averages 1260 mm/yr (Instituto Meteorológico Nacional 2008).

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In recent years tourism has overtaken agricultural activities as the primary source ofincome for Curú (Baker and Schutt 2005). The refuge hosts roughly 10,000 interna-tional and Costa Rican visitors annually (F. Schutt, pers. comm.). Most are day visitorswho take private or guided hikes along one of the eight hiking trails winding throughmangroves and forested areas of the refuge. One well-maintained dirt road crosses therefuge for a distance of ca. 3 km, bringing regular vehicular and foot traffic. Theproperty also houses six tourist cabins, a dining hall, a gift shop, and a family residence,all of which are sites of regular human activity. Curú management provisions monkeysto ensure that the monkeys visit tourist-heavy areas regularly, but discourage touristsfrom feeding or approaching the monkeys.

I chose four monkey groups ranging entirely within the boundaries of Curú for thisstudy during a pilot season in the summer of 2004. I selected one group of white-facedcapuchins and one group of mantled howlers to represent monkeys in high tourist trafficareas, and one comparable group of each species living in a more remote region of therefuge to serve as study controls. The two tourist groups were already well accustomedto human influence and needed no habituation before I could begin observations. Bothnon-tourist groups, by contrast, required some period of habituation. I considered thesemonkeys habituated once they would tolerate the presence of researchers with no overtsignals of stress or avoidance behavior (Williamson and Feistner 2003). The non-touristmantled howler group was fully habituated by the end of the 2004 pilot study. The non-tourist white-faced capuchin group was much more vigilant, and took ca. 3 mo tobecome comfortable with researcher presence. This group remained sensitive to rapidmovements, however, and was never as fully habituated as the tourist group. This fact,combined with the steep terrain and lower visibility in the non-tourist white-facedcapuchin group range, resulted in a lower data yield for this group. Details of eachgroup’s demographics and home range are provided in Table I. For clarity, groups areidentified here as the Tourist Group and Non-Tourist Group for each species.

Data Collection

I gathered all data for this study between January 2006 and December 2007. I collectedhuman–nonhuman primate interaction data in the form of 15-min whole-group all-occurrence samples (Altmann 1974). With clumped human distributions and goodvisibility at this site, I could reliably record all cases of human–monkey interactionsfor short sample periods. I identified actors by age and sex category, and recorded theinitiator of each interaction (either human or monkey). I also recorded the number ofhumans and domestic animals present during each 15-min all-occurrence sample.

I coded behavior using an ethogram that allowed human–monkey interactions, aswell as other social behaviors, to be denoted as either “monkey” or “human” (Table II).I logged the following behaviors for the monkeys: threatening postures or vocaliza-tions; taking or eating provisioned foods; approaching or running away from people;stealing food or other items; and vigilance of humans, dogs, or vehicles. I recorded thefollowing behaviors for humans: approaching the monkeys; offering food; calling,clapping, or making other noises; and stomping, waving their arms, or otherwisethreatening the monkeys. In addition to the actors and type of behaviors, I recordedthe length of each interaction, with individual bouts truncated at a maximum of 900 s(the full 15-min sample period). A total of 1670 15-min samples were completed,

White-Faced Capuchin and Mantled Howler Responses to Ecotourism 577

providing 417.5 h of data and 1949 individual bouts for analysis. Exact sample sizes foreach study group are provided in Table I.

Data Analysis

Because these behavioral data did not conform to a normal distribution (Kolmogrov–Smirnov goodness of fit, with P < 0.15 and N = 96 [group-months], N = 1949[interaction bouts]), I applied appropriate nonparametric tests. I followed all groupsfor the same 24-mo period, but for some tests the group-months were slightly lowerthan 24 owing to poor weather, field assistant absence, or other unavoidable circum-stances. To adjust for an unequal number of resulting observation hours, I calculated therate of interactions per hour. I then analyzed the variance in the rate of interactionsbetween groups, e.g., tourist and non-tourist; rainy and dry seasons, using the Kruskal–Wallis test (H). The chi-square test was used to compare initiation of interactions andsex/age class differences of interactions. The Mann–Whitney–Wilcoxon test (W)allowed for a comparison of human encounter rates across focal groups. I brokeinteraction rates per hour and visitor encounters down by month to allow for seasonalvariation, and applied Pearson’s correlation coefficient (r) to test the associationbetween the two. For all forms of analysis, confidence intervals were set at 95 %,and all tests were one-tailed unless otherwise noted.

Ethical Note

This research was conducted under the approval of The Ohio State UniversityInstitutional Animal Care and Use Committee (Protocol #2007A0142), and was in

Table I Demographic, ranging, and data collection details for four focal groups of Cebus imitator andAlouatta palliata at the Curú Wildlife Refuge, Costa Rica (January 2006–December 2007)

Tourist groupcapuchins

Non-touristgroupcapuchins

Tourist grouphowlers

Non-touristgrouphowlers

Group size 22 20 30 26

Number of adult males 3 3 5 4

Number of adult females 7 7 12 12

Male to female ratio 0.42 0.42 0.42 0.33

Number of immatures 12 10 17 10

Immature to female ratio 1.71 1.43 1.08 0.83

Habitat types Secondary forest,mangroves,agroecosystems,deforested areas

Primary andsecondaryforest

Riparian andsecondary forest,mangroves,agroecosystems

Primary andsecondaryforest

Home range size 66.2 ha 26.5 ha 41.6 ha 20.4 ha

Number of 15-min samples 545 122 611 392

Total hours of observation 136.25 30.5 152.75 98

Number of interaction bouts 1080 305 299 265

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compliance with Costa Rican law. With a purely observational protocol, unduestressors on the focal individuals were minimal.

Results

Variation in Human–Monkey Interactions

White-faced capuchins engaged in significantly more frequent interactions with humansthan did the mantled howlers in both the tourist (H = 16.98, df = 1, P < 0.001) and non-tourist (H = 7.36, df = 1, P = 0.007) groups (Fig. 1). Although human exposure differed

Table II Ethogram of human–monkey interactions observed for Cebus imitator and Alouatta palliata at theCurú Wildlife Refuge, Costa Rica (January 2006–December 2007)

Behaviors performedby monkeys

Alliance Monkey forms alliance with one or more group memberstoward a common opponent, such as the “double threat”posture in capuchins.

Approach Monkey approaches human to a distance of ≤1 m.

Beg Monkey begs person for food, with hand outstretched.

Chase Monkey chases a person or domestic animal.

Drink Monkey drinks or licks water from faucet, sink, or dishes.

Displace Monkey approaches human or domestic animal, who thenmoves out of the way with no further conflict.

Display Monkey performs a generalized display, which may includebranch bouncing, vocalizations, or other posturing.

Forage process Monkey handles (but does not eat) human-sourced food,such as trying to open packaged foods, rolling or smashingfood on a substrate, or otherwise manipulating food items.

Play Monkey plays with human objects.

Steal Monkey snatches nonfood item from person, bag, house, orgarbage bin.

Take food Monkey takes and/or eats food that was provided by humans,either by hand or thrown.

Threat Monkey threatens a person or domestic animal with facialexpression, lunge, or branch bounce.

Vigilance Monkey observes humans closely.

Vocalize Monkey makes vocalizations that appear directed towardhuman; excludes contact calls and food calls.

Behaviors performedby humans

Approach Human approaches monkey to a distance of ≤1 m.

Chase Child or domestic dog chases monkey.

Displace Monkey moves out of a human’s or domestic animal’s way,without further interaction.

Offer food Human throws food or offers food in hand to monkeys

Threat Person shouts, stomps, waves arms, or otherwise threatensmonkeys

Vigilance Person watches monkeys closely

Vocalize Human talks to or makes noises at monkey

White-Faced Capuchin and Mantled Howler Responses to Ecotourism 579

significantly between tourist and non-tourist troops for both capuchins (W = 204951.5,df = 1, P < 0.01) and howlers (W = 354772.5, df = 1, P < 0.01), the difference ininteraction rates between the two species was more pronounced than the differencebetween the non-tourist and tourist groups of the same species. The duration ofinteractions significantly differed between the tourist and non-tourist groups of mantledhowlers (H = 37.50, df = 1, P < 0.001) and between species in the non-tourist groupsonly (H = 35.92, df = 1, P < 0.001) (Fig. 1).

In addition to differences in frequency and duration of interactions, the two speciesdiffered qualitatively, with each presenting a distinct repertoire of responses (Table III).Mantled howler interactions were dominated by vocalizations and vigilance behaviors.Along with the vigilance and threats observed in the other focal groups, white-faced

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Fig. 1 Mean and SEM interaction rates (bouts/h) and duration of interactions (in seconds) for four focalgroups of Cebus imitator and Alouatta palliata at the Curú Wildlife Refuge, Costa Rica (January 2006–December 2007).

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capuchin individuals in the tourist group also approached human visitors and acceptedfood handouts.

Initiators of Cross-Species Interactions

Most cross-species interactions were initiated by the monkeys; humanswere the primaryinitiators for the tourist group mantled howlers only (Fig. 2). This difference in initiationrates between the tourist and non-tourist groups is significant for both white-facedcapuchins (χ2 = 98.556, df = 1, P < 0.001) and mantled howlers (χ2 = 83.788, df = 1,P < 0.001).

Age and Sex of Participants

Juvenile white-faced capuchins participated in interactions more often than adults did(χ2 = 18.249, df = 1,P < 0.001), but there was no difference in age of participants amongmantled howlers (χ2 = 2.090, df = 1, P = 0.148). There was a significant difference inparticipation by sex for the mantled howlers, with adult males being the principal actorin a majority (66.12 %) of all interactions (χ2 = 17.641, df = 1, P < 0.001). By contrast,adult male and female white-faced capuchins were equally likely to be involved ininteractions (χ2 = 0.048, df = 1, P = 0.827) (Fig. 3).

Table III Breakdown of all human–monkey interactions, including proportions total interactions for eachtype, observed for four focal groups of Cebus imitator and Alouatta palliata at the Curú Wildlife Refuge,Costa Rica (January 2006–December 2007)

Behaviors observed Tourist groupcapuchins

Non-touristcapuchins

Tourist grouphowlers

Non-touristhowlers

No. % No. % No. % No. %

Alliance against human 4 0.37 1 0.33 — — — —

Approach human 25 2.31 3 1.00 — — — —

Beg human for food 56 5.19 — — — — — —

Chase human/dog 7 0.65 — — — — — —

Drink from faucet or sink 6 0.56 — — — — — —

Displace human/dog 3 0.28 — — — — — —

Display toward human, vehicle, or animal 17 1.57 19 6.35 — — — —

Forage in garbage bin 3 0.28 — — — — — —

Process provisioned food item 1 0.09 — — — — — —

Play with human objects 2 0.19 — — — — — —

Steal food from person, house, or table 62 5.74 — — — — — —

Steal nonfood item 6 0.56 — — — — — —

Take/eat offered food from humans 198 16.30 — — 1 0.33 — —

Threaten human/dog 227 21.02 65 21.74 1 0.33 — —

Vigilance towards humans/dogs/etc. 385 35.65 153 51.17 103 33.77 172 64.91

Vocalize toward humans/dogs/etc. 78 7.22 58 19.40 200 65.57 93 35.09

Total 1080 100.01 299 99.99 305 100.00 265 100.00

White-Faced Capuchin and Mantled Howler Responses to Ecotourism 581

Relationship Between Human Presence and Frequency of Interactions

The mean number of humans the monkeys were exposed to per sample period did notsignificantly differ by season (Table IV). It follows, then, that there was no significantseasonal variation in human–monkey interaction rates for any study group. A closerexamination, however, did reveal some relationship between human presence andhuman–monkey interaction rates. Mantled howlers showed a strong interaction be-tween the number of people encountered and the rate of human–monkey interactions inthe tourist group (Pearson’s r = 0.670, P < 0.01), but this pattern was not evident in thenon-tourist group (r = 0.273, P = 0.866). The white-faced capuchins showed theopposite pattern, with a significant association between human encounter rates andhuman–monkey interaction rates in the non-tourist group (r = 0.643, P < 0.01), but notin the tourist group (r = 0.322, P = 0.134) (Fig. 4).

Discussion

White-faced capuchins and mantled howlers demonstrated clear species-specific tenden-cies with regard to potential interactions with tourists. These interspecific differencesencompassed not only frequency but also types of interaction. White-faced capuchinswere far more likely to engage with tourists than are mantled howlers, and to take onmore direct interactions. The tourist-area focal group was observed taking offered food,

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Monkey-Initiated

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Human-Initiated

Monkey-Initiated 70%

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Human-Initiated

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Fig. 2 Proportion of interactions initiated by humans and by monkeys for four focal groups of Cebus imitatorand Alouatta palliata at the Curú Wildlife Refuge, Costa Rica (January 2006–December 2007).

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stealing food from rubbish bins or tables, and approaching or threatening visitors. Suchbehaviors place the monkeys at risk of disease transmission (Fuentes and Gamerl 2005;Muehlenbein et al. 2010), encounters with domestic dogs (De Oliveira et al. 2008),altered diet and foraging patterns (McKinney 2011), or direct conflict with tourists andpark management (Chism 2005; Singla et al. 1997). The mantled howlers, by contrast,showed little interest in engagement with tourists, but appeared to be particularlyvulnerable to anthropogenic noise. Their vocalization in response to such disturbancelikely affects intergroup relationships (de Cunha and Byrne 2006; Grossberg et al. 2003).

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Fig. 3 Actors and initiators of observed human–monkey interactions for four focal groups of Cebus imitatorand Alouatta palliata at the Curú Wildlife Refuge, Costa Rica (January 2006–December 2007).

White-Faced Capuchin and Mantled Howler Responses to Ecotourism 583

One surprising finding was that the tourist and non-tourist groups did not signifi-cantly differ in their overall interaction rate, despite having exposure to very differentnumbers of people. This pattern may be explained by insufficient habituation on the

Table IV Seasonal variation in tourist exposure and human–monkey interaction rates for four study groups ofCebus imitator and Alouatta palliata at the CurúWildlife Refuge, Costa Rica (January 2006–December 2007)

Tourist exposure per sample: mean,SEM, Kruskal–Wallis H, degreesfreedom, and significance

Interaction rates: mean, SEM,Kruskal–Wallis H, degreesfreedom, and significance

Tourist group capuchins Dry season: 6.06 ± 0.33 Dry season: 8.13 ± 1.82

Rainy season: 6.47 ± 0.36 Rainy season: 9.42 ± 2.10

H = 1.23, df = 1, P = 0.267 H = 0.19, df = 1, P = 0.666

Non-tourist group capuchins Dry season: 2.07 ± 0.14 Dry season: 7.36 ± 2.98

Rainy season: 1.57 ± 0.14 Rainy season: 12.10 ± 2.81

H = 0.06, df = 1, P = 0.813 H = 1.73, df = 1, P = 0.188

Tourist group howlers Dry season: 3.12 ± 0.11 Dry season: 1.56 ± 0.40

Rainy season: 3.64 ± 0.09 Rainy season: 2.44 ± 0.74

H = 0.00, df = 1, P = 0.0.975 H = 1.23, df = 1, P = 0.267

Non-tourist group howlers Dry season: 2.10 ± 0.09 Dry season: 3.08 ± 1.05

Rainy season: 2.41 ± 0.09 Rainy season: 1.80 ± 0.43

H = 0.03, df = 1, P = 0.866 H = 0.35, df = 1, P = 0.554

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Fig. 4 Relationship between human encounter rates and human–monkey interaction rates for four studygroups of Cebus imitator and Alouatta palliata at the Curú Wildlife Refuge, Costa Rica (January 2006–December 2007). Human encounter rates are denoted by the solid line, and human-monkey interaction ratesare denoted by the dashed line. Significant associations between the two, measured with Pearson’s correlationcoefficient, are marked with an asterisk.

584 T. McKinney

part of the non-tourist groups. The tourist groups in this study have been graduallyhabituated to human presence over the years. While I followed standard methods(Williamson and Feistner 2003) to ensure that the two non-tourist groups were appro-priately habituated for this study, any short period of habituation could not be trulyequivalent to habituation through years of frequent human exposure (Jack et al. 2008).It is also possible that the monkeys may simply respond to tourist and researcherpresence differently. One study suggested that researchers have a greater impact ongorilla behavior than tourists do, possibly owing to the distances between the peopleand the primates (Klailova et al. 2010). In this case, perhaps the closer viewing range ofthe researchers and the relative novelty of human presence influenced the unexpectedlyhigh rate of interaction among the control troops.

A second important intraspecies distinction lies in the initiation of and participationin cross-species encounters. For the white-faced capuchins, nearly all human–monkeyinteractions were initiated by the monkeys. An interaction between a white-facedcapuchin and a tourist usually attracted the attention of group members, underscoringthe gregariousness and curiosity of this species. Novel sources of food or amusementare likely to disseminate rapidly throughout the social group, and new behavioralpatterns can develop quickly with this species (Fragaszy et al. 2004; Panger et al.2002). The mantled howlers, however, rarely responded to tourists unless they wereintentionally provoked. Mantled howler interactions generally involved single individ-uals interacting with tourists; because their responses were primarily vocal in nature,these interactions disproportionately featured adult males.

The association between human presence and human–monkey interaction rates ismore complex than expected. Other than the obvious caveat—without any humans,there can be no interactions—the influence of increasing human presence is notstraightforward. The mantled howlers showed the predicted increase in human inter-action rates with greater tourist numbers. The tourist-area white-faced capuchins,however, showed no significant difference in interaction rates with respect to touristnumbers. Considering that the white-faced capuchins were also likely to instigate themajority of human–monkey encounters, it appears that this species will take anyopportunity to engage with humans if there is the possibility of a reward.

Such differences between the two species’ responses to interaction are noteworthy.Many of the human–monkey interactions observed are consistent with the behavioralrepertoire of the species, leaving them fundamentally different tools with which torespond to human disturbance. White-faced capuchins, for example, regularly travel onthe ground and are known to engage in an active, destructive feeding method (Fragaszyet al. 2004). These behaviors explain why white-faced capuchins likely view back-packs, rubbish bins, and humans themselves as potential sources of food. In contrast,the mantled howlers rarely come to the ground and rely on easily visible foliage andfruit for their diet (Milton 1980). In addition to these differences in dietary and travelpatterns, white-faced capuchins are highly active animals, with more than half of theirday devoted to foraging activities (Rose 1998). Mantled howlers are more sedentaryanimals (Milton 1980; Pavelka and Knopff 2004), and generally retreat or remain silentin the presence of humans (De la Torre et al. 1999; Grossberg et al. 2003). The noisy,playful behavior of the white-faced capuchins, coupled with their distinct black-and-white pelage, makes them more attractive and visible to tourists than the quiet, dark-furred mantled howlers, which tourists often walk directly under without notice.

White-Faced Capuchin and Mantled Howler Responses to Ecotourism 585

These finding illustrate that the response to tourist pressure can vary across sym-patric species. The primates living in ecotourism sites are active participants in cross-species encounters, and show some autonomy over the degree to which they choose tointeract with tourists. The specific relationships between the monkeys and the humansthey encounter may have a profound influence on the types of interactions that takeplace. For example, both non-tourist groups lived in areas with no tourist or otherhuman traffic, and therefore encountered only quiet researchers. Tourist area monkeys,however, are forced to deal with inconsistent behavior on the part of their humanvisitors. These monkeys must constantly assess possible outcomes of interaction, whichcould range from a food reward, to harassment, to simply being ignored.

The results of this study are consistent with behavioral characteristics of the twospecies, and support the idea that the effects of tourist interaction are likely to be species-specific. Further investigation into species-specific variation regarding human–nonhu-man primate interactions will lead to better wildlife management policies. In particular,we must begin to consider tourist behavior along with tourist numbers. As the averagetourist should not be expected to understand monkey postures, facial expressions, orvocalizations, it is up to park management to encourage species-appropriate viewingbehaviors (Sabbatini et al. 2006; Treves and Brandon 2005). Signs or handouts aboutmonkey viewing behavior have been used successful at some sites (Fuentes et al. 2007),and are one cost-effective way to reduce tourist–monkey conflict. Other simple mea-sures include changing staff behaviors. In this case, tour guides may be discouragedfrom provoking mantled howler vocalizations and causing undue stress for the mon-keys. Guides could promote their tours as more “naturalistic” or “wildlife-friendly” toencourage visitors to minimize their impact on the monkeys. Monkey-proof garbagebins and stronger efforts to deter provisioning would reduce interactions with white-faced capuchins. Overall, it is clear that the cross-species comparison of human–nonhuman primate interactions is an important tool in ensuring that human contact doesnot undermine the goals of primate ecotourism (Sutherland 2007).

Acknowledgments I thank the Schutt Family of Refugio Curú for their kindness in allowing me to collectdata on their property. This research was generously funded by Earthwatch Institute, Conservation Interna-tional, and The Ohio State University. Caspar Harris, Carolina Orozco Zamora, and many Earthwatchvolunteers provided excellent field assistance. I also thank Lexine Trask, Rob Schubert, Joanna Setchell,and two anonymous reviewers for their helpful comments on earlier versions of this manuscript.

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