Social correlates of variation in urinary oxytocin concentrations of mantled howler monkeys Alouatta palliata (Gray, 1849) (Primates: Atelidae): A preliminary assessment

Autores/as

  • Diana Moreno-Espinoza Primate Behavioral Ecology Lab, Instituto de Neuroetología, Universidad Veracruzana, Av. Dr. Luis Castelazo Ayala S/N Colonia Industrial Animas, Xalapa, Veracruz, 91190, México.
  • Pedro Américo D. Dias Primate Behavioral Ecology Lab, Instituto de Neuroetología, Universidad Veracruzana, Av. Dr. Luis Castelazo Ayala S/N Colonia Industrial Animas, Xalapa, Veracruz, 91190, México. https://orcid.org/0000-0002-2919-6479
  • Alejandro Coyohua-Fuentes Primate Behavioral Ecology Lab, Instituto de Neuroetología, Universidad Veracruzana, Av. Dr. Luis Castelazo Ayala S/N Colonia Industrial Animas, Xalapa, Veracruz, 91190, México.
  • Domingo Canales-Espinosa Primate Behavioral Ecology Lab, Instituto de Neuroetología, Universidad Veracruzana, Av. Dr. Luis Castelazo Ayala S/N Colonia Industrial Animas, Xalapa, Veracruz, 91190, México.
  • Ariadna Rangel-Negrín Primate Behavioral Ecology Lab, Instituto de Neuroetología, Universidad Veracruzana, Av. Dr. Luis Castelazo Ayala S/N Colonia Industrial Animas, Xalapa, Veracruz, 91190, México.

DOI:

https://doi.org/10.21829/azm.2021.3712319

Palabras clave:

afiliación, Alouatta, mecanismos neuroendocrinos, platirrinos, sociabilidad

Resumen

Existe una creciente evidencia de que la sociabilidad en primates no humanos está relacionada con mecanismos neuroendocrinos. La arginina vasopresina, las endorfinas y la oxitocina pueden estar involucradas en tales mecanismos. Aquí, realizamos un análisis preliminar de los correlatos sociales de la variación en las concentraciones de oxitocina urinaria en monos aulladores de manto (Alouatta palliata). De enero a diciembre de 2017, estudiamos 13 monos aulladores de manto adultos pertenecientes a dos grupos. Registramos la ocurrencia de interacciones sociales (547.5 horas de observación); evaluamos la proximidad entre los miembros del grupo (2.194 registros instantáneos); y recolectamos 172 muestras de orina. Analizamos las muestras de orina (ELISA) para determinar las concentraciones de oxitocina, las cuales corregimos por la gravedad específica, lo que resultó en 54 muestras analizadas. Con respecto a cuando no ocurrieron interacciones afiliativas, las concentraciones de oxitocina aumentaron aproximadamente un 62% cuando los individuos participaron en interacciones afiliativas, y las concentraciones de oxitocina fueron mayores cuando díadas con una relación social de baja calidad se afiliaron. Estos resultados convergen con propuestas previas de que la oxitocina está vinculada a la participación en interacciones afiliativas. La convergencia entre estos resultados y los reportados para otros taxa apoya la hipótesis de que los mecanismos biológicos que permiten la sociabilidad de los primates se comparten entre las especies.

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Citas

Alberts, S. (2018) Social influences on survival and reproduction: Insights from a long-term study of wild baboons. Journal of Animal Ecology, 88, 47–66. https://doi.org/10.1111/1365-2656.12887 DOI: https://doi.org/10.1111/1365-2656.12887

Altmann, J. (1974) Observational study of behavior: Sampling methods. Behaviour, 49, 227–267. https://doi.org/10.1163/156853974X00534 DOI: https://doi.org/10.1163/156853974X00534

Altmann, J., Alberts, S. C. (2003) Intraspecific variability in fertility and offspring survival in a nonhuman primate: Behavioral control of ecological and social sources. Pp. 140–169. In: K. W. B. Wachter, R. A. Bulatao (Eds.). Offspring: Human fertility behavior in biodemographic perspective. National Academies Press, Washington, DC.

Amico, J. A., Ulbrecht, J. S., Robinson, A. G. (1987) Clearance studies of oxytocin in humans using radioimmunoassay measurements of the hormone in plasma and urine. Journal of Clinical Endocrinology and Metabolism, 64, 340–345. https://doi.org/10.1210/jcem-64-2-340 DOI: https://doi.org/10.1210/jcem-64-2-340

Anacker, A. M., Beery, A. K. (2013) Life in groups: the roles of oxytocin in mammalian sociality. Frontiers in Behavioral Neuroscience, 7, 1–10. https://doi.org/10.3389/fnbeh.2013.00185 DOI: https://doi.org/10.3389/fnbeh.2013.00185

Anestis, S. F. (2010) Hormones and social behavior in primates. Evolutionary Anthropology, 19, 66–78. https://doi.org/10.1002/evan.20253 DOI: https://doi.org/10.1002/evan.20253

Aureli, F., Fraser, O. N., Schaffner, C. M., Schino, G. (2012) The regulation of social relationships. Pp. 531–551. In: J. C. Mitani, J. Call, P. M. Kappeler, R. A. Palombit, J. B. Silk (Eds.). The evolution of primate societies. Chicago University Press, Chicago.

Beery, A. K., Zucker, I. (2010) Oxytocin and same-sex social behavior in female meadow voles. Neuroscience, 169, 665–673. https://doi.org/10.1016/j.neuroscience.2010.05.023 DOI: https://doi.org/10.1016/j.neuroscience.2010.05.023

Benarroch, E. (2013) Oxytocin and vasopressin. Social neuropeptides with complex neuromodulatory functions. American Academy of Neurology, 80, 1521–1528. https://doi.org/10.1212/WNL.0b013e31828cfb15 DOI: https://doi.org/10.1212/WNL.0b013e31828cfb15

Benítez, M. E., Sosnowski, M. J., Tomeo, O. B., Brosnan, S. F. (2018) Urinary oxytocin in capuchin monkeys: Validation and the influence of social behavior. American Journal of Primatology, 88, 1–11. https://doi.org/10.1002/ajp.22877 DOI: https://doi.org/10.1002/ajp.22877

Bezanson, M., Garber, P. A., Murphy, J. T., Premo, L. S. (2008) Patterns of subgrouping and spatial affiliation in a community of mantled howling monkeys (Alouatta palliata). American Journal of Primatology, 70, 282–293. https://doi.org/10.1002/ajp.20486 DOI: https://doi.org/10.1002/ajp.20486

Bick, J., Dozier, M. (2010) Mothers’ concentrations of oxytocin following close, physical interactions with biological and nonbiological children. Developmental Psychobiology, 52, 100–107. https://doi.org/10.1002/dev.20411 DOI: https://doi.org/10.1002/dev.20411

Boose K., White F., Brand, C., Meinelt, A., Snodgradd, J. (2018) Infant handling in bonobos (Pan paniscus): Exploring functional hypotheses and the relationship to oxytocin. Physiology & Behavior, 193, 154–166. https://doi.org/10.1016/j.physbeh.2018.04.012 DOI: https://doi.org/10.1016/j.physbeh.2018.04.012

Cavanaugh, J., Mustoe, A., French, J. A. (2018) Oxytocin regulates reunion affiliation with a pair mate following social separation in marmosets. American Journal of Primatology, 88, 1–9. https://doi.org/10.1002/ajp.22750 DOI: https://doi.org/10.1002/ajp.22750

Crockett, C. M., Eisenberg, J. F. (1987) Howlers: Variations in group size and demography. Pp. 54–68. In: B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, T. T. Struhsaker (Eds.). Primate societies. University of Chicago Press, Chicago.

Crockford, C., Wittig, R., Langergraber, K., Ziegler, T., Zuberbühler, K., Deschner, T. (2013) Urinary oxytocin and social bonding in related and unrelated wild chimpanzees. Proceedings of The Royal Society, 280, e20122765. https://doi.org/10.1098/rspb.2012.2765 DOI: https://doi.org/10.1098/rspb.2012.2765

De Dreu, C. (2012) Oxytocin modulates cooperation within and competition between groups: An integrative review and research agenda. Hormones and Behavior, 61, 419–428. https://doi.org/10.1016/j.yhbeh.2011.12.009 DOI: https://doi.org/10.1016/j.yhbeh.2011.12.009

Di Fiore, A., Campbell, C. J. (2007) The atelines: Variation in ecology, behavior, and social organization. Pp. 155–185. In: C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger S. K. Bearder (Eds.). Primates in perspective. Oxford University Press, Oxford, NY.

Dias, P. A. D., Rangel-Negrín, A. (2015) An ethogram for the social behavior of adult Alouatta palliata mexicana and A. pigra. Laboratorio de Ecología del Comportamiento de Primates, Instituto de Neuroetología, Universidad Veracruzana, Xalapa, Veracruz, Mexico. https://doi.org/10.13140/RG.2.1.1043.7840

Fujii, T., Schug, J., Nishina, K., Takahashi, T., Okada, H., Takagishi, H. (2016) Relationship between salivary oxytocin levels and generosity in preschoolers. Scientific Reports, 6, 1–7. https://doi.org/10.1038/srep38662 DOI: https://doi.org/10.1038/srep38662

González-Hernández, M., Rangel-Negrín, A., Schoof, V., Chapman, C., Canales-Espinoza, D., Dias, P. A. D. (2014) Transmission patterns of pinworms in two sympatric congeneric primate species. International Journal of Primatology, 35, 445–462. https://doi.org/10.1007/s10764-014-9751-y DOI: https://doi.org/10.1007/s10764-014-9751-y

Insel, T. R. (2010) The challenge of translation in social neuroscience: A review of oxytocin, vasopressin, and affiliative behavior. Neuron, 65, 768–779. https://doi.org/10.1016/j.neuron.2010.03.005 DOI: https://doi.org/10.1016/j.neuron.2010.03.005

Jasso del Toro, C., Kekaris, K. A-I. (2019) Affiliative behaviors. Encyclopedia of animal cognition and behavior. Springer, New York. https://doi.org/10.1007/978-3-319-47829-6_1040-1 DOI: https://doi.org/10.1007/978-3-319-47829-6_1040-1

Kumaresan, P., Subramanian, M., Anandarangam, P. B., Kumaresan, M. (1979) Radioimmunoassay of plasma and pituitary oxytocin in pregnant rats during various stages of pregnancy and parturition. Journal of Endocrinological Investigation, 2, 65–70. https://doi.org/10.1007/bf03349277 DOI: https://doi.org/10.1007/BF03349277

Liu, Y., Wang, Z. X. (2003) Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles. Neuroscience, 121, 537–544. https://doi.org/10.1016/S0306-4522(03)00555-4 DOI: https://doi.org/10.1016/S0306-4522(03)00555-4

Love, T. M. (2014) Oxytocin, motivation and the role of dopamine. Pharmacology, Biochemistry and Behavior, 119, 49–60. https://doi.org/10.1016/j.pbb.2013.06.011 DOI: https://doi.org/10.1016/j.pbb.2013.06.011

Massen, J., de Voss, H., Sterck, E. (2010) Close social associations in animals and humans: functions and mechanisms of friendship. Behaviour, 147, 1379–1412. https://doi.org/10.1163/000579510X528224 DOI: https://doi.org/10.1163/000579510X528224

Meyer-Lindenberg, A., Domes, G., Kirsch, P., Heinrichs, M. (2011) Oxytocin and vasopressin in the human brain: social neuropeptides. Nature Reviews Neuroscience, 12, 524–538. https://doi.org/10.1038/nrn3044 DOI: https://doi.org/10.1038/nrn3044

Miller, R., Brindle, E., Holman, D. J., Shofer, J., Klein, N. A., Soules, M. R., O’Connor, K. A. (2004) Comparison of specific gravity and creatinine for normalizing urinary reproductive hormone concentrations. Clinical Chemistry, 50, 924–932. https://doi.org/10.1373/clinchem.2004.032292 DOI: https://doi.org/10.1373/clinchem.2004.032292

Morhenn, V. B., Park, J. W., Piper, E., Zak, P. J. (2008) Monetary sacrifice among strangers is mediated by endogenous oxytocin release after physical contact. Evolution and Human Behavior, 29, 375–383. https://doi.org/10.1016/j.evolhumbehav.2008.04.004 DOI: https://doi.org/10.1016/j.evolhumbehav.2008.04.004

Neumann, I. D. (2003) Brain mechanisms underlying emotional alterations in the peripartum period in rats. Depression and Anxiety, 17, 111–121. https://doi.org/10.1002/da.10070 DOI: https://doi.org/10.1002/da.10070

Packer, C., Collins, D. A., Sindimwo, A., Goodall, J. (1995) Reproductive constraints on aggressive competition in female baboons. Nature, 373, 60–63. https://doi.org/10.1038 / 373060a0 DOI: https://doi.org/10.1038/373060a0

Pinheiro, J., Bates, D. (2000) Mixed-effects models in S and S-plus. Springer, New York, NY, 528 pp. DOI: https://doi.org/10.1007/978-1-4419-0318-1

R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

Rincon, A. V., Deschner, T., Schülke, O., Ostner, J. (2020) Oxytocin increases after affiliative interactions in male Barbary macaques. Hormones and Behavior, 119, 104661. https://doi.org/10.1016/j.yhbeh.2019.104661 DOI: https://doi.org/10.1016/j.yhbeh.2019.104661

Ryu, H., Hill, D. A., Furuichi, T. (2014) Prolonged maximal sexual swelling in wild bonobos facilitates affiliative interactions between females. Behaviour, 152, 285–311. https://doi.org/10.1163/1568539X-00003212 DOI: https://doi.org/10.1163/1568539X-00003212

Samuni, L., Preis, A., Mundry, R., Deschner, T., Crockford, C., Wittig, R. M. (2016) Oxytocin reactivity during intergroup conflict in wild chimpanzees. Proceedings of the National Academy of Sciences, 14, 268–273. https://doi.org/10.1073/pnas.1616812114 DOI: https://doi.org/10.1073/pnas.1616812114

Seltzer, L. J., Ziegler, T. E. (2007) Non-invasive measurement of small peptides in the common marmoset (Callithrix jacchus): A radiolabeled clearance study and endogenous excretion under varying social conditions. Hormones and Behavior, 51, 436–442. https://doi.org/10.1016/j.yhbeh.2006.12.012 DOI: https://doi.org/10.1016/j.yhbeh.2006.12.012

Snowdon, C., Pieper, B., Boe, C., Cronin, K., Kurian, A., Ziegler, T. (2010) Variation in oxytocin is related to variation in affiliative behavior in monogamous, pairbonded tamarins. Hormones and Behavior, 58, 614–618. https://doi.org/10.1016/j.yhbeh.2010.06.014 DOI: https://doi.org/10.1016/j.yhbeh.2010.06.014

Spinolo, L. H., Raghow, R., Crowley, W. R. (1992). Oxytocin messenger RNA levels in hypothalamic, paraventricular, and supraoptic nuclei during pregnancy and lactation in rats. Annals of the New York Academy of Sciences, 652, 425–428. https://doi.org/10.1111/j.1749-6632.1992.tb34373.x DOI: https://doi.org/10.1111/j.1749-6632.1992.tb34373.x

Van Belle, S., Estrada, A., Strier, K. B. (2008). Social relationships among male Alouatta pigra. International Journal of Primatology, 29, 1481–1498. https://doi.org/10.1007/s10764-008-9309-y DOI: https://doi.org/10.1007/s10764-008-9309-y

Young, C. (2019) Agonistic behavior. Encyclopedia of animal cognition and behavior. Springer, New York. https://doi.org/10.1007/978-3-319-47829-6_320-1 DOI: https://doi.org/10.1007/978-3-319-47829-6_320-1

Wang, E., Milton, K. (2003) Intragroup social relationships of male Alouatta palliata on Barro Colorado Island, Republic of Panama. International Journal of Primatology, 24, 1227–1243. https://doi.org/10.1023/B:IJOP.0000005989.29238.ce DOI: https://doi.org/10.1023/B:IJOP.0000005989.29238.ce

Witting, R., Crockford, C., Deschner, T., Langergraber, K., Ziegler, T., Zuberbühler, K. (2014) Food sharing is linked to urinary oxytocin levels and bonding. Proceedings of the Royal Society, 281, e20133096. https://doi.org/10.1098/rspb.2013.3096 DOI: https://doi.org/10.1098/rspb.2013.3096

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Publicado

15-07-2021

Cómo citar

Moreno-Espinoza, D., Dias, P. A. D., Coyohua-Fuentes, A., Canales-Espinosa, D., & Rangel-Negrín, A. (2021). Social correlates of variation in urinary oxytocin concentrations of mantled howler monkeys Alouatta palliata (Gray, 1849) (Primates: Atelidae): A preliminary assessment. ACTA ZOOLÓGICA MEXICANA (N.S.), 37(1), 1–13. https://doi.org/10.21829/azm.2021.3712319
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