Abstract
The present study aimed to compare the plant food diet of woolly spider monkeys (Brachyteles arachnoides) inhabiting Intervales State Park in São Paulo, Brazil, with medicinal plant species used by humans in the surrounding areas of the park. The diet of a group of woolly spider monkeys living in an Atlantic forest area was recorded during 43 months of fieldwork. Fifty-three species (87 food items) were recorded. Plant specimens were collected and identified at the University of São Paulo and the Botanical Institute of São Paulo State. Using semi-structured interviews, ethnomedicinal data were also collected from four preselected respondents regarding the human therapeutic value of these plants. The study showed that 24.5% (13/53) of these species are used by residents around the park for medicinal purposes. Of these thirteen, seven species also have validated pharmacological properties, and three are utilized by local residents for similar medicinal purposes. Overlap in the plant food/medicinal diet of woolly spider monkey populations elsewhere were also noted, suggesting potential overlap in their medicinal value for humans and primates. The similarities between the ingestion of plants by primates and their medicinal use by humans provide a bio-rational for the search of bioactive plants in the primate diet. Further detailed investigation of their pharmacological and phytochemical value is warranted.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Altmann J., 1974. Observational study of behavior: sampling methods. Behaviour 49, p227–267.
Altmann, S.A., 1998. Foraging for Survival, Yearling Baboon in Africa. Chicago University of Chicago Press.
Andrade, M.A., Cardoso M.d.G., Gomes M.d.S., de Azeredo C.M.O., Batista L.R., Soares, M.J., Rodrigues L.M.A., Figueiredo A.C.S., 2015. Biological activity of the essential oils from Cinnamodendron dinisii and Siparuna guianensis. Braz. J. the essential oils from Cinnamodendron dinisii and Siparuna guianensis. Braz. J. Microbiol. 46, 189–194.
Ashafa, A.O., Sunmonu T.O., Afolayan, A.J., 2010. Toxicological evaluation of aqueous leaf and berry extracts of Phytolacca dioica L. in male Wistar rats. Food Chem. Toxicol. 48, 1886–1889.
Assumpção, C.T., 1983. Ecological and behavioural information on Brachyteles arach-noides. Primates 24, 584–593.
Baker, M., 1996. Fur rubbing: use of medicinal plants by capuchin monkeys (Cebus capucinus). Am. J. Primatol. 38, 263–270.
Bernard, H.R., 1988. Research Methods in Cultural Anthropology. Sage Publications, London.
Brozek, R.M., 1991. Observacões sobre a ecologia alimentar e a dispersão de sementes pelo muriqui (Brachyteles arachnoides E. Geoffroy, 180. -Cebidae, Primates). Graduate thesis presented to Universidade Estadual Paulista, Rio Claro - SP.
Bueno, R.S., Guevara R., Ribeiro M.C., Culot, L., Bufalo, F.S., Galetti M., 2013. Functional redundancy and complementarities of seed dispersal by the last neotropical megafrugivores. PLoS ONE 8, e56252.
Calvo, T.R., Demarco D., Santos F.V., Moraes, H.P., Bauab T.M., Varanda, E.A., Cólus, I.M., Vilegas W., 2010. Phenolic compounds in leaves of Alchornea triplinervia: anatomical localization, mutagenicity, and antibacterial activity. Nat. Prod. Commun. 5, 1225–1232.
Campos, F.F., Rosa L.H., Cota, B.B., Caligiorne R.B., Rabello, A.L., Alves T.M., Rosa, C.A., Zani C.L., 2008. Leishmanicidal metabolites from Cochliobolus sp., an endophytic fungus isolated from Piptadenia adiantoides (Fabaceae). PLoS Negl. Trop. Dis. 2, 348.
Carrai, V., Borgognini-Tarli, S.M., Huffman M.A., Bardi M., 2003. Increase in tannin consumption by sifaka (Propithecus verreauxi verreauxi) females during the birth season: a case for self-medication in prosimians? Primates 44, 61–66.
Carvalho Jr., O., 1996. Dieta, padrões de atividades e de agrupamento do mono-carvoeiro (Brachyteles arachnoides) no Parque Estadual de Carlos Botelho, SP. Master’s degree thesis presented to Universidade Federal do Pará.
Coelho, A.A., de Paula, J.E., Espíndola, L.S., 2006. Insecticidal activity of cerrado plant extracts on Rhodnius milesi Carcavallo, Rocha, Galvão & Jurberg (Hemiptera: Reduviidae), under laboratory conditions. Neotrop. Entomol. 35, 133–138.
Cousins, D., Huffman M.A., 2002. Medicinal properties in the diet of gorillas: an ethno-pharmacological evaluation. Afr. Study Monogr. 23, 65–89.
de Amorin, A., Borba H.R., Carauta, J.P., Lopes D., Kaplan M.A., 1999. Anthelmintic activity of the latex of Ficus species. J. Ethnopharmacol. 64, 255–258.
De Souza, G.C., Haas A.P., von Poser, G.L., Schapoval E.E., Elisabetsky E., 2004. Ethnopharmacological studies of antimicrobial remedies in the south of Brazil. J. Ethnopharmacol. 90, 135–143.
Di Liberto, M., Svetaz L., Furlán, R.L., Zacchino S.A., Delporte, C., Novoa M.A., Asencio M., Cassels B.K., 2010. Antifungal activity of saponin-rich extracts of Phytolacca dioica and of the sapogenins obtained through hydrolysis. Nat. Prod. Commun. 5, 1013–1018.
Dos Santos L.B.D., Souza J.K., Papassoni B., Borges D.G.L., Junior G.A.D., Souza, J.M.E.D, Carollo C.A., Borges F.D.A., 2013. Efficacy of extracts from plants of the Brazilian Pantanal against Rhipicephalus (Boophilus) microplus. Rev. Bras. Parasitol. Vet. 22, 532–538.
Fischer, D.C., de Amorim G.N.C., Bachiega D., Carvalho C.S., Lupo, F.N., Bonotto S.V., Alves Mde, O., Yogi A., Santi S.M., Avila, P.E., Kirchgatter K., Moreno P.R., 2004. In vitro screening for antiplasmodial activity of isoquinoline alkaloids from Brazilian plant species. Acta Trop. 92, 261–266.
Glander, K.E., 1982. The impact of plant secondary compounds on primate feeding behavior. Am. J. Phys. Anthropol. 25 (Suppl. 3), S1–S18.
Glander, K.E., 1994. Nonhuman primate self-medication with wild plant foods. In: Etkin, N.L. (Ed.), Eating on the Wild side: The Pharmacologic, Ecological, and Social Implications of Using Noncultigens. University of Arizona Press T.s.o., pp. 239–256.
Gottlieb, O.R., de Borin, M.R., Bosisio B.M., 1996. Trends of plant use by humans and nonhuman primates in Amazonia. Am. J. Primatol. 40, 189–195.
Gurgel, L.A., Silva R.M., Santos, F.A., Martins D.T., Mattos, P.O., Rao V.S., 2001. Studies on the antidiarrhoeal effect of dragon’s blood from Croton urucurana. Phytother. Res. 15, 319–322.
Gustafsson, E., Saint Jalme, M., Kamoga D., Mugisha L., Snounou G., Bomsel M.C., Krief S., 2016. Food acceptance and social learning opportunities in semi-free Eastern chimpanzees (Pantroglodytes schweinfurthii). Ethology 122, 158–170.
Hueck, K., 1972. As florestas da América do Sul. Editora Polígono S.A., São Paulo.
Huffman, M.A., Seifu M., 1989. Observations on the illness and consumption of a possibly medicinal plant Vernonia amygdalina by a wild chimpanzee in the Mahale Mountains, Tanzania. Primates 30, 51–63.
Huffman, M.A., 1997. Current evidence for self-medication in primates: a multidis-ciplinary perspective. Yearbk. Phys. Anthropol. 40, 171–200.
Huffman, M.A., 2003. Animal self-medication and ethnomedicine: exploration and exploitation of the medicinal properties of plants. Proc. Nutr. Soc. 62, 371–381.
Huffman, M.A., Gotoh S., Izutsu D., Koshimizu K., Kalunde M.S., 1993. Further observations on the use of the medicinal plant, Vernonia amygdalina (Del) by a wild chimpanzee, its possible effect on parasite load, and its phytochemistry. Afr. Study Monogr. 14, 227–240.
Huffman, M.A., Page J.E., Sukhdeo M.V.K., Gotoh S., Kalunde M.S., Chandrasiri T., Towers G.H.N., 1996. Leaf-swallowing by chimpanzees, a behavioral adaptation for the control of strongyle nematode infections. Int. J. Primatol. 17, 475–503.
Huffman, M.A., Gotoh S., Turner L., Hamai M., Yoshida K., 1997. Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains National Park, Tanzania. Primates 38, 111–125.
Huffman, M.A., Ohigashi H., Kawanaka M., Page J.E., Kirby, G.C., Gasquet M., Murakami A., Koshimizu K., 1998. African great ape self-medication: a new paradigm for treating parasite disease with natural medicines. In: Ebizuka, Y. (Ed.), Towards Natural Medicine Research in the 21st Century. Elsevier Science B.V., Amsterdam, pp. 113–123.
Huffman, M.A., Caton J.M., 2001. Self-induced increase of gut motility and the control of parasitic infections in wild chimpanzees. Int. J. Primatol. 22, 329–346.
Janzen, D.H., 1978. Complications in interpreting the chemical defenses of trees against tropical arboreal plant-eating vertebrates. In: Montgomery, G.G. (Ed.), The Ecology of Arboreal Folivores. Smithsonian Institute Press, Washington D., pp. 73–84.
Kassuya, C.A., Cremoneze A., Barros L.F., Simas, A.S., Lapa, F. da R., Mello-Silva, R., Stefanello M.E., Zampronio, A.R., 2009. Antipyretic and antiinflammatory properties of the ethanolic extract, dichloromethane fraction and costunolide from Magnolia ovata (Magnoliaceae). J. Ethnopharmacol. 124, 369–376.
Kowalewski, M.M., Salzer J.S., Deutsch, J.C., Raño, M., Kuhlenschmidt M.S., Gillespie, T.R., 2010. Black and gold howler monkeys (Alouatta caraya) as sentinels of ecosystem health: patterns of zoonotic protozoa infection relative to degree of human-primate contact. Am. J. Primatol. 71, 1–9.
Krief, S., Martin M., Grellier P., Kasenene J., Sévenet, T., 2004. Novel antimalarial compounds isolated in a survey of self-medicative behavior ofwild chimpanzees in Uganda. Antimicrob. Agents Chemother. 48, 3196–3199.
Krief, S., Hladik, C.M., Haxaire, C., 2005. Ethnomedicinal and bioactive properties of the plants ingested by wild chimpanzees in Uganda. J. Ethnopharmacol. 101, 1–15.
Krief, S., Wrangham R.W., Lestel D., 2006. Diversity of items of low nutritional value ingested by chimpanzees from Kanyawara, Kibale National Park, Uganda: an example of the etho-ethnology of chimpanzees. Soc. Sci. Inf. 45, 227–263.
Kuroshima, K.N., de Campos, F., de Souza, M.M., Yunes R.A., Delle Monache, F., Cechinel Filho, V., 2001. Phytochemical and pharmacological investigations of Virola oleifera leaves. Z. Naturforsch. C 56, 703–706.
Lambert, J.E., 2011. Primate nutritional ecology. Feeding biology and diet at ecological and evolutionary scales. In: Campbell, C., Fuentes A., MacKinnon K., Panger M., Bearder, S. (Eds.), Primates in Perspective. University of Oxford Press, Oxford, pp. 512–522.
Lemos de Sá, R.M., 1988. Situacão de uma populacão de mono-carvoeiro, Brachyte-les arachnoides, em fragmento de Mata Atlântica (MG), e implicacões para sua conservacão. Master’s degree thesis presented to Universidade de Brasília, Brasília.
Lima, Z.P., Calvo T.R., Silva, E.F., Pellizzon C.H., Vilegas W., Brito A.R., Bauab, T.M., Hiruma-Lima, C.A., 2008. Brazilian medicinal plant acts on prostaglandin level and Helicobacter pylori. J. Med. Food 11, 701–708.
Lopes, F.C., Calvo T.R., Vilegas W., Carlos I.Z., 2010. Antiinflammatory activity of Alchornea triplinervia ethyl acetate fraction: inhibition of HO, NO and TNF-a. Pharm. Biol. 48, 1320–1327.
MacIntosh A.J.J., Huffman M.A., 2010. Towards understanding the role of diet in host-parasite interactions in the case of Japanese macaques. In: Nakagawa, F., Nakamichi M., Sugiura, H. (Eds.), The Japanese Macaques. Springer, Tokyo, pp. 323–344.
Martins, M.M., 2008. Fruit diet of Alouatta guariba and Brachyteles arachnoides in Southeastern Brazil: comparison of fruit type, color, and seed size. Primates 49, 1–8.
Medeiros M.F.T., da Fonseca, V.S., Andreata R.H.P., 2004. Plantas medicinais e seus usos pelos sitiantes da Reserva Rio das Pedras, Mangaratiba R., Brasil. Acta Bot. Bras. 18, 391–399.
Milton, K., 1984. Habitat, diet, and activity patterns of free-ranging woolly spider monkeys (Brachyteles arachnoides E. Geoffroy 1806). Int. J. Primatol. 5, 491–514.
Moraes, P.L.R.d., 1992. Espécies utilizadas na alimentacão do mono-carvoeiro (Brachyteles arachnoides E. Geoffroy, 1806. no Parque Estadual de Carlos Botelho. In: Anais do 2° Congresso Nacional sobre Essências Nativas, São Paulo 3., pp. 1206–1208.
Morato, G.S., Calixto J.B., Cordeiro, L., de Lima, T.C., Morato E.F., Nicolau M., Rae G.A., Takahashi, R.N., Valle R.M., Yunes, R.A., 1989. Chemical and pharmacological studies on Talauma ovata St. Hil. (Magnoliaceae). J. Ethnopharmacol. 26, 277–286.
Mori, S.A., Silva L.A.M., Lisboa G., Coradin L., 1985. Manual de manejo do herbário fanerogâmico. Centro de Pesquisas do Cacau, Ilhéus.
Oats, J.F., 1987. Food distribution and foraging behavior. In: Smuts, B.B., Cheney D.L., Seyfarth, R.M., Wrangham R.W., Struhsaker, T.T. (Eds.), Primate Societies. University of Chicago Press, Chicago.
Ohigashi, H., Huffman M.A., Izutsu D., Koshimizu K., Kawanaka M., Sugiyama H., Kirby, G.C, Warhurst, D.C., Allen D., Wright C.W., Phillipson, J.D., Timmon-David, P., Delmas F., Elias R., Balansard G., 1994. Toward the chemical ecology of medicinal plant use in chimpanzees: the case of Vernonia amygdalina, a plant used by wild chimpanzees possibly for parasite-related diseases. J. Chem. Ecol. 20, 541–553.
Peres, M.T., Delle Monache, F., Cruz A.B., Pizzolatti, M.G., Yunes R.A., 1997. Chemical composition and antimicrobial activity of Croton urucurana Baillon (Euphor-biaceae). J. Ethnopharmacol. 56, 223–226.
Petroni, L.M., 1993. Aspectos da ecologia e comportamento do mono-carvoeiro Brachyteles arachnoides (E. Geoffroy, 1806. (Cebidae, Primates), na Fazenda Intervales, Serra de Paranapiacaba, São Paulo. Master’s degree thesis presented to Pontifícia Universidade Católica do Rio Grande do Sul. Porto Alegre.
Petroni, L.M., 2000. Caracterizacão da área de uso e dieta do mono-carvoeiro (Brachyteles arachnoides, Cebidae-Primates) na Mata Atlântica, Serra de Paranapiacaba, SP. Doctorade thesis presented to Universidade de São Paulo. São Paulo.
Rao, V.S., Gurgel L.A., Lima-Júnior, R.C., Martins D.T., Cechinel-Filho, V., Santos F.A., 2007. Dragon’s blood from Croton urucurana (Baill.) attenuates visceral nociception in mice. J. Ethnopharmacol. 113, 357–360.
Rocha, F.F., Lapa A.J., De Lima, T.C., 2002. Evaluation of the anxiolytic-like effects of Cecropia glazioui Sneth in mice. Pharmacol. Biochem. Behav. 71, 183–190.
Rocha, F.F., Lima-Landman, M.T., Souccar, C., Tanae M.M., De Lima, T.C, Lapa A.J., 2007. Antidepressant-like effect of Cecropia glazioui Sneth and its constituents - in vivo and in vitro characterization of the underlying mechanism. Phytomedicine 14, 396–402.
Rodriguez, E., Wrangham R.W., 1993. Zoopharmacognosy: the Use of Medicinal Plants by Animals. In: Downum, K.R., Romeo J.T., Stafford, H. (Eds.), Recent Advances in Phytochemistry, Phytochemical Potential of Tropic Plants. Plenum Press, New York, pp. 89–105.
Rosário, M.M., Noleto G.R., Bento, J.F., Reicher F., Oliveira M.B., Petkowicz, C.L., 2008. Effect of storage xyloglucans on peritoneal macrophages. Phytochemistry 69, 464–472.
Roumy, V., Fabre N., Portet B., Bourdy G., Acebey L., Vigor, C., Valentin A., Moulis, C., 2009. Four antiprotozoal and anti-bacterial compounds from Tapirira guia-nensis. Phytochemistry 70, 305–311.
Souccar, C., Cysneiros R.M., Tanae, M.M., Torres L.M., Lima-Landman, M.T., Lapa A.J., 2008. Inhibition of gastric acid secretion by a standardized aqueous extract of Cecropia glaziovii Sneth and underlying mechanism. Phytomedicine 15, 462–469.
Talebi, M., Bastos A., Lee, P.C., 2005. Diet of southern muriquis in continuous Brazilian Atlantic forest. Int. J. Primatol. 26, 1175–1187.
Vieira, E.M., Izar P., 1999. Interactions between aroids and arboreal mammals in the Brazilian Atlantic rainforest. Plant Ecol. 145, 75–82.
Yamaguchi, M.U., Garcia F.P., Cortez D., Ueda-Nakamura, T., Filho B.P., Nakamura, C.V., 2011. Antifungal effects of Ellagitannin isolated from leaves of Ocotea odorífera (Lauraceae). Antonie Van Leeuwenhoek 99, 507–514.
Author information
Authors and Affiliations
Corresponding author
Additional information
Authors’ contributions
LP and ER have together idealized this study. LP has collected data among the muriquis and ER has collected the ethnomedicinal data among the interviewees. MAH contributed to the writing, analysis and literature search. All authors have read the final manuscriptand approved submission.
Rights and permissions
This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Petroni, L.M., Huffman, M.A. & Rodrigues, E. Medicinal plants in the diet of woolly spider monkeys (Brachyteles arachnoides, E. Geoffroy, 1806) - a bio-rational for the search of new medicines for human use?. Rev. Bras. Farmacogn. 27, 135–142 (2017). https://doi.org/10.1016/j.bjp.2016.09.002
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1016/j.bjp.2016.09.002