Two-year laboratory experiment in group housing of young unrelated rhesus macaques: Analysis of behavioral dynamics and influence of social experience
DOI:
https://doi.org/10.33910/2687-1270-2025-6-1-125-136Keywords:
rhesus macaques, longitudinal study, affiliative behavior, social behavior, exploratory behavior, hierarchical relations, collective aggression, ontogenesis, sexual maturation, captive reproductionAbstract
Group housing of macaques in captivity requires strategies to mitigate injury risks and promote reproductive success. This study summarizes a two-year longitudinal observation of rhesus macaques (Macaca mulatta) grouped during early adolescence under controlled laboratory conditions. We aimed to analyze sex- and age-specific behavioral patterns post-grouping and after two years of cohabitation, while evaluating the impact of social experience on individual development. Nine unrelated rhesus macaques from the Kurchatov Complex of Medical Primatology were housed at the Pavlov Institute of Physiology. The cohort was stratified by age into older (16–18 months; 2 males, 2 females) and younger (14–16 months; 2 males, 3 females) subgroups. Hierarchical structures emerged within two months: older individuals consistently dominated younger counterparts, with stable intra-subgroup dominance relationships observed only among older macaques. Longitudinal behavioral shifts were pronounced in older individuals: males exhibited increased affiliative behaviors, whereas older females displayed heightened affiliative and exploratory behaviors. Collective aggression manifested during the third year, with younger females being most vulnerable. Reproductive onset occurred at 28–32 months, dominated by the older male. Although all females conceived by the third year, only the dominant older female delivered a viable offspring. These findings elucidate ontogenetic trajectories of primates in artificial social environments and inform best practices for maintaining unrelated macaques in laboratory settings.
References
ЛИТЕРАТУРА
Бутовская, М. Л., Файнберг, Л. А. (1993) У истоков человеческого общества (поведенческие аспекты эволюции человека). М.: Наука, 255 с.
Дерягина, М. А., Бутовская, М. Л. (1992) Этология приматов. М.: Изд-во Московского государственного университета, 192 с.
Мейшвили, Н. В. (1998) Социо-демографическое исследование родительского поведения низших обезьян в свете проблем антропосоциогенеза. Автореферат диссертации на соискание ученой степени кандидата биологических наук. М., Московский государственный университет им. М. В. Ломоносова, 21 с.
Мейшвили, Н. В., Чалян, В. Г., Липина, Я. Ю., Пачулия, И. Г. (2015) Сравнительное исследование поведения самцов макак-резусов в условиях индивидуального и группового содержания. В кн.: Д. Б. Богоявленская (ред.). От истоков к современности. 130 лет организации психологического общества при Московском университете: сборник материалов юбилейной конференции в 5 томах. Т. 5. М.: Когито-Центр, с. 422–424.
Фирсов, Л. А. (1977) Поведение антропоидов в природных условиях. Л.: Наука, 163 с.
Чалян, В. Г., Мейшвили, Н. В., Пачулия, И. Г. и др. (2023) Летальная агрессия у содержащихся в неволе обезьян. Российский физиологический журнал им. И. М. Сеченова, т. 109, № 2, с. 178–191. https://doi.org/10.31857/S0869813923020036
Beisner, B. A., Jackson, M. E., Cameron, A. N., McCowan, B. (2011) Detecting instability in animal social networks: Genetic fragmentation is associated with social instability in rhesus macaques. PLoS ONE, vol. 6, no. 1, article e16365. https://doi.org/10.1371/journal.pone.0016365
Beisner, B. A., Remillard, C. M., Moss, S. et al. (2021) Factors influencing the success of male introductions into groups of female rhesus macaques: Introduction technique, male characteristics and female behavior. American Journal of Primatology, vol. 83, no. 9, article e23314. https://doi.org/10.1002/ajp.23314
Bernstein, I. S. (1976) Dominance, aggression and reproduction in primate societies. Journal of Theoretical Biology, vol. 60, no. 2, pp. 459–472. https://doi.org/10.1016/0022-5193(76)90072-2
Casarrubea, M., Leca, J.-B., Gunst, N. et al. (2022) Structural analyses in the study of behavior: From rodents to non-human primates. Frontiers in Psychology, vol. 13, article 1033561. https://doi.org/10.3389/fpsyg.2022.1033561
Charbonneau, J. A., Amaral, D. G., Bliss-Moreau, E. (2022) Social housing status impacts rhesus monkeys’ affective responding in classic threat processing tasks. Scientific Reports, vol. 12, no. 1, article 4140. https://doi.org/10.1038/s41598-022-08077-4
Fischer, J. (2023) Aging rhesus monkeys stick to friends and family. Proceedings of the National Academy of Sciences, vol. 120, no. 1, article e2219062120. https://doi.org/10.1073/pnas.2219062120
Hannibal, D. L., Bliss-Moreau, E., Vandeleest, J. et al. (2017) Laboratory rhesus macaque social housing and social changes: Implications for research. American Journal Primatology, vol. 79, no. 1, article e22528. https://doi.org/10.1002/ajp.22528
Kaufmann, J. H. (1965) A three-year study of mating behavior in a freeranging band of rhesus monkeys. Ecology, vol. 46, no. 4, pp. 500–512. https://doi.org/10.2307/1934881
Kuznetsova, T. G., Golubeva, I. U., Meishvili, N. V., Chalyan, V. G. (2024) Group behavior of rhesus macaques in the second year of their lifespan. Journal of Evolutionary Biochemistry and Physiology, vol. 60, no. 6, pp. 2451– 2459. https://doi.org/10.1134/S0022093024060231
Ljungberg, T., Westlund, K. (2000) Impaired reconciliation in rhesus macaques with a history of early weaning and disturbed socialization. Primates, vol. 41, no. 1, pp. 79–88. https://doi.org/10.1007/BF02557463
Lutz, C. K., Coleman, K., Hopper, L. M. et al. (2022) Nonhuman primate abnormal behavior: Etiology, assessment, and treatment. American Journal of Primatology, vol. 84, no. 6, article e23380. https://doi.org/10.1002/ajp.23380
Maestripieri, D., Hoffman, C. L. (2012) Behavior and social dynamics of rhesus macaques on Cayo Santiago. In: Q. Wang (ed.). Bones, genetics, and behavior of rhesus macaques. Developments in primatology: Progress and prospects. New York: Springer Publ., pp. 247–262. https://doi.org/10.1007/978-1-4614-1046-1_12
Newman, L. E., Testard, C., DeCasien, A. R. et al. (2023) The biology of aging in a social world: Insights from free-ranging rhesus macaques. Neuroscience & Biobehavioral Reviews, vol. 154, article 105424. https://doi.org/10.1016/j.neubiorev.2023.105424
Newman, R., McKeown, S., Quirke, T. O’Riordan, R. M. (2021) The effect of a new enclosure on the behavior of a large captive group of lion-tailed macaques Macaca Silenus. Journal of Zoo and Aquarium Research, vol. 9, no. 1, pp. 20–25. https://doi.org/10.19227/jzar.v9i1.397
Novak, M. A. (2021) Self-Injurious behavior in rhesus macaques: Issues and challenges. American Journal of Primatology, vol. 83, no. 6, article e23222. https://doi.org/10.1002/ajp.23222
Pavez Fox, M. A., Siracusa, E. R., Ellis, S. et al. (2023) Socioecological drivers of injuries in female and male rhesus macaques (Macaca mulatta). BioRxiv. [Preprint]. Available at: https://doi.org/10.1101/2023.10.20.563310 (accessed 20.01.2025).
Qu, C., Ligneul, R., van der Henst, J.-B., Dreher, J.-C. (2017) An integrative interdisciplinary perspective on social dominance hierarchies. Trends in Cognitive Sciences, vol. 21, no. 11, pp. 893–908. http://dx.doi.org/10.1016/j.tics.2017.08.004
Reddy, R. B., Sandel, A. A. (2020) Social relationships between chimpanzee sons and mothers endure but change during adolescence and adulthood. Behavioral Ecology and Sociobiology, vol. 74, no. 12, article 150. https://doi.org/10.1007/s00265-020-02937-7
Reddy, R. B., Sandel, A. A., Dahl, R. E. (2022) Puberty initiates a unique stage of social learning and development prior to adulthood: Insights from studies of adolescence in wild chimpanzees. Developmental Cognitive Neuroscience, vol. 58, article 101176. https://doi.org/10.1016/j.dcn.2022.101176
Rommeck, I., Capitanio, J. P., Strand, S. C., McCowan, B. (2011) Early social experience affects behavioral and physiological responsiveness to stressful conditions in infant rhesus macaques (Macaca mulatta). American Journal of Primatology, vol. 73, no. 7, pp. 692–701. https://doi.org/10.1002/ajp.20953
Rothwell, E. S., Carp, S. B., Bliss-Moreau, E. (2023) The importance of social behavior in nonhuman primate studies of aging: A mini-review. Neuroscience & Biobehavioral Reviews, vol. 154, no. 13, article 105422. https://doi.org/10.1016/j.neubiorev.2023.105422
Simmons, H. A. (2016) Age-associated pathology in rhesus macaques (Macaca mulatta). Veterinary Pathology, vol. 53, no. 2, pp. 399–416. https://doi.org/10.1177/0300985815620628
Sliwa, J., Freiwald, W. A. (2017) A dedicated network for social interaction processing in the primate brain. Science, vol. 356, no. 6339, pp. 745–749. https://doi.org/10.1126/science.aam6383
Sosa, S. (2016) The influence of gender, age, matriline and hierarchical rank on individual social position, role and interactional patterns in Macaca sylvanus at ‘La Forêt des Singes’: A multilevel social network approach. Frontiers in Psychology, vol. 7, article 529. https://doi.org/10.3389/fpsyg.2016.00529
Thierry, B. (2007) Unity in diversity: Lessons from macaque societies. Evolutionary Anthropology Issues: News and Reviews, vol. 16, no. 6, pp. 224–238. https://doi.org/10.1002/evan.20147
Truelove, M. A., Martin, J. E., Langford, F. M., Leach, M. C. (2020) The identification of effective welfare indicators for laboratory-housed macaques using a Delphi consultation process. Scientific Reports, vol. 10, no. 1, article 20402. https://doi.org/10.1038/s41598-020-77437-9
Van Wagenen, G., Simpson, M. E. (1954) Testicular development in the rhesus monkey. The Anatomical Record, vol. 118, no. 2, pp. 231–251. https://doi.org/10.1002/ar.1091180209
Wooddell, L. J., Kaburu, S. S. K., Murphy, A. M. et al. (2017) Rank acquisition in rhesus macaque yearlings following permanent maternal separation: The importance of the social and physical environment. Developmental Psychobiology, vol. 59, no. 7, pp. 863–875. https://doi.org/10.1002/dev.21555
REFERENCES
Beisner, B. A., Jackson, M. E., Cameron, A. N., McCowan, B. (2011) Detecting instability in animal social networks: Genetic fragmentation is associated with social instability in rhesus macaques. PLoS ONE, vol. 6, no. 1, article e16365. https://doi.org/10.1371/journal.pone.0016365 (In English)
Beisner, B. A., Remillard, C. M., Moss, S. et al. (2021) Factors influencing the success of male introductions into groups of female rhesus macaques: Introduction technique, male characteristics and female behavior. American Journal of Primatology, vol. 83, no. 9, article e23314. https://doi.org/10.1002/ajp.23314 (In English)
Bernstein, I. S. (1976) Dominance, aggression and reproduction in primate societies. Journal of Theoretical Biology, vol. 60, no. 2, pp. 459–472. https://doi.org/10.1016/0022-5193(76)90072-2 (In English)
Butovskaya, M. L., Feinberg, L. A. (1993) U istokov chelovecheskogo obshchestva (povedencheskie aspekty evolyutsii cheloveka) [The origins of human society. Behavioral aspects of human evolution]. Moscow: Nauka Publ., 255 p. (In Russian)
Casarrubea, M., Leca, J.-B., Gunst, N. et al. (2022) Structural analyses in the study of behavior: From rodents to non-human primates. Frontiers in Psychology, vol. 13, article 1033561. https://doi.org/10.3389/fpsyg.2022.1033561 (In English)
Chalyan, V. G., Meishvili, N. V., Pachulia, I. G. et al. (2023) Letal’naya agressiya u soderzhashchikhsya v nevole obez’yan [Lethal aggression in captive monkeys]. Rossijskij fiziologicheskij zhurnal im. I. M. Sechenova — Russian Journal of Physiology, vol. 109, no. 2, pp. 178–191. https://doi.org/10.31857/S0869813923020036 (In Russian)
Charbonneau, J. A., Amaral, D. G., Bliss-Moreau, E. (2022) Social housing status impacts rhesus monkeys’ affective responding in classic threat processing tasks. Scientific Reports, vol. 12, no. 1, article 4140. https://doi.org/10.1038/s41598-022-08077-4 (In English)
Deryagina, M. A., Butovskaya, M. L. (1992) Etologiya primatov [Ethology of primates]. Moscow: Moscow State University Publ., 192 p. (In Russian)
Firsov, L. A. (1977) Povedenie antropoidov v prirodnykh usloviyakh [Behavior of anthropoids in natural conditions]. Leningrad: Nauka Publ., 163 p. (In Russian)
Fischer, J. (2023) Aging rhesus monkeys stick to friends and family. Proceedings of the National Academy of Sciences, vol. 120, no. 1, article e2219062120. https://doi.org/10.1073/pnas.2219062120 (In English)
Hannibal, D. L., Bliss-Moreau, E., Vandeleest, J. et al. (2017) Laboratory rhesus macaque social housing and social changes: Implications for research. American Journal Primatology, vol. 79, no. 1, article e22528. https://doi.org/10.1002/ajp.22528 (In English)
Kaufmann, J. H. (1965) A three-year study of mating behavior in a freeranging band of rhesus monkeys. Ecology, vol. 46, no. 4, pp. 500–512. https://doi.org/10.2307/1934881 (In English)
Kuznetsova, T. G., Golubeva, I. U., Meishvili, N. V., Chalyan, V. G. (2024) Group behavior of rhesus macaques in the second year of their lifespan. Journal of Evolutionary Biochemistry and Physiology, vol. 60, no. 6, pp. 2451– 2459. https://doi.org/10.1134/S0022093024060231 (In English)
Ljungberg, T., Westlund, K. (2000) Impaired reconciliation in rhesus macaques with a history of early weaning and disturbed socialization. Primates, vol. 41, no. 1, pp. 79–88. https://doi.org/10.1007/BF02557463 (In English)
Lutz, C. K., Coleman, K., Hopper, L. M. et al. (2022) Nonhuman primate abnormal behavior: Etiology, assessment, and treatment. American Journal of Primatology, vol. 84, no. 6, article e23380. https://doi.org/10.1002/ajp.23380 (In English)
Maestripieri, D., Hoffman, C. L. (2012) Behavior and social dynamics of rhesus macaques on Cayo Santiago. In: Q. Wang (ed.). Bones, genetics, and behavior of rhesus macaques. Developments in primatology: Progress and prospects. New York: Springer Publ., pp. 247–262. https://doi.org/10.1007/978-1-4614-1046-1_12 (In English)
Meyshvili, N. V. (1998) Sotsio-demorgaficheskoe issledovanie roditel’skogo povedeniya nizshikh obez’yan v svete problem antroposotsiogeneza [Socio-demographic study of parental behavior of lower apes in light of the problems of anthroposociogenesis]. Extended abstract of PhD dissertation (Biology). Moscow, M. V. Lomonosov Moscow State University, 21 p. (In Russian)
Meyshvili, N. V., Chalyan, V. G., Lipina, Ya. Yu., Pachulia, I. G. (2015) Sravnitel’noe issledovanie povedeniya samtsov makak-rezusov v usloviyakh individual’nogo i gruppovogo soderzhaniya [A comparative study of the behavior of housing individually or in group rhesus monkeys]. In: D. B. Bogoyavlenskaya (ed.). Ot istokov k sovremennosti. 130 let organizatsii psikhologicheskogo obshchestva pri Moskovskom universitete: sbornik materialov yubilejnoj konferentsii v 5 tomakh. T. 5 [From the origins to the present. 130 years of the organization of the Psychological Society at Moscow University: Collection of Proceedings of the anniversary conference in 5 volumes. Vol. 5]. Moscow: Kogito-Tsentr Publ., pp. 422–424. (In Russian)
Newman, L. E., Testard, C., DeCasien, A. R. et al. (2023) The biology of aging in a social world: Insights from free-ranging rhesus macaques. Neuroscience & Biobehavioral Reviews, vol. 154, article 105424. https://doi.org/10.1016/j.neubiorev.2023.105424 (In English)
Newman, R., McKeown, S., Quirke, T. O’Riordan, R. M. (2021) The effect of a new enclosure on the behavior of a large captive group of lion-tailed macaques Macaca Silenus. Journal of Zoo and Aquarium Research, vol. 9, no. 1, pp. 20–25. https://doi.org/10.19227/jzar.v9i1.397 (In English)
Novak, M. A. (2021) Self-Injurious behavior in rhesus macaques: Issues and challenges. American Journal of Primatology, vol. 83, no. 6, article e23222. https://doi.org/10.1002/ajp.23222 (In English)
Pavez Fox, M. A., Siracusa, E. R., Ellis, S. et al. (2023) Socioecological drivers of injuries in female and male rhesus macaques (Macaca mulatta). BioRxiv. [Preprint]. Available at: https://doi.org/10.1101/2023.10.20.563310 (accessed 20.01.2025). (In English)
Qu, C., Ligneul, R., van der Henst, J.-B., Dreher, J.-C. (2017) An integrative interdisciplinary perspective on social dominance hierarchies. Trends in Cognitive Sciences, vol. 21, no. 11, pp. 893–908. http://dx.doi.org/10.1016/j.tics.2017.08.004 (In English)
Reddy, R. B., Sandel, A. A. (2020) Social relationships between chimpanzee sons and mothers endure but change during adolescence and adulthood. Behavioral Ecology and Sociobiology, vol. 74, no. 12, article 150. https://doi.org/10.1007/s00265-020-02937-7 (In English)
Reddy, R. B., Sandel, A. A., Dahl, R. E. (2022) Puberty initiates a unique stage of social learning and development prior to adulthood: Insights from studies of adolescence in wild chimpanzees. Developmental Cognitive Neuroscience, vol. 58, article 101176. https://doi.org/10.1016/j.dcn.2022.101176 (In English)
Rommeck, I., Capitanio, J. P., Strand, S. C., McCowan, B. (2011) Early social experience affects behavioral and physiological responsiveness to stressful conditions in infant rhesus macaques (Macaca mulatta). American Journal of Primatology, vol. 73, no. 7, pp. 692–701. https://doi.org/10.1002/ajp.20953 (In English)
Rothwell, E. S., Carp, S. B., Bliss-Moreau, E. (2023) The importance of social behavior in nonhuman primate studies of aging: A mini-review. Neuroscience & Biobehavioral Reviews, vol. 154, no. 13, article 105422. https://doi. org/10.1016/j.neubiorev.2023.105422 (In English)
Simmons, H. A. (2016) Age-associated pathology in rhesus macaques (Macaca mulatta). Veterinary Pathology, vol. 53, no. 2, pp. 399–416. https://doi.org/10.1177/0300985815620628 (In English)
Sliwa, J., Freiwald, W. A. (2017) A dedicated network for social interaction processing in the primate brain. Science, vol. 356, no. 6339, pp. 745–749. https://doi.org/10.1126/science.aam6383 (In English)
Sosa, S. (2016) The influence of gender, age, matriline and hierarchical rank on individual social position, role and interactional patterns in Macaca sylvanus at ‘La Forêt des Singes’: A multilevel social network approach. Frontiers in Psychology, vol. 7, article 529. https://doi.org/10.3389/fpsyg.2016.00529 (In English)
Thierry, B. (2007) Unity in diversity: Lessons from macaque societies. Evolutionary Anthropology Issues: News and Reviews, vol. 16, no. 6, pp. 224–238. https://doi.org/10.1002/evan.20147 (In English)
Truelove, M. A., Martin, J. E., Langford, F. M., Leach, M. C. (2020) The identification of effective welfare indicators for laboratory-housed macaques using a Delphi consultation process. Scientific Reports, vol. 10, no. 1, article 20402. https://doi.org/10.1038/s41598-020-77437-9 (In English)
Van Wagenen, G., Simpson, M. E. (1954) Testicular development in the rhesus monkey. The Anatomical Record, vol. 118, no. 2, pp. 231–251. https://doi.org/10.1002/ar.1091180209 (In English)
Wooddell, L. J., Kaburu, S. S. K., Murphy, A. M. et al. (2017) Rank acquisition in rhesus macaque yearlings following permanent maternal separation: The importance of the social and physical environment. Developmental Psychobiology, vol. 59, no. 7, pp. 863–875. https://doi.org/10.1002/dev.21555 (In English)
Downloads
Published
Issue
Section
License
Copyright (c) 2025 Inna Yu. Golubeva, Tamara G. Kuznetsova, Maria N. Nikitina
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
The work is provided under the terms of the Public Offer and of Creative Commons public license Attribution-NonCommercial 4.0 International (CC BY-NC 4.0). This license allows an unlimited number of persons to reproduce and share the Licensed Material in all media and formats. Any use of the Licensed Material shall contain an identification of its Creator(s) and must be for non-commercial purposes only.
