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Crop Feeding by Brown Howlers (Alouatta guariba clamitans) in Forest Fragments: The Conservation Value of Cultivated Species

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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.

    Article  PubMed  Google Scholar 

  • Altmann, J. (1974). Observational study of behavior: sampling methods. Behavior, 49, 227–267.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • Chapman, C. A. (1987). Flexibility in diets of three species of Costa Rican primates. Folia Primatologica, 49, 90–105.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  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 (pp. 339–349). Norman, OK: The American Society of Primatologists.

    Google Scholar 

  • Crawley, M. J. (2012). The R book. Hoboken, NJ: John Wiley & Sons.

    Book  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    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 

  • Fournier, L. (1974). Un método cuantitativo para la medición de las características fenológicas en árboles. Turrialba, 24, 422–423.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Hill, C. M. (2000). Conflict of interest between people and baboons: Crop raiding in Uganda. International Journal of Primatology, 21, 299–315.

    Article  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 (pp. 40–59). Norman, OK: The American Society of Primatologists.

    Google Scholar 

  • Hill, C. M. (2015). Perspectives of “conflict” at the wildlife–agriculture boundary: 10 years on. Human Dimensions of Wildlife, 20, 296–301.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Hothorn, T., Bretz, F., & Westfall, P. (2008). Simultaneous inference in general parametric models. Biometrical Journal, 50, 346–363.

    Article  PubMed  Google Scholar 

  • Jones, C. B. (2005). Behavioral flexibility in primates: Causes and consequences. New York: Springer Science + Business Media.

    Book  Google Scholar 

  • Julliot, C. (1996). Fruit choice by red howler monkeys (Alouatta seniculus) in a tropical rain forest. American Journal of Primatology, 40, 261–282.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  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 

  • McKinney, T. (2015). A classification system for describing anthropogenic influence on nonhuman primate populations. American Journal of Primatology, 77, 715–726.

    Article  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • McLennan, M. R., & Hockings, K. J. (2014). Wild chimpanzees show group differences in selection of agricultural crops. Scientific Reports, 4, 5956.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Milton, K. (1981). Food choice and digestive strategies of two sympatric primate species. American Naturalist, 117, 476–495.

    Article  Google Scholar 

  • Naughton-Treves, L. (1997). Farming the forest edge: Vulnerable places and people around Kibale National Park, Uganda. Geographical Review, 87, 27–46.

    Article  Google Scholar 

  • Naughton-Treves, L. (1998). Predicting patterns of crop damage by wildlife around Kibale National Park, Uganda. Conservation Biology, 12, 156–168.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • Perry, S., & Manson, J. H. (2003). Traditions in monkeys. Evolutionary Anthropology, 12, 71–81.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • Scarano, F. R., & Ceotto, P. (2015). Brazilian Atlantic forest: Impact, vulnerability, and adaptation to climate change. Biodiversity and Conservation, 24, 2319–2331.

    Article  Google Scholar 

  • Seiler, N., & Robbins, M. M. (2016). Factors influencing ranging on community land and crop raiding by mountain gorillas. Animal Conservation, 19, 176–188.

    Article  Google Scholar 

  • Setubal, R. B., Boldrini, I. I., & Ferreira, P. M. A. (2011). Campos dos Morros de Porto Alegre. Porto Alegre: Associação Sócio-Ambientalista Igré.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

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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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Correspondence to Óscar M. Chaves.

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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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