Abstract
Anthropogenic influence is expanding, threatening primate taxa worldwide. With wildlife tourism a burgeoning industry, understanding human–primate interactions is key in avoiding primate defaunation. We observed interactions between humans and a group of wild Panamanian white-faced capuchin monkeys (Cebus imitator) at Curú Wildlife Refuge, Costa Rica, in June and July, 2019, and compared our findings with findings for the same group in May–October of 2006 and 2007, when the group received more provisioning. We recorded all occurrences of human–primate interactions in 323 15-min samples over 42 consecutive days. We found that capuchins initiated approximately twice as many interactions as humans did (a significant difference). We also found a strong positive correlation between engaging behaviors exhibited by humans and capuchin agonistic behaviors. Capuchins spent significantly more time engaging in moderate behaviors (snatch food, snatch item, vigilance, vocalization) and less time not interacting with humans, in the presence of tourists and staff, than in the presence of staff only. Time spent in moderate and intense behaviors (approach, beg, chase, offer, take food, threat) was lower in 2019 than in 2006 and 2007. These findings suggest that reducing engaging behaviors by humans may reduce primate agonistic behaviors, and that human group composition affects human–primate interactions. The reduction in moderate and intense behaviors between studies also suggests that reducing direct provisioning could reduce the frequency and intensity of human–primate interactions in tourist sites.
Similar content being viewed by others
References
Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49(3–4), 227–266.
Altmann, J., & Muruthi, P. (1988). Differences in daily life between semiprovisioned and wild-feeding baboons. American Journal of Primatology, 15(3), 213–221.
Becker, D. J., Streicker, D. G., & Altizer, S. (2015). Linking anthropogenic resources to wildlife–pathogen dynamics: A review and meta-analysis. Ecology Letters, 18(5), 483–495.
Behie, A. M., Pavelka, M. S., & Chapman, C. A. (2010). Sources of variation in fecal cortisol levels in howler monkeys in Belize. American Journal of Primatology, 72(7), 600–606.
Boubli, J. P., Rylands, A. B., Farias, I. P., Alfaro, M. E., & Alfaro, J. L. (2012). Cebus phylogenetic relationships: A preliminary reassessment of the diversity of the untufted capuchin monkeys. American Journal of Primatology, 74(4), 381–393.
Campos, F. A., Bergstrom, M. L., Childers, A., Hogan, J. D., Jack, K. M., Melin, A. D., Mosdossy, K. N., Myers, M. S., Parr, N. A., Sargeant, E., Schoof, V. A. M., Fedigan, L. M. (2014) Drivers of home range characteristics across spatiotemporal scales in a Neotropical primate, Cebus capucinus. Animal Behaviour 91:93–109.
Dirzo, R., Young, H. S., Galetti, M., Ceballos, G., Isaac, N. J., & Collen, B. (2014). Defaunation in the Anthropocene. Science, 345(6195), 401–406.
Estrada, A., Garber, P. A., Rylands, A. B., Roos, C., Fernandez-Duque, E., et al (2017). Impending extinction crisis of the world’s primates: Why primates matter. Science Advances, 3(1), e1600946.
Fragaszy, D. M., Visalberghi, E., & Fedigan, L. M. (2004). The complete capuchin: The biology of the genus Cebus. Cambridge University Press.
Fuentes, A., Kalchik, S., Gettler, L., Kwiatt, A., Konecki, M., & Jones-Engel, L. (2008). Characterizing human–macaque interactions in Singapore. American Journal of Primatology, 70(9), 879–883.
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(3), 214–222.
IBM Corp (2019). IBM SPSS Statistics for Windows, Version 26.0. IBM Corp.
Instituto Meteorológico Nacional. (2019). Interactive map. Retrieved from: https://www.imn.ac.cr/en/web/imn/inicio. Accessed 26 August 2019.
Jones-Engel, L., Engel, G. A., Heidrich, J., Chalise, M., Poudel, N., et al (2006). Temple monkeys and health implications of commensalism, Kathmandu, Nepal. Emerging Infectious Diseases, 12(6), 900.
Jones-Engel, L., Engel, G. A., Schillaci, M. A., Froehlich, J., Paputungan, U., & Kyes, R. C. (2004). Prevalence of enteric parasites in pet macaques in Sulawesi, Indonesia. American Journal of Primatology, 62(2), 71–82.
Kauffman, L. (2014). Interactions between tourists and white-faced monkeys (Cebus capucinus) at Manuel Antonio National Park, Quepos, Costa Rica. In A. E. Russon & J. Wallis (Eds.), Primate tourism: A tool for conservation? (pp. 215–229). Cambridge University Press.
Kurita, H. (2014). Provisioning and tourism in free-ranging Japanese macaques. In A. E. Russon & J. Wallis (Eds.), Primate tourism: A tool for conservation? (pp. 44–56). Cambridge University Press.
Lane, K. E., Lute, M., Rompis, A., Wandia, I. N., Putra, I. A., et al (2010). Pests, pestilence, and people: The long-tailed macaque and its role in the cultural complexities of Bali. In S. Gursky & J. Supriatna (Eds.), Indonesia primates, Developments in Primatology: Progress and Prospects (pp. 235–248). Springer Science+Business Media.
Maestripieri, D., & Hoffman, C. L. (2011). Chronic stress, allostatic load, and aging in nonhuman primates. Development and Psychopathology, 23(4), 1187–1195.
Maréchal, L., Levy, X., Meints, K., & Majolo, B. (2017). Experience-based human perception of facial expressions in Barbary macaques (Macaca sylvanus). PeerJ, 5, e3413.
Maréchal, L., MacLarnon, A., Majolo, B., & Semple, S. (2016). Primates’ behavioural responses to tourists: Evidence for a trade-off between potential risks and benefits. Scientific Reports, 6, 32465.
Maréchal, L., & McKinney, T. (2020). The (mis)use of the term “commensalism” in primatology. International Journal of Primatology, 41(8), 1–4.
Maréchal, L., Semple, S., Majolo, B., & MacLarnon, A. (2016). Assessing the effects of tourist provisioning on the health of wild Barbary macaques in Morocco. PLoS ONE, 11(5), e0155920.
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.
Marty, P. R., Balasubramaniam, K. N., Kaburu, S. S., Hubbard, J., Beisner, B., et al (2020). Individuals in urban dwelling primate species face unequal benefits associated with living in an anthropogenic environment. Primates, 61(2), 249–255.
Matheson, M. D., Sheeran, L. K., Li, J. H., & Wagner, R. S. (2006). Tourist impact on Tibetan macaques. Anthrozoös, 19(2), 158–168.
McKinney, T. (2010). Social and ecological impact of anthropogenic disturbance on the sympatric white-faced capuchin (Cebus capucinus) and mantled howler monkey (Alouatta palliata). MA dissertation, Ohio State University.
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(5), 439–448.
McKinney, T. (2014). Species-specific responses to tourist interactions by white-faced capuchins (Cebus imitator) and mantled howlers (Alouatta palliata) in a Costa Rican wildlife refuge. International Journal of Primatology, 35(2), 573–589.
McKinney, T. (2015). A classification system for describing anthropogenic influence on alloprimate populations. American Journal of Primatology, 77(7), 715–726.
McKinney, T. (2016). Ecotourism. The International Encyclopedia of Primatology (pp. 1–2). John Wiley & Sons.
McKinney, T., Westin, J. L., & Serio-Silva, J. C. (2015). Anthropogenic habitat modification, tourist interactions and crop-raiding in howler monkeys. In M. Kowalewski, P. Garber, L. Cortés-Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler monkeys, Developments in Primatology: Progress and Prospects (pp. 281–311). Springer Science+Business Media.
McLennan, M. R., Spagnoletti, N., & Hockings, K. J. (2017). The implications of primate behavioral flexibility for sustainable human–primate coexistence in anthropogenic habitats. International Journal of Primatology, 38(2), 105–121.
Mittermeier, R. A., Wilson, D. E. and Rylands, A. B. (Eds.) (2013). Handbook of the mammals of the world: Primates. Lynx Edicions. pp. 412–413.
Muehlenbein, M. P., Ancrenaz, M., Sakong, R., Ambu, L., Prall, S., et al (2012). Ape conservation physiology: Fecal glucocorticoid responses in wild Pongo pygmaeus morio following human visitation. PLoS ONE, 7(3), e33357.
Rose, L. M., Perry, S., Panger, M. A., Jack, K., Manson, J. H., Gros-Louis, J., Mackinnon, K. C. & Vogel, E. (2003). Interspecific interactions between Cebus capucinus and other species: Data from three Costa Rican sites. International Journal of Primatology, 24(4), 759–796.
Sabbatini, G., Stammati, M., Tavares, M. C. H., Giuliani, 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(2–4), 272–283.
Sapolsky, R. (2014). Some pathogenic consequences of tourism for nonhuman primates. In A. E. Russon & J. Wallis (Eds.), Primate tourism: A tool for conservation? (pp. 147–154). Cambridge University Press. https://doi.org/10.1017/CBO9781139087407.011.
Suzin, A., Back, J. P., Garey, M. V., & Aguiar, L. M. (2017). The relationship between humans and capuchins (Sapajus sp.) in an urban green area in Brazil. International Journal of Primatology, 38(6), 1058–1071.
Thatcher, H. R., Downs, C. T., & Koyama, N. F. (2018). Using parasitic load to measure the effect of anthropogenic disturbance on vervet monkeys. EcoHealth, 15(3), 676–681.
Thatcher, H. R., Downs, C. T., & Koyama, N. F. (2019). Anthropogenic influences on the time budgets of urban vervet monkeys. Landscape and Urban Planning, 181, 38–44.
Van Hulle, M., & Vaughan, C. (2009). The effect of human development on mammal populations of the Punta Leona private wildlife refuge, Costa Rica. Revista de biologia tropical, 57(1–2), 441–449.
Vogel, E. R., & Janson, C. H. (2007). Predicting the frequency of food-related agonism in white-faced capuchin monkeys (Cebus capucinus), using a novel focal-tree method. American Journal of Primatology, 69(5), 533–550.
Webb, S. E., & McCoy, M. B. (2014). Ecotourism and primate habituation: Behavioral variation in two groups of white-faced capuchins (Cebus capucinus) from Costa Rica. Revista de biologia tropical, 62(3), 909–918.
Westin, J. L. (2017). Habituation to tourists: Protective or harmful. In K. M. Dore, E. P. Riley, & A. Fuentes (Eds.), Ethnoprimatology: A practical guide to research at the human-nonhuman primate interface (pp. 15–28). Cambridge University Press.
Williamson, E. A., & Fiestner, A. T. C. (2003). Habituating primates: Process, techniques variables, and ethics. In J. M. Setchell & D. J. Curtis (Eds.), Field and laboratory methods in primatology: A practical guide (pp. 25–39). Cambridge University Press.
Zhang, P. (2011). A non-invasive study of alopecia in Japanese macaques Macaca fuscata. Current Zoology, 57(1), 26–35.
Acknowledgments
The authors thank the Schutt family and the staff of Curú Wildlife Refuge. The 2019 study presented here was supported by a grant from Primate Conservation, Inc. The 2006–2007 study was supported by Earthwatch Insitute, Primate Conservation, Inc., and the Ohio State University. We also thank Joanna Setchell and the two anonymous reviewers for their helpful notes on earlier drafts of the manuscript.
Author information
Authors and Affiliations
Contributions
TM conceived and designed the research protocol. NLM conducted fieldwork in 2019, TM conducted fieldwork in 2006 and 2007. NLM and TM analysed the data, and wrote the manuscipt.
Corresponding author
Additional information
Handling Editor: Joanna Setchell
Rights and permissions
About this article
Cite this article
Mansell, N.L., McKinney, T. Interactions Between Humans and Panamanian White-Faced Capuchin Monkeys (Cebus imitator). Int J Primatol 42, 548–562 (2021). https://doi.org/10.1007/s10764-021-00218-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10764-021-00218-2