Abstract
Primates inhabiting human-modified habitats often complement their diets with cultivated species. Although this flexible foraging behavior reduces feeding stress in animals inhabiting small or low-quality habitats, its potential economic costs may promote negative human–nonhuman primate interactions. It is critical to assess the importance of cultivated species to primate diets, the factors influencing their exploitation, and their associated economic costs to evaluate the conservation value of cultivated species and the impact of crop feeding on human–nonhuman primate coexistence. Based on a 30-months study of three groups of brown howlers (Alouatta guariba clamitans) inhabiting <10-ha forest fragments in Rio Grande do Sul State, southern Brazil, and semistructured interviews with landowners, we assessed 1) the cultivated species used as food sources, 2) the relationship between food availability and crop feeding, and 3) the potential economic costs of crop feeding and their impact on landowner–howler coexistence. Brown howlers exploited six cultivated species as fruit or seed sources. This exploitation was concentrated on ripe fruit of Psidium guajava, Citrus reticulata, Diospyros kaki, and Eriobotrya japonica, which together accounted for up to 32% of total feeding records during some months. Availability predicted fruit consumption for three of these species. The overall availability of cultivated fruit also predicted its consumption, whereas overall wild fruit availability did not. Despite potential economic costs of crop feeding (US$320–US$1141 per year), landowners reported no conflict with howlers arising from their behavior, an amicable response that supports the conservation value of cultivated plants in different landscape elements of the anthropogenic matrix.
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References
Agostini, I., Holzmann, I., & Di Bitetti, M. S. (2010). Are howler monkey species ecologically equivalent? Trophic niche overlap in syntopic Alouatta guariba clamitans and Alouatta caraya. American Journal of Primatology, 72, 173–186.
Altmann, J. (1974). Observational study of behavior: sampling methods. Behavior, 49, 227–267.
Anderson, J. J., Rowcliffe, M., & Cowlishaw, G. (2007). Does the matrix matter? A forest primate in a complex agricultural landscape. Biological Conservation, 135, 212–222.
Asensio, N., Arroyo-Rodríguez, V., Dunn, J. C., & Cristóbal-Azkarate, J. (2009). Conservation value of landscape supplementation for howler monkeys living in forest patches. Biotropica, 41, 768–773.
Behie, A. M., & Pavelka, M. S. M. (2015). Fruit as a key factor in howler monkey population density: Conservation implications. In M. Kowalewski, P. A. Garber, L. Cortés-Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler monkeys: Behavior, ecology, and conservation (pp. 357–382). New York: Springer Science + Business Media.
Bicca-Marques, J. C. (2003). How do howler monkeys cope with habitat fragmentation? In L. K. Marsh (Ed.), Primates in fragments: Ecology and conservation (pp. 283–303). New York: Kluwer Academic/Plenum Publishers.
Bicca-Marques, J. C. (2009). Integrando ensino, pesquisa e extensão para resolver um problema de conservação ambiental e saúde pública. In J. L. N. Audy & M. C. Morosini (Eds.), Inovação, universidade e relação com a sociedade: Boas práticas na PUCRS (pp. 119–130). Porto Alegre: EDIPUCRS.
Bicca-Marques, J. C., & Calegaro-Marques, C. (1994). Exotic plant species can serve as staple food sources for wild howler populations. Folia Primatologica, 63, 209–211.
Bicca-Marques, J. C., Muhle, C. B., Prates, H. M., Oliveira, S. G., & Calegaro-Marques, C. (2009). Habitat impoverishment and egg predation by Alouatta caraya. International Journal of Primatology, 30, 743–748.
Buss, G., Romanowski, H. P., & Becker, F. G. (2015). O bugio que habita a mata e a mente dos moradores de Itapuã-Uma análise de percepção ambiental no entorno do Parque Estadual de Itapuã, Viamão, RS. Revista Biociências, 21, 14–28.
Campbell-Smith, G., Simanjorang, H. V. P., Leader-Williams, N., & Linkie, M. (2010). Local attitudes and perceptions toward crop-raiding by orangutans (Pongo abelii) and other nonhuman primates in northern Sumatra, Indonesia. American Journal of Primatology, 72, 866–876.
Chakravarthy, A. K., & Thyagaraj, N. E. (2005). Coexistence of bonnet macaques (Macaca radiata radiata Geoffroy) with planters in the cardamom (Elettaria cardamomum Maton) and coffee (Coffea arabica Linnaeus) plantations of Karnataka, south India: Hospitable or hostile? In J. D. Paterson & J. Wallis (Eds.), Commensalism and conflict: The human–primate interface (pp. 271–293). Norman, OK: The American Society of Primatologists.
Chalise, M. K., & Johnson, R. L. (2005). Farmer attitudes toward the conservation of “pest” monkeys: The view from Nepal. In J. D. Paterson & J. Wallis (Eds.), Commensalism and conflict: The human–primate interface (pp. 223–239). Norman, OK: The American Society of Primatologists.
Chapman, C. A. (1987). Flexibility in diets of three species of Costa Rican primates. Folia Primatologica, 49, 90–105.
Chapman, C. A., & Fedigan, L. M. (1990). Dietary differences between neighboring Cebus capucinus groups: Local traditions, food availability or responses to food profitability? Folia Primatologica, 54, 177–186.
Chaves, Ó. M., & Bicca-Marques, J. C. (2013). Dietary flexibility of the brown howler monkey throughout its geographic distribution. American Journal of Primatology, 75, 16–29.
Chaves, Ó. M., & Bicca-Marques, J. C. (2016). Feeding strategies of brown howler monkeys in response to variations in food availability. PLoS ONE, 11, e0145819.
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 (pp. 339–349). Norman, OK: The American Society of Primatologists.
Crawley, M. J. (2012). The R book. Hoboken, NJ: John Wiley & Sons.
Enari, H., & Suzuki, T. (2010). Risk of agricultural and property damage associated with the recovery of Japanese monkey populations. Landscape and Urban Planning, 97, 83–91.
Engeman, R. M., Laborde, J. E., Constantin, B. U., Shwiff, S. A., Hall, P., et al. (2010). The economic impacts to commercial farms from invasive monkeys in Puerto Rico. Crop Protection, 29, 401–405.
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.
Fournier, L. (1974). Un método cuantitativo para la medición de las características fenológicas en árboles. Turrialba, 24, 422–423.
Freitas, C. H., Setz, E. Z., Araújo, A. R. B., & Gobbi, N. (2008). Agricultural crops in the diet of bearded capuchin monkeys, Cebus libidinosus Spix (Primates: Cebidae), in forest fragments in southeast Brazil. Revista Brasileira de Zoologia, 25, 32–39.
Ganzhorn, J. U., & Abraham, J. P. (1991). Possible role of plantations for lemur conservation in Madagascar: Food for folivorous species. Folia Primatologica, 56, 171–176.
Gérard, A., Ganzhorn, J. U., Kull, C. A., & Carrière, S. M. (2015). Possible roles of introduced plants for native vertebrate conservation: The case of Madagascar. Restoration Ecology, 23, 768–775.
Goulart, V. D. L. R., Teixeira, C. P., & Young, R. J. (2010). Analysis of callouts made in relation to wild urban marmosets (Callithrix penicillata) and their implications for urban species management. European Journal of Wildlife Research, 56, 641–649.
Guzmán, A., Link, A., Castillo, J. A., & Botero, J. E. (2016). Agroecosystems and primate conservation: Shade coffee as potential habitat for the conservation of Andean night monkeys in the northern Andes. Agriculture, Ecosystems & Environment, 215, 57–67.
Hemingway, C. A., & Bynum, N. (2005). The influence of seasonality on primate diet and ranging. In D. K. Brockman & C. P. van Schaick (Eds.), Seasonality in primates: Studies of living and extinct human and non-human primates (pp. 57–104). Cambridge: Cambridge University Press.
Hill, C. M. (1997). Crop-raiding by wild vertebrates: The farmer’s perspective in an agricultural community in western Uganda. International Journal of Pest Management, 43, 77–84.
Hill, C. M. (2000). Conflict of interest between people and baboons: Crop raiding in Uganda. International Journal of Primatology, 21, 299–315.
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 (pp. 40–59). Norman, OK: The American Society of Primatologists.
Hill, C. M. (2015). Perspectives of “conflict” at the wildlife–agriculture boundary: 10 years on. Human Dimensions of Wildlife, 20, 296–301.
Hockings, K. J., & McLennan, M. R. (2012). From forest to farm: Systematic review of cultivar feeding by chimpanzees-management: Implications for wildlife in anthropogenic landscapes. PLoS ONE, 7, e33391.
Hockings, K. J., Anderson, J. R., & Matsuzawa, T. (2009). Use of wild and cultivated foods by chimpanzees at Bossou, Republic of Guinea: Feeding dynamics in a human-influenced environment. American Journal of Primatology, 71, 636–646.
Hothorn, T., Bretz, F., & Westfall, P. (2008). Simultaneous inference in general parametric models. Biometrical Journal, 50, 346–363.
Jones, C. B. (2005). Behavioral flexibility in primates: Causes and consequences. New York: Springer Science + Business Media.
Julliot, C. (1996). Fruit choice by red howler monkeys (Alouatta seniculus) in a tropical rain forest. American Journal of Primatology, 40, 261–282.
Lambert, J. E. (2011). Primate nutritional ecology: Feeding biology and diet at ecological and evolutionary scales. In C. J. Campbell, A. Fuentes, K. C. Mackinnon, M. Panger, S. K. Bearder, & R. Stumpf (Eds.), Primates in perspective (pp. 512–522). Oxford: Oxford University Press.
Lee, P. C., & Priston, N. E. C. (2005). Human attitudes to primates: Perceptions of pests, conflict and consequences for primate conservation. In J. D. Paterson & J. Wallis (Eds.), Commensalism and conflict: The human–primate interface (pp. 1–23). Norman, OK: The American Society of Primatologists.
Ludwig, G., Aguiar, L. M., & Rocha, V. J. (2006). Comportamento de obtenção de Manihot esculenta Crantz (Euphorbiaceae), mandioca, por Cebus nigritus (Goldfuss) (Primates, Cebidae) como uma adaptação alimentar em períodos de escassez. Revista Brasileira de Zoologia, 23, 888–890.
Maibeche, Y., Moali, A., Yahi, N., & Menard, N. (2015). Is diet flexibility an adaptive life trait for relictual and peri-urban populations of the endangered primate Macaca sylvanus? PLoS ONE, 10, e0118596.
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.
McKinney, T. (2015). A classification system for describing anthropogenic influence on nonhuman primate populations. American Journal of Primatology, 77, 715–726.
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. A. Garber, L. Cortés-Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler monkeys: Behavior, ecology, and conservation (pp. 281–311). New York: Springer Science + Business Media.
McLennan, M. R. (2013). Diet and feeding ecology of chimpanzees (Pan troglodytes) in Bulindi, Uganda: Foraging strategies at the forest-farm interface. International Journal of Primatology, 34, 585–614.
McLennan, M. R., & Hockings, K. J. (2014). Wild chimpanzees show group differences in selection of agricultural crops. Scientific Reports, 4, 5956.
McLennan, M. R., & Hockings, K. J. (2016). The aggressive apes? Causes and contexts of great ape attacks on local persons. In F. M. Angelici (Ed.), Problematic wildlife: A cross-disciplinary approach (pp. 373–394). Cham: Switzerland: Springer International Publishing.
McLennan, M. R., Hyeroba, D., Asiimwe, C., Reynolds, V., & Wallis, J. (2012). Chimpanzees in mantraps: Lethal crop protection and conservation in Uganda. Oryx, 46, 598–603.
Mikich, S. B., & Liebsch, D. (2014). Damage to forest plantations by tufted capuchins (Sapajus nigritus): Too many monkeys or not enough fruits? Forest Ecology and Management, 314, 9–16.
Milton, K. (1981). Food choice and digestive strategies of two sympatric primate species. American Naturalist, 117, 476–495.
Naughton-Treves, L. (1997). Farming the forest edge: Vulnerable places and people around Kibale National Park, Uganda. Geographical Review, 87, 27–46.
Naughton-Treves, L. (1998). Predicting patterns of crop damage by wildlife around Kibale National Park, Uganda. Conservation Biology, 12, 156–168.
Naughton-Treves, L., Treves, A., Chapman, C., & Wrangham, R. (1998). Temporal patterns of crop-raiding by primates: Linking food availability in croplands and adjacent forest. Journal of Applied Ecology, 35, 596–606.
Newmark, W. D., Manyanza, D. N., Gamassa, D. M., & Sariko, H. I. (1994). The conflict between wildlife and local people living adjacent to protected areas in Tanzania: Human density as a predictor. Conservation Biology, 8, 249–255.
Onderdonk, D. A., & Chapman, C. A. (2000). Coping with forest fragmentation: The primates of Kibale National Park, Uganda. International Journal of Primatology, 21, 587–611.
Paterson, J. D. (2005). Primate and human interaction in Masindi District, Uganda. In J. D. Paterson & J. Wallis (Eds.), Commensalism and conflict: The human–primate interface (pp. 77–89). Norman, OK: The American Society of Primatologists.
Perry, S., & Manson, J. H. (2003). Traditions in monkeys. Evolutionary Anthropology, 12, 71–81.
Prates, H. M., & Bicca-Marques, J. C. (2011). Vivendo no limite? Dieta de um grupo de bugios-pretos (Alouatta caraya) habitante de um pomar. In F. R. de Melo & I. Mourthé (Eds.), A primatologia no Brasil (Vol. 11, pp. 77–91). Belo Horizonte: Sociedade Brasileira de Primatologia.
R Core Team. (2016). R: A language and environment for statistical computing. R Foundation for Statistical Computing. http://www.R-project.org/ (Accessed March 16, 2016).
Ribeiro, M. C., Metzger, J. P., Martensen, A. C., Ponzoni, F. J., & Hirota, M. M. (2009). The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation, 142, 1141–1153.
Righini, N., Garber, P. A., & Rothman, J. M. (2015). The effects of plant nutritional chemistry on food selection of Mexican black howler monkeys (Alouatta pigra): The role of lipids. American Journal of Primatology. doi:10.1002/ajp.22524.
Saj, T. L., Sicotte, P., & Paterson, J. D. (2001). The conflict between vervet monkeys and farmers at the forest edge in Entebbe, Uganda. African Journal of Ecology, 39, 195–199.
Santos, C. V., Morais, M. M., Jr., Oliveira, M. M., Mikich, S. B., Ruiz-Miranda, C. R., & Moore, K. P. L. (2007). Ecologia, comportamento e manejo de primatas invasores e populações-problema. In J. C. Bicca-Marques (Ed.), A primatologia no Brasil (Vol. 10, pp. 101–118). Porto Alegre: Sociedade Brasileira de Primatologia.
Scarano, F. R., & Ceotto, P. (2015). Brazilian Atlantic forest: Impact, vulnerability, and adaptation to climate change. Biodiversity and Conservation, 24, 2319–2331.
Seiler, N., & Robbins, M. M. (2016). Factors influencing ranging on community land and crop raiding by mountain gorillas. Animal Conservation, 19, 176–188.
Setubal, R. B., Boldrini, I. I., & Ferreira, P. M. A. (2011). Campos dos Morros de Porto Alegre. Porto Alegre: Associação Sócio-Ambientalista Igré.
Silver, S. C., Ostro, L. E. T., Yeager, C. P., & Horwich, R. (1998). Feeding ecology of the black howler monkey (Alouatta pigra) in northern Belize. American Journal of Primatology, 45, 263–279.
Tweheyo, M., Hill, C. M., & Obua, J. (2005). Patterns of crop raiding by primates around the Budongo Forest Reserve, Uganda. Wildlife Biology, 11, 237–247.
Acknowledgements
We thank the guest editors Noemi Spagnoletti, Kimberley Hockings, and Matthew McLennan for inviting us to contribute to this special issue. We also thank the guest editors, Joanna M. Setchell, and two anonymous reviewers for constructive reviews of the manuscript; Edalina Fernandes, Eduvaldo Vianna, and Felipe Vianna (Instituto Econsciência) for giving us permission to conduct this research; Danielle Camaratta for providing logistical support in the field; and Regis A. Lahm and Everton L. Quadros (Laboratório de Tratamento de Imagens e Geoprocessamento/PUCRS) for preparing the map of the study region. This study was supported by a grant from the Programa Nacional de Pós-Doutorado of the Brazilian Higher Education Authority/CAPES (PNPD grant no. 2755/2010). OMC was supported by a PNPD postdoctoral fellowship. JCBM thanks the Brazilian National Research Council/CNPq for research fellowships (PQ no. 303154/2009-8 and 303306/2013-0).
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Chaves, Ó.M., Bicca-Marques, J.C. Crop Feeding by Brown Howlers (Alouatta guariba clamitans) in Forest Fragments: The Conservation Value of Cultivated Species. Int J Primatol 38, 263–281 (2017). https://doi.org/10.1007/s10764-016-9927-8
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DOI: https://doi.org/10.1007/s10764-016-9927-8