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Species-Specific Responses to Tourist Interactions by White-Faced Capuchins (Cebus imitator) and Mantled Howlers (Alouatta palliata) in a Costa Rican Wildlife Refuge

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Abstract

Ecotourism shows great potential for primate conservation, but further investigation through an ethnoprimatological lens is vital to understanding species-specific variation in human–nonhuman primate interactions at ecotourism sites. This study measured the rates and types of human–monkey interactions, the participants in these encounters, and the association between tourist numbers and interaction rates with white-faced capuchin monkeys (Cebus imitator) and mantled howlers (Alouatta palliata) at the Curú Wildlife Refuge in western Costa Rica. I collected data through 15-min all-occurrence samples for human–monkey interactions between January 2006 and December 2007. I recorded and analyzed a total of 1949 discrete interactions, representing one tourist group and one non-tourist group for each species. For both species, tourist groups showed more varied and more intense—but not more frequent—human–monkey interactions than the non-tourist groups. White-faced capuchins differed from mantled howlers in their greater frequency and more variable forms of human–monkey interactions. White-faced capuchins also showed a more gregarious pattern of interactions than mantled howlers, with most capuchin interactions being initiated by the monkeys and involving multiple actors. Although mantled howler human interaction rates correlated positively with levels of human traffic, white-faced capuchins did not show this relationship. These findings demonstrate that the differences in human–monkey interactions across species are an important consideration for the management of primate tourism sites. This study suggests that species-specific guidelines for ecotourism would reduce visitor impact on nonhuman primates.

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References

  • Altmann, J. (1974). Observational study of behavior: sampling methods. Behaviour, 49(3–4), 227–266.

    Article  PubMed  CAS  Google Scholar 

  • Altmann, J., & Muruthi, P. (1988). Differences in daily life between semiprovisioned and wild-feeding baboons. American Journal of Primatology, 15, 213–221.

    Article  Google Scholar 

  • Arroyo-Rodríguez, V., & Mandujano, S. (2006). Forest fragmentation modifies habitat quality for Alouatta palliata. International Journal of Primatology, 27(4), 1079–1096.

    Article  Google Scholar 

  • Baker, M., & Schutt, A. (2005). Managing monkeys and mangos. In J. D. Paterson & J. Wallis (Eds.), Commensalism and conflict: The human-primate interface. Norman: The American Society of Primatologists.

    Google Scholar 

  • Behie, A. M., Pavelka, M. S. M., & Chapman, C. A. (2010). Sources of variation in fecal cortisol levels in howler monkeys in Belize. American Journal of Primatology, 72(7), 600–606.

    PubMed  Google Scholar 

  • Berman, C. M., Li, J., Ogawa, H., Ionica, C., & Yin, H. (2007). Primate tourism, range restriction, and infant risk among Macaca thibetana at Mt. Huangshan, China. International Journal of Primatology, 28, 1123–1141.

    Article  Google Scholar 

  • Bezanson, M. (2009). Life history and locomotion in Cebus capucinus and Alouatta palliata. American Journal of Physical Anthropology, 140, 508–517.

    Article  PubMed  Google Scholar 

  • Brennan, E. J., Else, J. G., & Altmann, J. (1985). Ecology and behaviour of a pest primate: Vervet monkeys in a tourist-lodge habitat. African Journal of Ecology, 23, 35–44.

    Article  Google Scholar 

  • Chapman, C. A., Gillespie, T. R., & Goldberg, T. L. (2005). Primates and the ecology of their infectious disease: how will anthropogenic change affect host-parasite interactions? Evolutionary Anthropology, 14(4), 134–144.

    Article  Google Scholar 

  • Chapman, C. A., & Peres, C. A. (2001). Primate conservation in the new millennium: the role of scientists. Evolutionary Anthropology, 10, 16–33.

    Article  Google Scholar 

  • Chism, J. (2005). Round up the usual suspects: conflict between monkeys and farmers in Ghana and Kenya. In J. D. Paterson & J. Wallis (Eds.), Commensalism and conflict: The human-primate interface. Norman: The American Society of Primatologists.

    Google Scholar 

  • Cowlishaw, G., & Dunbar, R. (2000). Primate conservation biology. Chicago: University of Chicago Press.

    Google Scholar 

  • Da Cunha, R. G. T., & Byrne, R. (2006). Roars of black howler monkeys (Alouatta caraya): Evidence for a function in inter-group spacing. Behaviour, 143(10), 1169–1199.

    Article  Google Scholar 

  • De la Torre, S., Snowdon, C. T., & Bejarano, M. (1999). Preliminary study of the effects of ecotourism and human traffic on the howling behaviour of red howler monkeys, Alouatta seniculus, in Ecuadorian Amazon. Neotropical Primates, 7(3), 84–86.

    Google Scholar 

  • De la Torre, S., Snowdon, C. T., & Bejarano, M. (2000). Effects of human activities on wild pygmy marmosets in Ecuadorian Amazonia. Biological Conservation, 94, 153–163.

    Article  Google Scholar 

  • De Oliveira, V. B., Linares, A. M., Corrȇa, G. L. C., & Chiarello, A. G. (2008). Predation on the black capuchin monkey Cebus nigritus (Primates: Cebidae) by domestic dogs Canis lupus familiaris (Carnivora: Canidae) in the Parque Estadual Serrado Bigadira, Minas Gerais, Brazil. Revista Brasileira de Zoología, 25(2), 376–378.

    Article  Google Scholar 

  • Estrada, A., Raboy, B. E., & Oliveira, L. C. (2012). Agroecosystems and primate conservation in the tropics: a review. American Journal of Primatology, 74, 696–711.

    Article  PubMed  Google Scholar 

  • Fragaszy, D. M., Visalberghi, E., & Fedigan, L. M. (2004). The complete capuchin: The biology of the genus Cebus. Cambridge: Cambridge University Press.

    Google Scholar 

  • Fuentes, A. (2012). Ethnoprimatology and the anthropology of the human-primate interface. Annual Review of Anthropology, 41, 101–117.

    Article  Google Scholar 

  • Fuentes, A., & Gamerl, S. (2005). Disproportionate participation by age/sex class in aggressive interactions between long-tailed macaques and human tourists at Padangtegal Monkey Forest, Bali, Indonesia. American Journal of Primatology, 66, 197–204.

    Article  PubMed  Google Scholar 

  • Fuentes, A., & Hockings, K. J. (2010). The ethnoprimatological approach in primatology. American Journal of Primatology, 72, 841–847.

    Article  PubMed  Google Scholar 

  • Fuentes, A., Shaw, E., & Cortes, J. (2007). Qualitative assessment of macaque tourist sites in Padangtegal, Bali, Indonesia, and the Upper Rock Nature Reserve, Gibraltar. International Journal of Primatology, 28, 1143–1158.

    Article  Google Scholar 

  • Grossberg, R., Treves, A., & Naughton-Treves, L. (2003). The incidental ecotourist: measuring visitor impacts on endangered howler monkeys at a Belizean archaeological site. Environmental Conservation, 30(1), 40–51.

    Article  Google Scholar 

  • Herzog, P., & Vaughan, C. (1998). Conserving biodiversity in the tropics: the role of private nature reserves in Costa Rica. Revista de Biología Tropical, 46(2), 183–190.

    Google Scholar 

  • Hill, C. M. (2005). People, crops, and primates: a conflict of interest. In J. D. Paterson & J. Wallis (Eds.), Commensalism and conflict: The human-primate interface. Norman: The American Society of Primatologists.

    Google Scholar 

  • Hoffman, T. L., & O’Riain, M. J. (2011). The spatial ecology of chacma baboons (Papio ursinus) in a human-modified environment. International Journal of Primatology, 32, 308–328.

    Article  Google Scholar 

  • Horton, L. R. (2009). Economic and social impacts of Costa Rica’s ecotourism boom. Latin American Perspectives, 166(36), 93–107.

    Article  Google Scholar 

  • Hsu, M. J., Kao, C. C., & Agoramoorthy, G. (2009). Interactions between visitors and Formosan macaques (Macaca cyclopis) at Shou-Shan Nature Park, Taiwan. American Journal of Primatology, 71, 214–222.

    Article  PubMed  Google Scholar 

  • Instituto Meteorológico Nacional de Costa Rica (2008) Datos climáticos: Puntarenas. Retrieved from www.imn.ac.cr

  • Jack, K. M., Lenz, B. B., Healan, E., Rudman, S., Schoof, V. A. M., & Fedigan, L. (2008). The effects of observer presence on the behaviour of Cebus capucinus in Costa Rica. American Journal of Primatology, 70, 490–494.

    Article  PubMed  Google Scholar 

  • Klailova, M., Hodgkinson, C., & Lee, P. C. (2010). Behavioral responses of one western lowland gorilla (Gorilla gorilla gorilla) group at Bai Hokou, Central African Republic, to tourists, researchers, and trackers. American Journal of Primatology, 72, 897–906.

    Article  PubMed  Google Scholar 

  • Krüger, O. (2005). The role of ecotourism in conservation: Panacea or Pandora’s box? Biodiversity and Conservation, 14, 579–600.

    Article  Google Scholar 

  • Lee, P. C. (2010). Sharing space: Can ethnoprimatology contribute to the survival of nonhuman primates in human-dominated globalized landscapes? American Journal of Primatology, 72, 925–931.

    Article  PubMed  CAS  Google Scholar 

  • López-Espinosa de los Monteros, R. (2002). Evaluating ecotourism in natural protected areas of La Paz Bay, Baja California Sur, México: Ecotourism or nature-based tourism? Biodiversity and Conservation, 11, 1539–1550.

    Article  Google Scholar 

  • Maréchal, L., Semple, S., Majolo, B., Qarro, M., Heistermann, M., & MacLarnon, A. (2011). Impacts of tourism on anxiety and physiological stress levels in wild male Barbary macaques. Biological Conservation, 144(9), 2188–2193.

    Article  Google Scholar 

  • McCarthy, M. S., Matheson, M. D., Lester, J. D., Sheeran, L. K., Li, J. H., & Wagner, R. S. (2009). Sequences of Tibetan macaque (Macaca thibetana) and tourist behaviors at Mt. Huangshan, China. Primate Conservation, 24, 145–151.

    Article  Google Scholar 

  • McKinney, T. (2011). The effects of provisioning and crop-raiding on the diet and foraging activities of human-commensal white-faced capuchins (Cebus capucinus). American Journal of Primatology, 73, 439–448.

    Article  PubMed  Google Scholar 

  • Michalski, F., & Peres, C. A. (2005). Anthropogenic determinants of primate and carnivore local extinctions in a fragmented forest landscape of southern Amazonia. Biological Conservation, 124, 383–396.

    Article  Google Scholar 

  • Milton, K. (1980). The foraging strategy of howler monkeys: a study in primate economics. New York: Columbia University Press.

    Google Scholar 

  • Muehlenbein, M. P., Martinez, L. A., Lemke, A. A., Ambu, L., Nathan, S., Alsisto, S., & Sakong, R. (2010). Unhealthy travellers present challenges to sustainable primate ecotourism. Travel Medicine and Infectious Disease, 8, 169–175.

    Article  PubMed  Google Scholar 

  • Nakamura, M., & Nishida, T. (2009). Chimpanzee tourism in relation to the viewing regulations at the Mahale Mountains National Park, Tanzania. Primate Conservation, 24, 85–90.

    Article  Google Scholar 

  • O’Leary, H., & Fa, J. E. (1993). Effects of tourists on Barbary macaques at Gibraltar. Folia Primatologica, 61, 77–91.

    Article  Google Scholar 

  • Panger, M. A., Perry, S., Rose, L., Gros-Luis, J., Vogel, E., Mackinnon, K. C., & Baker, M. (2002). Cross-site differences in foraging behavior of white-faced capuchins (Cebus capucinus). American Journal of Physical Anthropology, 119, 52–66.

    Article  PubMed  Google Scholar 

  • Pavelka, M. M. (2002). Resistance to the cross-species perspective in anthropology. In L. D. Wolfe & A. Fuentes (Eds.), Primates face to face: The conservation implications of human-nonhuman primate interconnections. Cambridge: Cambridge University Press.

    Google Scholar 

  • Pavelka, M. S. M., & Knopff, K. H. (2004). Diet and activity in black howler monkeys (Alouatta pigra) in southern Belize: does degree of frugivory influence activity level? Primates, 45, 105–111.

    Article  PubMed  Google Scholar 

  • Riley, E. P. (2007). Flexibility in diet and activity patterns of Macaca tonkeana in response to anthropogenic habitat alteration. International Journal of Primatology, 28(1), 107–133.

    Article  Google Scholar 

  • Rose, L. M. (1998). Behavioral ecology of white-faced capuchins (Cebus capucinus) in Costa Rica. Ph,D. dissertation, Washington University of St. Louis.

  • Ross, C., Srivastava, A., & Pirta, R. S. (1993). Human influences on the population density of Hanuman langurs (Presbytis entellus) and rhesus macaques (Macaca mulatta) in Shimla, India. Biological Conservation, 65, 159–163.

    Article  Google Scholar 

  • Sabbatini, G., Stammati, M., Tavares, M. C. H., Guiliani, M. V., & Visalberghi, E. (2006). Interactions between humans and capuchin monkeys (Cebus libidinosus) in the Parque Nacional de Brasília, Brazil. Applied Animal Behaviour Science, 97, 272–283.

    Article  Google Scholar 

  • Saj, T., Sicotte, P., & Paterson, J. D. (1999). Influence of human food consumption on the time budget of vervets. International Journal of Primatology, 20(6), 977–994.

    Article  Google Scholar 

  • Singh, M., & Rao, N. R. (2004). Population dynamics and conservation of commensal bonnet macaques. International Journal of Primatology, 25(4), 847–859.

    Article  Google Scholar 

  • Singla, S. L., Kaur, M., & Lal, S. (1997). Monkey bites: A public health problem in urban settings. Indian Journal of Public Health, 41(1), 3–5. 24.

    PubMed  CAS  Google Scholar 

  • Sorensen, T. C., & Fedigan, L. M. (2000). Distribution of three monkey species along a gradient of regenerating tropical dry forest. Biological Conservation, 92, 227–240.

    Article  Google Scholar 

  • Sponsel, L. E. (1997). The human niche in Amazonia: Explorations in ethnoprimatology. In W. Kinzey (Ed.), New world primates: Ecology, evolution, and behaviour (pp. 143–165). New York: Aldine de Gruyter.

    Google Scholar 

  • Struhsaker, T. (1999). Primate communities in Africa: Consequences of long-term evolution or the artifact of recent hunting? In J. G. Fleagle, C. Janson, & K. E. Reed (Eds.), Primate communities. Cambridge: Cambridge University Press.

    Google Scholar 

  • Strum, S. C. (2010). The development of primate raiding: implications for management and conservation. International Journal of Primatology, 31, 133–156.

    Article  PubMed Central  PubMed  Google Scholar 

  • Sutherland, W. J. (2007). Future directions for disturbance research. Ibis, 149(Suppl. 1), 120–124.

    Article  Google Scholar 

  • Timm, R. M., Lieberman, D., Lieberman, M., & McClearn, D. (2009). Mammals of Cabo Blanco: history, diversity, and conservation after 45 years of regrowth of a Costa Rican dry forest. Forest Ecology and Management, 258, 997–1013.

    Article  Google Scholar 

  • Treves, A., & Brandon, K. (2005). Tourist impacts on the behaviour of black howling monkeys (Alouatta pigra) at Lamanai, Belize. In J. D. Paterson & J. Wallis (Eds.), Commensalism and conflict: The human-primate interface. Norman: American Society of Primatologists.

    Google Scholar 

  • Treves, A., & Carlson, A. E. (2012). Botfly parasitism and tourism on the endangered black howler monkey of Belize. Journal of Medical Primatology, 41, 284–287.

    Article  PubMed  Google Scholar 

  • Unwin, T., & Smith, A. (2010). Behavioral differences between provisioned and non-provisioned Barbary macaques (Macaca sylvanus). Anthrozoös, 23(2), 109–118.

    Article  Google Scholar 

  • Williamson, E. A., & Feistner, A. T. C. (2003). Habituating primates: Processes, techniques, variables, and ethics. In J. M. Setchell & D. J. Curtis (Eds.), Field and laboratory methods in primatology: A practical guide. Cambridge: Cambridge University Press.

    Google Scholar 

  • Zaldívar, M. E., Rocha, O., Glander, K. E., Aguilar, G., Huertas, A. S., Sánchez, R., & Wong, G. (2004). Distribution, ecology, life history, genetic variation, and risk of extinction of non-human primates from Costa Rica. Revista de Biología Tropical, 52(3), 679–693.

    PubMed  Google Scholar 

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Acknowledgments

I thank the Schutt Family of Refugio Curú for their kindness in allowing me to collect data on their property. This research was generously funded by Earthwatch Institute, Conservation International, and The Ohio State University. Caspar Harris, Carolina Orozco Zamora, and many Earthwatch volunteers 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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  1. Sixth Form Academy, City of Bristol College, St. Stephen’s Road, Soundwell, Bristol, BS16 4RL, UK

    Tracie McKinney

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McKinney, T. Species-Specific Responses to Tourist Interactions by White-Faced Capuchins (Cebus imitator) and Mantled Howlers (Alouatta palliata) in a Costa Rican Wildlife Refuge. Int J Primatol 35, 573–589 (2014). https://doi.org/10.1007/s10764-014-9769-1

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