cabreúva; camera trap; fur-rubbing; medicinal plants; Myroxylon peruiferum; zoopharmacognosy; Ecology, Evolution, Behavior and Systematics
Abstract :
[en] We present camera trap evidence of 10 Atlantic Forest mammals fur-rubbing, licking, or biting balsam from cabreúvas (Myroxylon peruiferum, Fabaceae), native trees used in traditional medicine for their prophylactic and therapeutic virtues. Given the antiparasitic properties of cabreúvas, mammals may be using the balsam as topical self-medication to repel ectoparasites. Abstract in Portuguese is available with online material.
Disciplines :
Zoology
Author, co-author :
Kaisin, Olivier ✱; Université de Liège - ULiège > Sphères ; Departamento de Biodiversidade, Laboratório de Primatologia, São Paulo State University (UNESP), Rio Claro, Brazil ; Programa de PósGraduaçãoem Ecologia, Evolução e Biodiversidade, São Paulo State University (UNESP), Rio Claro, Brazil
Rocha, Fernanda Corrêa ✱; Laboratório de PatologiaVeterinária, University of Brasília (UnB), Distrito Federal, Brazil
Amaral, Rodrigo Gonçalves; Departamento de Biodiversidade, Laboratório de Primatologia, São Paulo State University (UNESP), Rio Claro, Brazil ; Programa de PósGraduaçãoem Ecologia, Evolução e Biodiversidade, São Paulo State University (UNESP), Rio Claro, Brazil
Bufalo, Felipe ; Departamento de Biodiversidade, Laboratório de Primatologia, São Paulo State University (UNESP), Rio Claro, Brazil ; Programa de PósGraduaçãoem Ecologia, Evolução e Biodiversidade, São Paulo State University (UNESP), Rio Claro, Brazil
Sabino, Gabriel Pavan; Departemento de Botânica, São Paulo State University (UNESP), Rio Claro, Brazil
Culot, Laurence ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie du comportement - Ethologie et psychologie animale ; Departamento de Biodiversidade, Laboratório de Primatologia, São Paulo State University (UNESP), Rio Claro, Brazil
✱ These authors have contributed equally to this work.
Language :
English
Title :
A universal pharmacy: Possible self-medication using tree balsam by multiple Atlantic Forest mammals
FAPESP - Fundação de Amparo à Pesquisa do Estado de São Paulo F.R.S.-FNRS - Fonds de la Recherche Scientifique CNPq - Conselho Nacional de Desenvolvimento Científico e Tecnológico CAPES - Coordenação de Aperfeicoamento de Pessoal de Nível Superior
Funding text :
We would like to thank Guilherme Garbino for identifying the bat species in the video. OK received a fellowship from the National Fund for Scientific Research (FRS‐FNRS, Belgium), RGA from the Coordination for the Improvement of Higher Education Personnel (CAPES), and FB from the Brazilian National Council for Scientific and Technological Development (CNPq: 443489/2020‐3). This research was financed by a Young Investigator grant from the São Paulo Research Foundation (FAPESP) given to LC (#2014/14739‐0).
Andrade, M. A., Azevedo, C. D. S., Motta, F. N., Santos, M. L. D., Silva, C. L., Santana, J. M. D., & Bastos, I. M. D. (2016). Essential oils: In vitro activity against Leishmania amazonensis, cytotoxicity and chemical composition. BMC Complementary and Alternative Medicine, 16(1), 444. https://doi.org/10.1186/s12906-016-1401-9
Baker, M. (1996). Fur rubbing: Use of medicinal plants by capuchin monkeys (Cebus capucinus). American Journal of Primatology, 38(3), 263–270.
Birkinshaw, C. R. (1999). Use of millipedes by black lemurs to anoint their bodies. Folia Primatologica, 70(3), 170–171. https://doi.org/10.1159/000021691
Bowyer, R. T., Ballenberghe, V. V., & Rock, K. R. (1994). Scent marking by Alaskan moose: Characteristics and spatial distribution of rubbed trees. Canadian Journal of Zoology, 72(12), 2186–2192. https://doi.org/10.1139/z94-292
da Silva Junior, C. A., da Silva, L. C. N., de Souza, R. M., Aranda-Souza, M. A., Pereira, D., Silva, M. V., & Correira, M. T. S. (2014). Myroxylum peruiferum: Antioxidant activity and phenolic content. Current Topics in Phytochemistry, 12, 21–25.
de Roode, J. C., Lefevre, T., & Hunter, M. D. (2013). Self-medication in animals. Science, 340(6129), 150–151. https://doi.org/10.1126/science.1235824
Fruth, B., Ikombe, N. B., Matshimba, G. K., Metzger, S., Muganza, D. M., Mundry, R., & Fowler, A. (2014). New evidence for self-medication in bonobos: Manniophyton fulvum leaf- and stemstrip-swallowing from LuiKotale, Salonga National Park, DR Congo. American Journal of Primatology, 76(2), 146–158. https://doi.org/10.1002/ajp.22217
Gompper, M. E., & Hoylman, A. M. (1993). Grooming with Trattinnickia resin: Possible pharmaceutical plant use by coatis in Panama. Journal of Tropical Ecology, 9(4), 533–540. https://doi.org/10.1017/S0266467400007616
Gonçalves, A. L., Filho, A. A., & Menezes, H. (2005). Estudo comparativo da atividade antimicrobiana de extratos de algumas árvores nativas. Arquivos do Instituto Biologico, 72(3), 353–358.
Gosling, L. M., & McKay, H. V. (1990). Scent-rubbing and status signalling by male mammals. Chemoecology, 1(3–4), 92–95. https://doi.org/10.1007/BF01241649
Guidorizzi, C. E., & Raboy, B. E. (2009). Fur-rubbing with plant exudates in wild golden-headed lion tamarins (Leontopithecus chrysomelas). Proceedings of the Annual Meeting of the American Society of Primatologists, Bahia, 71.
Heymann, E. W. (2006). Scent marking strategies of new world primates. American Journal of Primatology, 68(6), 650–661. https://doi.org/10.1002/ajp.20258
Hirano, Z. M. B., Correa, I. C., & de Oliveira, D. A. G. (2008). Contexts of rubbing behavior in Alouatta guariba clamitans: A scent-marking role? American Journal of Primatology, 70(6), 575–583. https://doi.org/10.1002/ajp.20531
Huffman, M. A. (1997). Current evidence for self-medication in primates: A multidisciplinary perspective. Yearbook of Physical Anthropology, 40, 171–200.
Huffman, M. A. (2006). Primate Self-Medication. In C. J. Campbell, A. Fuentes, K. MacKinnon, M. Panger, & S. Bearder (Eds.), Primates in perspectives (pp. 677–689). Oxford University Press.
Huffman, M. A., & Pebsworth, P. A. (2018). Medicinal plant use by nonhuman primates. In A. Fuentes (Ed.), The international encyclopedia of biological anthropology (pp. 1–4). John Wiley & Sons. https://doi.org/10.1002/9781118584538.ieba0315
Janzen, D. (1978). Complications in interpreting the chemical defences of trees against tropical arboreal plant-eating vertebrates In G. G. Montgomery (Ed.), The ecology of arboreal folivores (pp. 73–84). Smithsonian Institute Press.
Johansson, A., Liberg, O., & Wahlstrom, L. K. (1995). Temporal and physical characteristics of scraping and rubbing in roe deer (Capreolus capreolus). Journal of Mammalogy, 76(1), 123–129. https://doi.org/10.2307/1382320
Kaisin, O., Corrêa Rocha, F., Gonçalves Amaral, R., Bufalo, F., Pavan Sabino, G., & Culot, L. (2022). Data from: A universal pharmacy: possible self-medication using tree balsam by multiple Atlantic Forest mammals. Dryad Digital Repository. https://doi.org/10.5061/dryad.qnk98sfjv
Leca, J.-B., Gunst, N., & Petit, O. (2007). Social Aspects of Fur-rubbing in Cebus capucinus and C. apella. International Journal of Primatology, 28(4), 801–817. https://doi.org/10.1007/s10764-007-9162-4
Lorenzi, H., & Matos, F. J. A. (2002). Plantas medicinais no Brasil, Nativas e exóticas. Plantarum.
Lozano, G. A. (1998). Parasitic stress and self-medication in wild animals. Advances in the Study of Behavior, 27, 291–317. https://doi.org/10.1016/S0065-3454(08)60367-8
Mares-Guia, M. A. M. D. M., Horta, M. A., Romano, A., Rodrigues, C. D. S., Mendonça, M. C. L., dos Santos, C. C., Torres, M. C., Araujo, E. S. M., Fabri, A., de Souza, E. R., Ribeiro, R. O. R., Lucena, F. P., Junior, L. C. A., da Cunha, R. V., Nogueira, R. M. R., Sequeira, P. C., & de Filippis, A. M. B. (2020). Yellow fever epizootics in non-human primates, Southeast and Northeast Brazil (2017 and 2018). Parasites and Vectors, 13(1), 1–8. https://doi.org/10.1186/s13071-020-3966-x
Mclennan, M. R., & Huffman, M. A. (2012). High frequency of leaf swallowing and its relationship to intestinal parasite expulsion in “Village” Chimpanzees at Bulindi, Uganda. American Journal of Primatology, 74(7), 642–650. https://doi.org/10.1002/ajp.22017
Miller, K. E., Laszlo, K., & Dietz, J. M. (2003). The role of scent marking in the social communication of wild golden lion tamarins, Leontopithecus rosalia. Animal Behaviour, 65(4), 795–803. https://doi.org/10.1006/anbe.2003.2105
Moraes, I. A., De-carvalho, M. C. A., De Azevedo Valle, H., Pessoa, V. P., Ferreira, A. M. R., & Pissinatti, A. (2006). Histology of the sternal and suprapubic skin areas in lion tamarins (Leontopithecus sp. Callitrichidae–Primates). American Journal of Primatology, 68(11), 1120–1126. https://doi.org/10.1002/ajp.20287
Morrogh-Bernard, H. C. (2008). Fur-Rubbing as a Form of self-medication in Pongo pygmaeus. International Journal of Primatology, 29(4), 1059–1064. https://doi.org/10.1007/s10764-008-9266-5
Muñoz, V., Sauvain, M., Bourdy, G., Arrázola, S., Callapa, J., Ruiz, G., Choque, J., & Deharo, E. (2000). A search for natural bioactive compounds in Bolivia through a multidisciplinary approach. Journal of Ethnopharmacology, 71(1–2), 123–131. https://doi.org/10.1016/S0378-8741(99)00191-9
Oliveira, P. R., Borges, L. M., Lopes, C. M., & Leite, R. (2000). Population dynamics of the free-living stages of Amblyomma cajennense (Fabricius, 1787) (Acari: Ixodidae) on pastures of Pedro Leopoldo, Minas Gerais State, Brazil. Veterinary Parasitology, 92(4), 295–301. https://doi.org/10.1016/S0304-4017(00)00322-8
Pereira, R., de Matos Neto, F. Â., de Aguiar, F. L. L., de Souza, E. B., Santos, H. S., de Cavalcante, C. S., & Fontenelle, R. O. D. S. (2018). Atividade antifungica, sinergismo e citotoxicidade do extrato etanolico da casca de Myroxylon peruiferum. Revista Da Universidade Vale do Rio Verde, 16, 3751. https://doi.org/10.5892/ruvrd.v16i1.3751
Raman, R., & Kandula, S. (2008). Zoopharmacognosy. Resonance, 13(3), 245–253. https://doi.org/10.1007/s12045-008-0038-5
Ryon, J., Fentress, J. C., Harrington, F. H., & Bragdon, S. (1986). Scent rubbing in wolves (Canis lupus): The effect of novelty. Canadian Journal of Zoology, 64(3), 573–577. https://doi.org/10.1139/z86-084
Sartori, A. L. B. (2015). Myroxylon in Lista de Espécies da Flora do Brasil. Retrieved from Jardim Botânico do Rio De Janeiro Website. http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB29797
Seo, S.-M., Park, H.-M., & Park, I.-K. (2012). Larvicidal Activity of Ajowan (Trachyspermum ammi) and Peru Balsam (Myroxylon pereira) Oils and Blends of Their Constituents against Mosquito, Aedes aegypti, Acute Toxicity on Water Flea, Daphnia magna, and Aqueous Residue. Journal of Agricultural and Food Chemistry, 60(23), 5909–5914. https://doi.org/10.1021/jf301296d
Shurkin, J. (2014). Animals that self-medicate. Proceedings of the National Academy of Sciences, 111(49), 17339–17341. https://doi.org/10.1073/pnas.1419966111
Souza, L. F., Dias, R. F., Guilherme, F. A. G., & Coelho, C. P. (2016). Plantas medicinais referenciadas por raizeiros no município de Jataí, estado de Goiás. Revista Brasileira De Plantas Medicinais, 18(2), 451–461. https://doi.org/10.1590/1983-084X/15_173
Souza-Alves, J. P., Chagas, R. R. D., Boyle, S. A., Barnett, A. A., & Bezerra, B. M. (2021). Throat-to-Chest Behavior in Coimbra-Filho’s Titi Monkeys (Callicebus coimbrai) Is Potentially Associated with Olfactory Communication. International Journal of Primatology. https://doi.org/10.1007/s10764-021-00232-4
Trentin, D. D. S., Giordani, R. B., Zimmer, K. R., da Silva, A. G., da Silva, M. V., Correia, M. T. D. S., Baumvol, I. J. R., & Macedo, A. J. (2011). Potential of medicinal plants from the Brazilian semi-arid region (Caatinga) against Staphylococcus epidermidis planktonic and biofilm lifestyles. Journal of Ethnopharmacology, 137(1), 327–335. https://doi.org/10.1016/j.jep.2011.05.030
Wilson, N., Dietz, J. M., & Whitaker, J. O. (1989). Ectoparasitic Acari found on golden lion tamarins (Leontopithecus rosalia rosalia) from Brazil. Journal of Wildlife Diseases, 25(3), 433–435. https://doi.org/10.7589/0090-3558-25.3.433