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American Journal of Primatology 73:439–448 (2011)

RESEARCH ARTICLE The Effects of Provisioning and Crop-Raiding on the Diet and Foraging Activities of Human-Commensal White-Faced Capuchins (Cebus capucinus) TRACIE MCKINNEY Marshall University, Huntington, West Virginia

Non-human primates are coming into increasingly frequent contact with humans and with humanmodified environments. The potential for monkeys to survive in such modified landscapes is questionable, and is likely related to a species’ behavioral plasticity, particularly as it relates to diet. In this study, I explore the ways in which white-faced capuchins (Cebus capucinus) adjust their diet and foraging behaviors in response to anthropogenic impact. I compare a troop of human-commensal ´ Wildlife Refuge in western monkeys and a similar troop of wild-feeding monkeys living within the Curu Costa Rica for differences in overall diet composition and activity budgets to evaluate the impact of habitat change in this context. The commensal-living white-faced capuchins rely on raided coconut (Cocos nucifera) and oil palm (Elaeis guineensis) crops and provisioned or stolen human foods for over one-half of their total diet. Regardless of this highly anthropogenic diet, the two study troops do not significantly differ in their activity budgets, and the human-commensal troop maintains wild-foraging activities consistent with those of the wild-feeding troop. These data suggest that the white-faced capuchins at this site are responding to anthropogenic disturbance primarily through the exploitation of human food resources, but they do not yet appear to have lost the foraging skills required to survive in this modified landscape on their own. This study adds to our growing body of knowledge on primate survival in matrix habitats, and will hopefully inform primate management plans throughout the Neotropics. Am. J. Primatol. 73:439–448, 2011. r 2010 Wiley-Liss, Inc. Key words: Cebus capucinus; anthropogenic change; provisioning; diet; habitat disturbance; ethnoprimatology

INTRODUCTION Nonhuman primates have long been sympatric with humans throughout their geographic range [Fuentes, 2006]. Although many primate populations are diminished or locally exterminated by extreme anthropogenic disturbance, other species—if offered some degree of protection from human hunting or exploitation—respond relatively well to the habitat modification. These flexible, human-commensal populations can survive in forest fragments, agricultural lands, or matrix habitats [Bowne & Bowers, 2004; Fischer & Lindenmayer, 2007; Gascon et al., 1999; Ricketts, 2001]. In this study, I explore the strategies of one resilient species, the white-faced capuchin (Cebus capucinus), for survival in agricultural matrix habitat. It is widely accepted that generalist species adjust more readily to habitat alteration than ´squez & specialists [Fisher & Owens, 2004; Va Simberloff, 2002], and some primate species are naturally more adaptable to anthropogenic disturbance. The degree of frugivory is negatively associated with survival in altered or fragmented landscapes [Fimbel, 1994; Sorensen & Fedigan,

r 2010 Wiley-Liss, Inc.

2000], while species with the most dietary plasticity have the greatest chance of survival in degraded habitats [Chapman et al., 2007; Estrada et al., 2002; Onderdonk & Chapman, 2000]. Primate species that use a broad range of habitats also have the opportunity to exploit alternative food resources [Lehman, 2004], and may be better suited for survival along forest edges or in areas of secondary growth. Species that are capable of crossing open spaces terrestrially or that regularly forage in the undergrowth are also less vulnerable to anthropogenic modification and patch isolation than those which are confined to the forest canopy [Fimbel, 1994; Michalski & Peres, 2005; Onderdonk & Contract grant sponsor: Earthwatch Institute, Conservation International, The Ohio State University. Correspondence to: Tracie McKinney, Department of Sociology and Anthropology, Marshall University, One John Marshall Drive, Huntington, WV 25755. E-mail: [email protected]

Received 29 June 2010; revised 5 December 2010; revision accepted 5 December 2010 DOI 10.1002/ajp.20919 Published online 31 December 2010 in Wiley Online Library (wiley onlinelibrary.com).

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Chapman, 2000]. Life history variables, such as body size and reproductive rates, also play a role in a primate species’ susceptibility to anthropogenic change. Species with a higher rate of natural population increase tend to be more resilient to habitat change [Harcourt, 2006; Reynolds, 2003]. The ability for primates to adjust to anthropogenic habitat modification is uncertain, and this human–primate interface remains a key area of investigation for the emerging field of ethnoprimatology [Fuentes & Hocking, 2010; Lee, 2010; Wolfe & Fuentes, 2007]. Preliminary studies of primates in anthropogenic landscapes suggest that habit modification influences varied aspects of primate socioecology. Dietary stress or loss of habitat may alter male takeover rates [Moore, 1999], trigger infanticide events [Fedigan, 2003; Ramı´rez-Llorens et al., 2008; Sterck, 1998], or lower female fecundity [Martı´nez-Mota et al., 2007], all negatively influencing population growth. However, the most flexible of the human-commensal primates (e.g., Macaca, Cebus, Papio) compensate for dietary stress associated with anthropogenic habitats through crop- or garbage-raiding. Some studies credit supplemental dietary resources with higher birth rates, shorter weaning time, and reduced interbirth intervals [Di Bitetti & Janson, 2001; Kogenezawa & Imaki, 1999; Loy, 1988; Wada & Xiong, 1996]. However, other studies associate frequent human interactions with lowered reproductive rates and increased infant mortality [Berman et al., 2007; De la Torre et al., 2000; Grossberg et al., 2003; O’Leary & Fa, 1993]. Food-enhanced primate groups often show altered activity budgets, spending less time at foraging and feeding and more time at rest [Altmann & Muruthi, 1988; Forthman Quick & Demment, 1988; Saj et al., 1999]. These human-commensal primates also maintain larger troops [Biquand et al., 1992], face higher population densities [Moore, 1999; Singh et al., 2006], and have altered adult sex ratios [Mori et al., 2007; Singh & Rao, 2004; Sterck, 1998] in relation to their wild-feeding counterparts. Clearly, the effects of anthropogenic disturbance are speciesspecific at best, and are also dependent on individual site conditions. Much of the ethnoprimatological literature to date has focused on ‘‘conflict paradigms’’ [Lee, 2010], including bi-directional disease transmission [Chapman et al., 2005; Wallis & Lee, 1999], attacks on humans [Hockings et al., 2010; Singla et al., 1997], and crop-raiding [Hill, 2005; NaughtonTreves et al., 1998; Saj et al., 2001]. Crop-raiding, in particular, has dominated the ethnoprimatological literature, as primates are among the most commonly reported problem species. At least three Cebus species are documented crop-raiders [C. apella: de Oliveira & de Souza Fialho, 2007; Galetti & Pedroni, ´les1994; C. capucinus: Baker & Schutt, 2005; Gonza Kirchner & Sainz de la Maza, 1998; C. libidinosus:

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De Freitas et al., 2008], leading to the perception of these monkeys throughout the Neotropics as agricultural pests. Although crop-raiding primate species rarely forgo foraging on wild foods [De Freitas et al., 2008; Naughton-Treves et al., 1998], the altered quantity or composition of their diets may have important consequences. Supplemental feeding, whether in the form of crop-raiding, tourists handouts, or active provisioning, has the potential to be one of the most influential forms of anthropogenic disturbance, affecting primate ecology, demographics, and social behavior. One of the principle concerns regarding the effects of anthropogenic dietary changes among nonhuman primates is the maintenance of speciestypical foraging behavior. There is evidence that social learning is necessary for the development of foraging behavior among young primates [Gunst et al., 2008; Jaeggi et al., 2010; Rappaport & Brown, 2008; Schiel & Huber, 2006]. The New World primates are particularly noted for high rates of cofeeding and food transfer between adults and juveniles [Rappaport & Brown, 2008], possibly due to the frequent encounters with novel food associated with extractive foraging techniques [Schiel & Huber, 2006]. The foraging methods of Cebus capucinus, for example, appear to consist of local traditions [O’Malley & Fedigan, 2006; Panger et al., 2002], indicating a high degree of social learning for food acquisition. Furthermore, juvenile primates spend more time than adults interacting with humans and eating provisioned foods [O’Leary & Fa, 1993; Saj et al., 1999], and quickly associate humans with food rewards. It is reasonable to ask whether these young animals will lose vital opportunities to learn species-typical foraging methods when the adults of their community have shifted their attention to anthropogenic food items [Sabbatini et al., 2006]. It is important to note that, if species-typical foraging behavior is lost among young animals, the effects of this change would eventually be evident at the community level; if provisioning were to be removed at some point in the future, the consequences could be severe. Ultimately, the long-term effects of behavioral modifications and the potential for primate survival in these altered environments remain unknown [Fuentes & Hocking, 2010; Sutherland, 2007]. The white-faced capuchin is a frequent resident of anthropogenic landscapes throughout its range [Fragaszy et al., 2004]. Like all capuchins, C. capucinus is a small arboreal primate that occupies a variety of habitat types, often foraging in the understory [Sorensen & Fedigan, 2000]. The species is a true dietary generalist, but is primarily classified as a frugivore–insectivore [Fragaszy et al., 2004]. White-faced capuchins are destructive foragers, using their strong jaws and dexterous hands to access embedded food resources. Despite an unu-

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sually slow life history [Fedigan & Rose, 1995; Fragaszy et al., 2004; Jack & Fedigan, 2005], whitefaced capuchins appear to retain viable populations in highly disturbed habitats [De Oliveira & De Souza Fialho, 2007; Fragaszy et al., 2004; Galetti & Pedroni, 1994]. In this study, I compare the diet and foraging behaviors of a troop of human-commensal whitefaced capuchins with those of a neighboring wild´ Wildlife feeding troop, both living within the Curu Refuge in western Costa Rica. As dietary and habitat generalists, these monkeys are expected to readily alter their diet, ranging and activity patterns to meet their energetic needs in a modified landscape. To understand the impact of anthropogenic foods on their diet and foraging behaviors, I test three specific predictions: (1) The human-commensal troop, with ample access to crops and provisioned fruits, will have a more frugivorous diet than the wild-feeding troop; (2) The human-commensal troop, with relatively greater access to food resources than the wild-feeding troop, will have decreased travel and foraging times; and (3) If the commensal troop has become reliant on provisioned foods for their survival, their wild-resource foraging patterns should differ from those of the wild-feeding troop. This study should provide some indication whether or not this human-commensal troop of white-faced capuchins is supplementing or replacing their traditional diet with human foods. METHODS Study Site and Population ´ Wildlife Refuge is a small, privately The Curu owned wildlife refuge and hacienda in western Costa Rica (N 91470 4400 , W 841550 1500 ). Approximately onethird of the 1,492-ha property is modified for human use, primarily as pasture for zebu cattle (Bos indica) and for small plantations of mango (Mangifera indica), banana (Musa acuminata), soursop (Annona muricata), guava (Psidium guajava), and African oil palm (Elaeis guineensis). Coconut palm (Cocos nucifera) is an invasive species common to the Pacific coast, and is plentiful throughout these modified areas of the refuge; because they are harvested for sale, coconuts are considered a crop for the purposes of this study. The remaining two-thirds of the property is left in a natural state [Baker & Schutt, 2005; Williams & Vaughan, 2001] and is composed of primary and advanced secondary forest. Tourism is a key component of the refuge’s income, and the property hosts roughly 10,000 tourists annually. ´ has two distinct seasons, with rainy season Curu ranging from May through October and dry season from November through April. Temperatures range from 20 to 351C, with a mean monthly temperature of 27.31C during the dry season and 26.51C during rainy season. Rainfall averages 1,260 mm per year,

with a dry season mean of 21.7 mm of precipitation monthly and a rainy season mean of 185.8 mm ´gico Nacional, 2008]. monthly [Instituto Meteorolo ´ is classified as tropical moist/transiOverall, Curu tional forest [Herzog & Vaughan, 1998], but it incorporates a number of microhabitats, including primary and secondary forest, riparian forest, mangrove swamp, marine beach, and anthropogenic landscapes (see Fig. 1). Two troops of white-faced capuchins are considered here to allow for a comparison of habitat modification on diet and foraging behaviors. The human-commensal troop maintains a 66.2-ha home range in the heavily traveled area of the refuge, which encompasses plantations, secondary forest, mangrove swamp, pasture edge, and areas of human use. These monkeys have access to crops, garbage cans, and the occasional handout from tourists, and are provisioned on a near daily basis with a variable quantity of domestic bananas. Because the animals ´ staff, provisioning is independent of are fed by Curu tourist numbers. The wild-feeding troop, which serves as a study control, has no access to plantations, provisioning, or any other human foods. The 26.5 hectare range of this troop incorporates both primary and advanced secondary tropical forests. All study animals in both troops are identifiable to the level of sex and approximate age category. Age categories are defined here as infant (still nursing, or o1 year old), juveniles (1–7 years), and adults (47 years) [Jack & Fedigan, 2004]. Key features of the two study troops, including group size, demographics, home range, and habitat characteristics, are provided in Table I.

Key: Transitional tropical forest

Secondary/ coconut forest

Pasture

Mangrove swamp

Plantation

Beach/ cabin area

´ Wildlife Refuge, showing primary habitat types Fig. 1. Curu within the study area. The approximate home ranges of the two study troops are marked by the ovals (solid 5 commensal; dashed 5 wild-feeding).

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Data Collection Data were collected between January 2006 and December 2007 as part of a larger study concerning the behavioral adaptations of Cebus capucinus to modified landscapes in Costa Rica [McKinney, 2010]. Observations were conducted between 5:00 am and 5:00 pm, or roughly dawn to dusk. Data collection was balanced across seasons and throughout the day; a detailed account of data collection for each troop may be found in Table II. The order of data collection activities was randomized in advance to avoid temporal biases. Diet data were collected through 15-min wholetroop scan samples at 1-min intervals [Altmann, 1974]. Because white-faced capuchins remain in relatively cohesive groups while feeding, with group members often feeding on a single resource, it was possible to sample overall feeding patterns using whole-troop scan sampling. Each individual scan equaled a single point of feeding data, which identified the primary food source being consumed by the troop. Although each feeding scan was not necessarily an independent data point (and therefore cannot be considered a feeding bout), these data allow for an approximation of diet based on time spent feeding [Zinner, 1998]. All food items were identified as ‘‘human’’ or ‘‘wild’’ foods. Foods were then further classified by category as fruits, leaves, flowers, insects, other invertebrates, vertebrate prey, exudates, shoots, or non-natural foods, such as cookies or chips. All plant-based foods were then identified to the genusor species-level whenever possible.

Ranging patterns were calculated using a Garmin e-Trex handheld Global Positioning System (GPS) unit. GPS measurements were recorded only when receiving a signal with an error of less than 10 m. Coordinates were taken from the approximate center of the monkey group at 15-min intervals throughout the day. Weather and canopy conditions during the rainy season often prohibited accurate GPS readings; therefore, this data set is somewhat biased toward the dry season. Activity budgets were calculated through 20-min interval focal animal follows, with behavior recorded throughout the sample at 1-min intervals. Only adult animals were used for focal follows, and the first adult monkey visible became the first focal subject [Altmann, 1974; Lehner, 1996]. Most adult animals in both study groups were individually known by hair patterns, scars, size, and temperament, which facilitated focal animal sampling. To calculate activity budgets, all behaviors were assigned to one of four categories: feeding (all food consumption, processing, and foraging), social (all affiliative and aggressive social interactions), travel (any directed individual or troop movement, excluding movement during foraging), and rest (sleep or otherwise inactive). Focal samples were discarded if the subject disappeared from view for more than 60 sec, of if the animal interacted with other individuals in ways that compromised the identity of the focal subject. The remaining ‘‘out of view’’ notations make up a negligible fragment (o1%) of the total results and do not significantly influence the activity budget estimates.

TABLE I. General Characteristics of the Two Study Troops and Their Territories Human-commensal troop Group size Group composition

Home range size Home range habitat type(s)

Level of landscape alteration (after McIntyre and Hobbes [1999])

Wild-feeding troop

22 Three adult males Seven adult females 12 immatures 66.2 ha Secondary forest, plantation, mangrove swamp, pasture edge, open/developed areas Fragmented

20 Three adult males 6–7 adult females 10–11 immatures 26.54 ha Advanced secondary forest Primary forest Intact

TABLE II. Breakdown of Data Collection by Season, Troop, and Type of Data 20-min focal samples

Commmensal (total) Rainy Dry Wild-feeding (total) Rainy Dry

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15-min diet scan samples

] samples

Hours

] samples

] points

Hours

GPS points

315 131 184 60 37 23

105 43.67 61.33 20 12.33 7.67

644 305 339 121 56 65

10,304 4,880 5,424 1,936 896 1,040

161 76.25 84.75 30.25 14 16.25

1,150 397 753 390 172 218

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Data Analysis These analyses are based on 266 hr of behavioral observations, exclusive of GPS ranging data, with the human-commensal troop. An additional 50.25 hr of behavioral and diet data were collected from the wildfeeding troop for comparison, using identical methods. Search time for the wild-feeding troop was much longer than for the commensal troop, and the study yielded fewer observation hours with this troop. To accommodate for these unequal sample sizes, the unit of analysis for diet and activity data was the hourly rate of behavior. All statistical analyses were performed with Minitab Version 15 software (Minitab Inc., 2007), and data are presented here with P-values and confidence intervals are set at 95%. These data did not conform to a standardized distribution (Kolomorov– Smirnoff Goodness of Fit test, with Po0.10) and therefore have been analyzed with the appropriate nonparametric tests. Home range estimates were determined using the Minimum Convex Polygon (MCP) method in ArcGIS 9.3 software (ESRI, 2008). The MCP method was chosen for this study because it provides a good approximation of seasonal range variation and is not generally limited by statistical assumptions [Lehner, 1996; Powell, 2000]. The MCP method is found to be quite precise with small sample sizes [Grueter et al., 2009], which was an important consideration for the more elusive wildfeeding troop. This research protocol was approved through The Ohio State University Institutional Animal Care and Use Committee (Protocol ]2007A0142), was conducted in full compliance with Costa Rican law, and adhered to the American Society of Primatologists ethical principles for the treatment of primates.

identified over the course of the study; roughly three quarters of these identified resources comprise less than 1% of the total diet each. Approximately 60% of the commensal troop’s overall diet is derived from anthropogenic sources. The majority of these foods are raided crops and provisioned fruits, while roughly 2% of the total diet is composed of non-natural foods, including rice, sandwiches, cookies, and chips (Fig. 2). Coconuts are available year round, and bananas are provisioned almost daily. The near constant availability of these resources results in a highly frugivorous diet,

RESULTS Diet Table III lists key food resources used by the two study troops. For the human-commensal troop over 40 distinct food items (with insects as a single item) were

Fig. 2. A juvenile white-faced capuchin enjoys a scavenged bag of corn chips.

TABLE III. Key Food Sources Used by the Two White-Faced Capuchin Troops Proportion/diet Species – Musa acuminata Elaeis guineensis Cocos nucifera Anacardium excelsum Mangifera spp. Spondias mombin

Common name

Source

Parts

Months eaten

HC

WF

All insects/spiders Domestic banana Oil palm/palmiche Coconut Wild cashew/espavel Wild mango Hog plum/jobo

W P, R R R W W W

– Fr Fr Fr, Sh Fr Fr Fr

All All January, March—December All April–May, November April—July June, August–September

23.81 22.94 16.31 10.49 0.27 2.43 0.27

68.33 – – – 8.23 0.75 1.75

Foods listed here are those that comprise 45% of either troop’s total diet, or those that are eaten by both study troops. The mean proportion of each food item in the total annual diet of the human-commensal (HC) and the wild-feeding (WF) troops are listed in the last two columns. Sources are: P, provisioned; R, raided from plantations, homes or garbage; and W, wild-foraged. Parts eaten are: Fl, flowers; Fr, fruit; and Sh, shoots.

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with nearly 70% of feeding time devoted to fruit and roughly 25% to insect foraging. Ten distinct plant genera, plus the general category of ‘‘insects,’’ were identified for the wildfeeding troop. Their diet may appear less diverse than that of the human-commensal troop in part due to the heightened difficulty of field identifications of plant foods in the dense forest. However, unlike the commensal troop, the wild-feeding troop was never observed feeding on vertebrate prey, shoots, or nonnatural foods, and the resulting diet is based almost entirely on insect and fruit foraging. In contrast to the human-commensal troop, the wild-feeding troop spends about 70% of feeding time on insect foraging and roughly 25% of feeding time on fruit. Table IV describes the general diet of the two study troops, with foods divided into broad categories. The two study troops’ diets significantly differ in terms of the rate of foraging on fruit and leaves. Although the proportions of each dietary component vary between the groups, the two groups do not significantly differ in the rate of insect, flower, or exudate consumption. The use of non-natural food resources by the commensal white-faced capuchin troop increased drastically over the 2-year study period (see Fig. 3). This change is likely linked to an increase in development at the wildlife refuge around the midpoint of the study. This construction changed the commensal troop’s typical travel pattern, bringing them closer to tourists, picnic tables, and waste bins.

Foraging Patterns Comparative data on the activity budgets of the two study groups are presented in Figure 4. The commensal white-faced capuchins spend most of their time at rest (32.69%), followed by feeding (27.35%), social interactions (20.41%), and travel (19.27%). The control group places a slightly higher emphasis on social interactions (32.66%), dividing the remainder of their time among rest (23.56%), travel (21.8%), and feeding (21.14%). The two study troops do not significantly differ in any aspect of their activity budgets (feed: Kruskal–Wallis H 5 1.25, P 5 0.263; rest: H 5 1.85, P 5 0.174, N 5 39 social: H 5 0.25, P 5 0.620; travel: H 5 0.01, P 5 0.932; N 5 39 for all categories). Wild-Foraged Foods When provisioned foods are not immediately available, the human-commensal troop forages for wild plant and animal foods in nearly identical proportions to those seen in the control troop (see Fig. 5). When only wild-foraged foods are considered, the two troops significantly differed only in their use of leaves (Kruskal–Wallis H 5 10.03, P 5 0.002, N 5 48). DISCUSSION ´ are surviving The white-faced capuchins at Curu in a highly modified environment primarily through

TABLE IV. A Comparison of the General Dietary Categories Used by the Two Study Troops, Displayed as Percentage of Total Diet and Rate of Consumption Per Hour Commensal troop

Wild-feeding troop

Percentage

Rate per hour

Percentage

Rate per hour

Kruskal–Wallis

69.11

20.975

24.44

3.273

Flowers

1.80

0.546

2.24

0.264

Leaves

2.02

0.615

1.25

0.165

Exudates

0.57

0.174

3.74

0.496

23.81

7.242

68.33

9.058

Other invertebrates

0.43

0.13

0.00

0.00

Shoots

0.29

0.13

0.00

0.00

Vertebrates

0.10

0.13

0.00

0.00

Non-natural foods

1.88

0.031

0.00

0.00

H 5 27.98 P 5 0.00 H 5 1.90 P 5 0.168 H 5 10.18 P 5 0.001 H 5 0.01 P 5 0.933 H 5 0.63 P 5 0.426 H 5 7.96 P 5 0.005 H 5 7.96 P 5 0.005 H 5 2.04 P 5 0.153 H 5 12.15 P 5 0.000

Fruit

Insects

N 5 48 and df 5 48 for all tests. The category ‘‘insects’’ here includes insects, larvae/caterpillars, and spiders, while ‘‘other invertebrates’’ was used for snails, crabs, clams, or slugs. Although the wild-feeding troop was never observed feeding on noninsect invertebrates, shoots, vertebrate prey, or nonnatural foods, vertebrate predation in the commensal troop was sufficiently low as to show no significant difference between the two troops for this food category.

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80 70

Commensal Troop Wild-feeding Troop

60 50 40 30 20 10 0 Exudates

Fig. 3. Percent of non-natural foods in total monthly diet of the commensal troop over the study period (January 2006–December 2007).

Fig. 4. Activity budgets of the two study troops. There were no significant differences in any category (Po0.05).

the use of novel food resources. The prediction that the human-commensal troop would maintain a more frugivorous diet than the wild-feeding troop is supported by these data. Roughly 70% of the commensal troops’ total diet is devoted to fruit, a level considerably higher than the 25% fruit used by the wild-feeding troop. Food-enhanced primate groups have typically been found to have small home ranges and reduced travel and feeding time [Altmann & Muruthi, 1988; Kogenezawa & Imaki, 1999; Sabbatini et al., 2006; Saj et al., 1999; Strum, 2010]. Despite access to plentiful, high-calorie provisioned foods, the human-commensal troop at this site maintains a much larger territory and has a comparable activity budget to the wild-feeding control troop. Short of halting all provisioning at the study site, it is difficult to conclude whether the monkeys

Flowers

Fruits

Insects

Leaves

Fig. 5. Comparison of only wild-foraged foods between the two study troops, shown here as a proportion of their mean annual diet. The two groups significantly differed only in leaf consumption (Po0.05).

are dependent on provisioning for their dietary needs. However, if the human-commensal troop has become reliant on human foods, it is reasonable to expect a significant change in their foraging patterns from those seen in wild-feeding troops. The high proportion of anthropogenic foods in their diet notwithstanding, the data indicate that the commensal troop maintains similar foraging patterns to those of the control troop. This finding confirms previous suggestions that crop-raiding monkeys supplement—rather than replace—their existing diets [De Freitas et al., 2008; Naughton-Treves et al., 1998]. Crop-raiding among primates may be viewed as an ecological adaptation to the loss of natural food resources [Hockings et al., 2009; Naughton-Treves et al., 1998; Strum, 2010]. Intentionally provisioned animals, especially, often have thicker coats and are fatter [Forthman Quick & Demment, 1988], sometimes to the point of obesity [O’Leary & Fa, 1993]. However, the observed benefits of provisioning on primates are often ‘‘misleading and ephemeral’’ [Altmann & Muruthi, 1988, p 218]. At best, incorporating human foods into the diet is a temporarily successful strategy that requires the continued tolerance of landowners. ´’s acceptance of some crop destruction by wildlife Curu and their recognition of monkeys as key members of the forest community are certainly instrumental to the survival of healthy capuchin populations in this situation. There are a number of potential consequences of relying on provisioning for survival in anthropogenic habitats. In addition to the coconut and oil palm crops used by the human-commensal troop at this site, Cebus species are known to raid maize (Zea mays), sugar cane (Saccharum officinarum), mango, and banana plantations [Baker & Schutt, 2005; De Freitas et al., 2008; Gonzalez-Kirchner & Sainz de la

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Maza, 1998]. Destruction of a significant proportion of such crops will certainly lead to conflict with farmers that may include patrolling fields, trapping and removal of primates, and hunting monkeys as agricultural pests [De Freitas et al., 2008; Hill, 2005; Naughton-Treves et al., 1998; Newmark et al., 1994]. The perception of landowners often does not accurately represent actual economic loss caused by primate crop-raiding [Riley & Priston, 2010; Siex & Struhsaker, 1999], and monkeys may be persecuted even when they have relatively little impact on agricultural output. Raiding foods from homes, garbage bins, or harassing tourists is likely to lead to even more persecution from humans, as this behavior creates the risk of monkey bites and disease transmission [Fuentes & Gamerl, 2005; Southwick et al., 2005]. ´ , the levels of monkey–human interacAt Curu tion are in constant flux. The proportion of human foods in the commensal white-faced capuchin diet increased dramatically over the 2-year study period. The animals have been provisioned daily for years, but now additional bananas are thrown any time both monkeys and tourists are present. Despite numerous signs forbidding visitors to feed the wildlife, handouts from tourists are also becoming more common. Although these monkeys do not yet interact physically with humans, it is only a matter of time before they learn to harass tourists for a handout. Future research with this population will expand to include more study troops, a more robust sample size, and longitudinal data as tourism at the refuge continues to grow. Ultimately, the results of this project may be used to inform local management strategies on ways to reduce crop-raiding and human provisioning at this study site. Small plantations of indigenous, preferred food sources, for example, would simultaneously attract the monkeys for tourist viewing and remove the growing association between humans and food handouts. Understanding the synergistic effects of activity, ranging, and diet are vital for the conservation of Neotropical primates. The findings presented here suggest that white-faced capuchins survive in modified habitats by exploiting alternative food resources, with little modification of activity pat´ ’s monkeys, at present, do not terns. Although Curu appear to be dependent on provisioned resources for their survival, their focus on dietary modifications suggests that they could easily succumb to a dependence on anthropogenic resources in modified habitats. ACKNOWLEDGMENTS This study was conducted through generous financial support from Earthwatch Institute, Conservation International, and The Ohio State University. Caspar Harris, Carolina Orozco Zamora, and

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