Comportamiento de unción con milpiés por un grupo del mono nocturno caribeño (Aotus griseimembra) en vida silvestre en Colombia

Autores/as

  • Sebastián O. Montilla Laboratorio de Ecología de Bosques Tropicales y Primatología (LEBTYP), Departamento de Ciencias Biológicas, Universidad de los Andes, Bogotá D.C., Colombia. Fundación Proyecto Primates, Bogotá D.C., Colombia.
  • Maria José Pinilla-Aristizábal Fundación Proyecto Primates, Bogotá D.C., Colombia. Universidad de Caldas, Manizales, Caldas, Colombia.
  • Lina Antares Tachai Echavarría-Plata Fundación Proyecto Primates, Bogotá D.C., Colombia. Universidad Industrial de Santander, Bucaramanga, Santander, Colombia.
  • César A. Correa-Piñeros Jardín Botánico del Quindío, Calarcá, Quindío, Colombia.
  • Nicolás Corredor-Ospina Grupo de Investigación en Uso y Conservación de la Diversidad Forestal, Universidad Distrital Francisco José de Caldas, Bogotá D.C., Colombia. Fundación Gimnasio Moderno, Bogotá D.C., Colombia. Semillero de Evolución y Conservación, Universidad Militar Nueva Granada, Cajíca, Colombia.
  • Andrés Link Laboratorio de Ecología de Bosques Tropicales y Primatología (LEBTYP), Departamento de Ciencias Biológicas, Universidad de los Andes, Bogotá D.C., Colombia. Fundación Proyecto Primates, Bogotá D.C., Colombia.

DOI:

https://doi.org/10.31687/SaremNMS24.08.6

Palabras clave:

alo-unción, auto-unción, bosque tropical, medicinal, primates nocturnos, repelente

Resumen

La unción ocurre cuando los animales frotan sustancias sobre su cuerpo o el de otros individuos con diferentes propósitos. Aunque este comportamiento se ha descrito para varias especies, en el caso de monos nocturnos solo se ha observado en cautiverio. Presentamos el primer reporte de unción (autounción y alounción) en monos nocturnos silvestres ocurrido específicamente en el mono nocturno caribeño (Aotus griseimembra Elliot, 1912). En el evento participaron tres de los cinco individuos del grupo, quienes se retorcían, cerraban los ojos y salivaban. La unción en los monos nocturnos silvestres puede estar relacionada con la automedicación o puede servir como repelente de insectos, o ambas cosas, teniendo en cuenta las características químicas de los milpiés.

Citas

Abondano, L. A., & A. Link. 2012. The social behavior of brown spider monkeys (Ateles hybridus) in a fragmented forest in Colombia. International Journal of Primatology 33:769–783. https://doi.org/10.1007/s10764-012-9596-1.

Arab, A., G. G. Zacarin, C. S. Fontanetti, M. I. Camargo-Mathias, M. G. Dos Santos, & A. C. Cabrera. 2003. Composition of the defensive secretion of the Neotropical millipede Rhinocricus padbergi Verhoeff 1938 (Diplopoda: Spirobolida: Rhinocricidae). Entomotropica 18:79–82.

Aureli, F., C. M. Schaffner, & G. Schino. 2022. Variation in communicative complexity in relation to social structure and organization in non-human primates. Philosophical Transactions of the Royal Society B 377:20210306. https://doi.org/10.1098/rstb.2021.0306.

Baker, M. 1996. Fur rubbing: use of medicinal plants by capuchin monkeys (Cebus capucinus). American Journal of Primatology 38:263–270. https://doi.org/10.1002/(SICI)1098-2345(1996)38:3<263::AID-AJP5>3.0.CO;2-X.

Birkinshaw, C. R. 1999. Use of millipedes by black lemurs to anoint their bodies. Folia Primatologica 70:170–171. https://doi.org/10.1159/000021691.

Blum, M. 1981. Chemical defenses of arthropods. Academic Press, New York.

Brockie, R. 1976. Self-anointing by wild hedgehogs, Erinaceus europaeus, in New Zealand. Animal Behaviour 24:68–71. https://doi.org/10.1016/S0003-3472(76)80100-5.

Campbell, C. J. 2000. Fur rubbing behavior in free-ranging black-handed spider monkeys (Ateles geoffroyi) in Panama. American Journal of Primatology 51:205–208. https://doi.org/10.1002/1098-2345(200007)51:3<205::AID-AJP5>3.0.CO;2-L.

Carroll, J. F., M. Kramer, P. K. Weldon, & R. G. Robbins. 2005. Anointing chemicals and ectoparasites: effects of benzoquinones from millipedes on the lone star tick, Amblyomma americanum. Journal of Chemical Ecology 31:63–75. https://doi.org/10.1007/s10886-005-0974-4.

Charlton, B. D., M. A. Owen, H. Zhang, & R. R. Swaisgood. 2020. Scent anointing in mammals: functional and motivational insights from giant pandas. Journal of Mammalogy 101:582–588. https://doi.org/10.1093/jmammal/gyaa014.

Cortés-Vesga, L. & A. Link. 2022. Age-sex differences in the social behavior of zoo-housed Colombian black spider monkeys (Ateles fusciceps rufiventris). Mastozoología Neotropical 29:e0566. https://doi.org/10.31687/saremMN.22.29.1.01.e0566.

Coulson, J. O. 2023. Turquoise jay (Cyanolyca turcosa) self-anointing (anting) with a millipede. Ornitología Neotropical 34:17–20. https://doi.org/10.58843/ornneo.v34i1.971.

De la Fuente, M. F., A. Souto, U. P. Albuquerque, & N. Uchiel. 2022. Self-medication in nonhuman primates: a systematic evaluation of the possible function of the use of medicinal plants. American Journal of Primatology 84:e23438. https://doi.org/10.1002/ajp.23438.

De Luna, A. G., A. Link, A. Montes, F. Alfonso, L. Mendieta, & A. Di Fiore. 2017. Increased folivory in brown spider monkeys Ateles hybridus living in a fragmented forest in Colombia. Endangered Species Research 32:123–134. https://doi.org/10.3354/esr00787.

Eisner, T., D, Alsop, K. Hicks, & J. Meinwald. 1978. Defensive secretions of millipeds. Arthropod venoms (S. Bettini, ed.). Springer, Berlin.

Erazo, P., S. O. Montilla, A. Link, & L. Laverde-R. 2023. Vocal repertoire of wild Andean night monkeys (Aotus lemurinus) in an Andean forest in Colombia. Folia Primatologica 94:147–157. https://doi.org/10.1163/14219980-bja10013.

Erkert, H. G., E. Fernandez-Duque, M. Rotundo, & A. Scheideler. 2012. Seasonal variation of temporal niche in wild owl monkeys (Aotus azarai azarai) of the Argentinean Chaco: a matter of masking? Chronobiology International 29:702–714. https://doi.org/10.3109/07420528.2012.673190.

Fairhurst, C. P. 1993. Poisonous exudates of millipedes. Analytical Proceedings 30:429–430.

Fernandez-Duque, E. 2003. Influences of moonlight, ambient temperature, and food availability on the diurnal and nocturnal activity of owl monkeys (Aotus azarai). Behavioral Ecology and Sociobioliology 54:431–440. https://doi.org/10.1007/s00265-003-0637-9.

Fernandez-Duque, E., & H. G. Erkert. 2006. Cathemerality and lunar periodicity of activity rhythms in owl monkeys of the Argentinian Chaco. Folia Primatologica 77:123–138. https://doi.org/10.1159/000089699.

Fernandez-Duque, E., H. de la Iglesia, & H. G. Erkert. 2010. Moonstruck primates: owl monkeys (Aotus) need moonlight for nocturnal activity in their natural environment. PLoS One 5:e12572. https://doi.org/10.1371/journal.pone.0012572.

Freeberg, T. M., R. I. Dunbar, & T. J. Ord. 2012. Social complexity as a proximate and ultimate factor in communicative complexity. Philosophical Transactions of the Royal Society B 367:1785–1801. https://doi.org/10.1098/rstb.2011.0213.

Fruth, B., et al. 2014 New evidence for self-medication in bonobos: Manniophyton fulvum leaf- and stem strip swallowing from LuiKotale, Salonga National Park, DR Congo. American Journal of Primatology 76:146–158. https://doi.org/10.1002/ajp.22217.

Garcia de la Chica, A., A. Spence-Aizenberg, C. K., Wolovich, S. Evans, & E. Fernandez-Duque. 2023. The social life of owl monkeys. Owl monkeys: biology, adaptive radiation, and behavioral ecology of the only nocturnal primate in the Americas (E. Fernandez-Duque, ed.). Springer International Publisher, New York.

Gasco, A. D., A. M. Pérez-Acosta, & P. F. Monticelli. 2016. Ring-tailed coatis anointing with soap: a new variation of self-medication culture? International Journal of Comparative Psychology 29:1–11. https://doi.org/10.46867/ijcp.2016.29.00.05.

Hoffman, R. L. 1998. Studies on spiroboloid millipeds. XIX. Thyroproctus, an exceptional genus in the Rhinocricidae. Myriapodologica 5:56–61.

Huck, M., E. Fernandez-Duque, P. Babb, & R. Schurr. 2014. Correlates of genetic monogamy in socially monogamous mammals: insights from Azara's owl monkeys. Proceedings of the Royal Society of London B 281:20140195. https://doi.org/10.1098/rspb.2014.0195.

Jefferson, J. P., E. Tapanes, & S. Evans. 2014. Owl monkeys (Aotus spp.) perform self-and social anointing in captivity. Folia Primatologica 85:119–134. https://doi.org/10.1159/000359970.

Laska, M., V. Bauer, & L. T. Hernandez. 2007. Self-anointing behavior in free-ranging spider monkeys (Ateles geoffroyi) in Mexico. Primates 48:160–163. https://doi.org/10.1007/s10329-006-0019-9.

Leca, J. B., N. Gunst, & O. Petit. 2007. Social aspects of fur-rubbing in Cebus capucinus and C. apella. International Journal of Primatology 28:801–817. https://doi.org/10.1007/s10764-007-9162-4.

Link, A., A. G. de Luna, F. Alfonso, P. Giraldo-Beltrán, & F. Ramírez. 2010. Initial effects of fragmentation on the density of three neotropical primate species in two lowland forests of Colombia. Endangered Species Research 13:41–50. https://doi.org/10.3354/esr00312.

Link, A., J. Muñoz-Delgado, & S. O. Montilla. 2023. Nocturnality and activity budgets of owl monkeys in tropical ecosystems. Owl monkeys: biology, adaptive radiation, and behavioral ecology of the only nocturnal primate in the Americas (E. Fernandez-Duque, ed.). Springer International Publisher, New York.

Lynch-Alfaro, J. W., et al. 2012. Anointing variation across wild capuchin populations: a review of material preferences, bout frequency and anointing sociality in Cebus and Sapajus. American Journal of Primatology 74:299–314. https://doi.org/10.1002/ajp.20971.

Marek, P. E., J. E. Bond, & P. Sierwald. 2003. Rhinocricidae systematics II: the species catalog of the Rhinocricidae (Diplopoda: Spirobolida) with synonymies. Zootaxa 308:1–108. https://doi.org/10.11646/zootaxa.308.1.1.

Medeiros, K., et al. 2020. Wild blonde capuchins (Sapajus flavius) perform anointing behaviour using toxic secretions of a millipede (Spirobolida: Rhinocricidae). Journal of Chemical Ecology 46:1010–1015. https://doi.org/10.1007/s10886-020-01215-0.

Messer, E. J., M. T. Bowler, N. Claidière, & A. Whiten. 2022. The role of anointing in robust capuchin monkey, Sapajus apella, social dynamics. Animal Behaviour 190:103–114. https://doi.org/10.1016/j.anbehav.2022.04.017.

Montilla, S. O., et al. 2021. Activity patterns, diet and home range of night monkeys (Aotus griseimembra and Aotus lemurinus) in tropical lowland and mountain forests of central Colombia. International Journal of Primatology 42:130–153. https://doi.org/10.1007/s10764-020-00192-1.

Morozov, N. S. 2015. Why do birds practice anting? Biology Bulletin Reviews 5:353–365. https://doi.org/10.1134/S2079086415040076.

Morrogh-Bernard, H. C. 2008. Fur-rubbing as a form of self-medication in Pongo pygmaeus. International Journal of Primatology 29:1059–1064. https://doi.org/10.1007/s10764-008-9266-5.

Morrogh-Bernard, H. C., et al. 2017. Self-medication by orang-utans (Pongo pygmaeus) using bioactive properties of Dracaena cantleyi. Scientific Reports 7:16653. https://doi.org/10.1038/s41598-017-16621-w.

Muñoz-Delgado, J., et al. 2021. Lunar periodic modulation of the circadian activity rhythm in a wild North Colombian night monkey (Aotus griseimembra). Chronobiology International 38:944–949. https://doi.org/10.1080/07420528.2021.1903029.

Peckre, L. R., C. Defolie, P. M. Kappeler, & C. Fichtel. 2018. Potential self-medication using millipede secretions in red-fronted lemurs: combining anointment and ingestion for a joint action against gastrointestinal parasites? Primates 59:483–494. https://doi.org/10.1007/s10329-018-0674-7.

Perin, A., & J. V Perin. 2023. Rufous Hornero (Furnarius rufus, Furnariidae) anointing with a millipede (Diplopoda, Spirobolidae) in southernmost Brazil. Journal of Field Ornithology 94:13. https://doi.org/10.5751/JFO-00394-940413.

Rimbach, R., A. Link, A. Montes-Rojas, A. Di Fiore, M. Heistermann, & E. W. Heymann. 2014. Behavioral and physiological responses to fruit availability of spider monkeys ranging in a small forest fragment. American Journal of Primatology 76:1049–1061. https://doi.org/10.1002/ajp.22292.

Rimbach, R., A. Pardo-Martinez, A. Montes-Rojas, A. Di Fiore, & A. Link. 2012. Interspecific infanticide and infant-directed aggression by spider monkeys (Ateles hybridus) in a fragmented forest in Colombia. American Journal of Primatology 74:990–997. https://doi.org/10.1002/ajp.22052.

Rondón, S., S. Cavallero, A. Link, M. De Meo, C. González, & S. D'Amelio. 2023a. Cuterebra baeri infecting grey-legged night monkeys (Aotus griseimembra) and red howler monkeys (Alouatta seniculus) in Colombia. Journal of Wildlife Diseases 59:181–185. https://doi.org/10.7589/JWD-D-22-00062.

Rondón, S., S. Cavallero, A. Link, C. González, & S. D'Amelio. 2023b. Prevalence and molecular characterization of Blastocystis sp. infecting free-ranging primates in Colombia. Pathogens 12:569. https://doi.org/10.3390/pathogens12040569.

Rondón, S., C. León, A. Link, & C. González. 2019. Prevalence of Plasmodium parasites in non-human primates and mosquitoes in areas with different degrees of fragmentation in Colombia. Malaria Journal 18:1–10. https://doi.org/10.1186/s12936-019-2910-z.

Sierwald, P. 2018. Milli-PEET: key to millipede orders. <https://www.fieldmuseum.org/science/special-projects/milli-peet-class-diplopoda/milli-peet-millipedes-made-easy/milli-peet-key>.

Souza-Alves, J. P., N. M. Albuquerque, L. Vinhas, T. S. Cardoso, R. Beltrão-Mendes, & L. Jerusalinsky. 2018. Self-anointing behaviour in captive titi monkeys (Callicebus spp.). Primate Biology 5:1–5. https://doi.org/10.5194/pb-5-1-2018.

Spence-Aizenberg, A., A. García de la Chica, S. Evans, & E. Fernandez-Duque. 2023. Communication in owl monkeys. Owl monkeys: biology, adaptive radiation, and behavioral ecology of the only nocturnal primate in the Americas (E. Fernandez-Duque, ed.). Springer International Publisher, New York.

Valderrama, X., J. G. Robinson, A. B. Attygalle, & T. Eisner. 2000. Seasonal anointment with millipedes in a wild primate: a chemical defense against insects? Journal of Chemical Ecology 26:2781–2790. https://doi.org/10.1023/A:1026489826714.

Weldon, P. J., J. R. Aldrich, J. A. Klun, J. E. Oliver, & M. Debboun. 2003. Benzoquinones from millipedes deter mosquitoes and elicit self-anointing in capuchin monkeys (Cebus spp.). Naturwissenschaften 90:301–304. https://doi.org/10.1007/s00114-003-0427-2.

Zito, M., S. Evans, & P. J. Weldon. 2003. Owl monkeys (Aotus spp.) self-anoint with plants and millipedes. Folia Primatologica 74:159–161. https://doi.org/10.1159/000070649.

Anointing behavior by a group of Caribbean night monkeys (Aotus griseimembra) in Colombia

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Publicado

10–09–2024

Cómo citar

O. Montilla, S., Pinilla-Aristizábal, M. J., Echavarría-Plata, L. A. T., Correa-Piñeros, C. A., Corredor-Ospina, N., & Link, A. (2024). Comportamiento de unción con milpiés por un grupo del mono nocturno caribeño (Aotus griseimembra) en vida silvestre en Colombia. Notas Sobre Mamíferos Sudamericanos, 6. https://doi.org/10.31687/SaremNMS24.08.6

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