Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-02T20:04:12.522Z Has data issue: false hasContentIssue false
  • English
  • Français

Contribution of adult sex ratio to trauma and reproductive output in large breeding groups of rhesus macaques (Macaca mulatta)

Published online by Cambridge University Press:  01 January 2023

J Crast ,
MA Bloomsmith ,
CM Remillard  and
T Meeker
J Crast
Affiliation:
Yerkes National Primate Research Center, Emory University, Atlanta, GA 30329, USA
MA Bloomsmith*
Affiliation:
Yerkes National Primate Research Center, Emory University, Atlanta, GA 30329, USA
CM Remillard
Affiliation:
Yerkes National Primate Research Center, Emory University, Atlanta, GA 30329, USA
T Meeker
Affiliation:
Yerkes National Primate Research Center, Emory University, Atlanta, GA 30329, USA
*
* Contact for correspondence: [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Maintaining stable breeding groups of rhesus macaques (Macaca mulatta) can be challenging due to the complex social dynamics and despotic nature of the species. Trauma from aggression is a common problem in rhesus colonies and can cause social disruption, strain veterinary and animal management resources, and potentially affect reproduction. Previous research has shown that increasing the number of non-natal adult males in a breeding group can improve group stability, reduce trauma, and increase reproduction. Here, we used mixed-effects regression models to examine the effects of sex ratio and other factors on trauma and reproduction at the Yerkes National Primate Research Center using a historical dataset made up of four large rhesus groups over an eleven-year period (2003-2013). As expected, sex ratio was a significant predictor for both trauma and reproduction. However, group age since formation was a stronger predictor of trauma frequency and the amount of space available was a slightly better predictor of reproduction than sex ratio or trauma. These results indicate that improving sex ratios can be a viable management strategy to reduce trauma and improve reproduction, particularly when it is difficult to manipulate the group compositions and/or their housing situations. Reducing trauma is a primary goal for rhesus breeding colonies, as it directly impacts the monkeys’ health and psychological well-being. Such improvements are necessary for the ethical treatment and care of the animals themselves, but also to reduce financial burdens and maintain a healthy colony for research purposes.

Keywords

animal welfarereproductionrhesus macaquesex ratiosocial stabilitytrauma
Type
Research Article
Information
Animal Welfare , Volume 30 , Issue 4 , November 2021 , pp. 479 - 492
Copyright
© 2021 Universities Federation for Animal Welfare

References

Adams, MR, Kaplan, JR and Koritnik, DR 1985 Psychosocial influences on ovarian endocrine and ovulatory function in Macaca fascicularis. Physiology and Behavior 35: 935–940. https://doi.org/10.1016/0031-9384(85)90262-8CrossRefGoogle ScholarPubMed
Alberts, SC, Sapolsky, RM and Altmann, J 1992 Behavioral, endocrine, and immunological correlates of immigration by an aggressive male into a natural primate group. Hormones and Behavior 26: 167–178. https://doi.org/10.1016/0018-506X(92)90040-3CrossRefGoogle ScholarPubMed
Altmann, J and Alberts, SC 2003 Variability in reproductive suc-cess viewed from a life-history perspective in baboons. American Journal of Human Biology 15(3): 401–409. https://doi.org/10.1002/ajhb.10157CrossRefGoogle Scholar
Arcese, P and Smith, JNM 1988 Effects of population density and supplemental food on reproduction in song sparrows. Journal of Animal Ecology 57: 119–136. https://doi.org/10.2307/4768CrossRefGoogle Scholar
Asensio, N, Korstjen, AH, Schaffner, CM and Aureli, F 2008 Intragroup aggression, fission–fusion dynamics and feeding compe-tition in spider monkeys. Behaviour 145: 983–1001. https://doi.org/10.1163/156853908784089234CrossRefGoogle Scholar
Beisner, BA and Isbell, LA 2011 Factors affecting aggression among females in captive groups of rhesus macaques. American Journal of Primatology 73: 1152–1159. https://doi.org/10.1002/ajp.20982CrossRefGoogle ScholarPubMed
Beisner, BA, Jackson, ME, Cameron, A and McCowan, B 2011a Effects of natal male alliances on aggression and power dynamics in rhesus macaques. American Journal of Primatology 73: 790–801. https://doi.org/10.1002/ajp.20907CrossRefGoogle ScholarPubMed
Beisner, BA, Jackson, ME, Cameron, AN and McCowan, B 2011b Detecting instability in animal social networks: Genetic fragmentation is associated with social instability in rhesus macaques. PLoS One 6(1): e16365. https://doi.org/10.1371/journal.pone.0016365CrossRefGoogle ScholarPubMed
Beisner, BA, Jackson, ME, Cameron, A and McCowan, B 2012 Sex ratio, conflict dynamics and wounding in rhesus macaques (Macaca mulatta). Applied Animal Behavior Science 137:137–147. https://doi.org/10.1016/j.applanim.2011.07.008CrossRefGoogle ScholarPubMed
Beisner, BA and McCowan, B 2013 Policing in nonhuman pri-mates: Partial interventions serve a prosocial conflict management function in rhesus macaques. PLoS One 8(10): 1–13. https://doi.org/10.1371/journal.pone.0077369CrossRefGoogle Scholar
Bercovitch, FB and Lebron, MR 1991 Impact of artificial fissioning and social networks on levels of aggression and affiliation in primates. Aggressive Behavior 17: 17–25. https://doi.org/10.1002/1098-2337(1991)17:1<17::AID-AB2480170104>3.0.CO;2-F3.0.CO;2-F>CrossRefGoogle Scholar
Bernstein, IS 1964 Role of the dominant male rhesus monkey in response to external challenges to the group. Journal of Comparative and Physiological Psychology 57: 404–406. https://doi.org/10.1037/h0041409CrossRefGoogle ScholarPubMed
Bernstein, IS and Draper, WA 1964 The behavior of juvenile rhesus monkeys in groups. Animal Behaviour 12(1): 84–91. https://doi.org/10.1016/0003-3472(64)90107-1CrossRefGoogle Scholar
Bernstein, IS and Gordon, TP 1974 The function of aggression in primate societies. American Scientist 62: 304–311Google ScholarPubMed
Bernstein, IS, Gordon, TP and Rose, RM 1974 Factors influencing the expression of aggression during introductions to rhesus monkey groups. In: Holloway, RL (ed) Primate Aggression, Territoriality, and Xenophobia: A Comparative Perspective pp 211–240. Academic Press: New York, USAGoogle Scholar
Bonenfant, C, Gaillard, JM, Klein, F and Loison, A 2002 Sex and age-dependent effects of population density on life history traits of red deer Cervus elaphus in a temperate forest. Ecography 25: 446–458. https://doi.org/10.1034/j.1600-0587.2002.250407.xCrossRefGoogle Scholar
Borries, C, Larney, E, Lu, A, Ossi, K and Koenig, A 2008 Costs of group size: Lower developmental and reproductive rates in larg-er groups of leaf monkeys. Behavioral Ecology 19: 1186–1191. https://doi.org/10.1093/beheco/arn088CrossRefGoogle Scholar
Cameron, JL 1997 Stress and behaviorally induced reproductive dysfunction in primates. Seminars in Reproductive Medicine 15: 37–45. https://doi.org/10.1055/s-2008-1067966CrossRefGoogle ScholarPubMed
Caws, C and Aureli, F 2003 Chimpanzees cope with temporary reduction of escape opportunities. International Journal of Primatology 24: 1077–1091. https://doi.org/10.1023/A:1026280329544Google Scholar
Cleveland, A, Westergaard, GC, Trenkle, MK and Higley, JD 2004 Physiological predictors of reproductive outcome and moth-er–infant behaviors in captive rhesus macaque females (Macaca mulatta). Neuropsychopharmacology 29: 901–910. https://doi.org/10.1038/sj.npp.1300361Google ScholarPubMed
Cordoni, G and Palagi, E 2007 Response of captive lowland gorillas (Gorilla gorilla gorilla) to different housing conditions: Testing the aggression-density and coping models. Journal of Comparative Psychology 121: 171–180. https://doi.org/10.1037/0735-7036.121.2.171CrossRefGoogle ScholarPubMed
Crast, J, Bloomsmith, MA and Jonesteller, T 2015 Effects of changing housing conditions on mangabey behavior (Cercocebus atys): Spatial density, housing quality, and novelty effects. American Journal of Primatology 77: 1001–1014. https://doi.org/10.1002/ajp.22430CrossRefGoogle ScholarPubMed
Dahlgren, BT 1979 The effects of population density on fecundi-ty and fertility in the guppy, Poecilia reticulata. Journal of Fish Biology 15: 71–91. https://doi.org/10.1111/j.1095-8649.1979.tb03573.xCrossRefGoogle Scholar
Dazey, J, Kuyk, K, Oswald, M, Martenson, J and Erwin, J 1977 Effects of group composition on agonistic behavior of captive pig-tail macaques, Macaca nemestrina. American Journal of Physical Anthropology 46: 73–76. https://doi.org/10.1002/ajpa.1330460110CrossRefGoogle Scholar
Demaria, C and Thierry, B 1989 Lack of effects of environmen-tal changes on agonistic behavior patterns in a stabilizing group of stumptailed macaques (Macaca arctoides). Aggressive Behavior 15: 353–360. https://doi.org/10.1002/1098-2337(1989)15:5<353::AID-AB2480150504>3.0.CO;2-43.0.CO;2-4>CrossRefGoogle Scholar
Dettmer, AM, Novak, MA, Meyer, JS and Suomi, SJ 2014 Population density-dependent hair cortisol concentrations in rhe-sus monkeys (Macaca mulatta). Psychoneuroendocrinology 42: 59–67. https://doi.org/10.1016/j.psyneuen.2014.01.002CrossRefGoogle ScholarPubMed
Dettmer, AM, Woodward, RA and Suomi, SJ 2015 Reproductive consequences of a matrilineal overthrow in rhesus monkeys. American Journal of Primatology 77: 346–352. https://doi.org/10.1002/ajp.22350CrossRefGoogle ScholarPubMed
Deutsch, JC and Lee, PC 1991 Dominance and feeding compe-tition in captive rhesus monkeys. International Journal of Primatology 12: 615–628. https://doi.org/10.1007/BF02547673CrossRefGoogle Scholar
Dittus, WP 1980 The social regulation of primate populations: a synthesis. In: Lindburg, DG (ed) The Macaques: Studies in Ecology, Behavior and Evolution pp 263–286. Van Nostrand Reinhold Company: New York, USA.Google Scholar
Dittus, WPJ 1977 The social regulation of population density and age-sex distribution in the toque monkey. Behaviour 63: 281–322. https://doi.org/10.1163/156853977X00450CrossRefGoogle Scholar
Eaton, GG, Modahl, KB and Johnson, DF 1981 Aggressive behavior in a confined troop of Japanese macaques: effects of den-sity, season, and gender. Aggressive Behaviour 7: 145–164. https://doi.org/10.1002/1098-2337(1981)7:2<145::AID-AB2480070207>3.0.CO;2-M3.0.CO;2-M>CrossRefGoogle Scholar
Elton, RH and Anderson, BV 1977 The social behavior of a group of baboons (Papio anubis) under artificial crowding. Primates 18: 225–234. https://doi.org/10.1007/BF02382961CrossRefGoogle Scholar
Erwin, J 1979 Aggression in captive macaques: interaction of social and spatial factors. In: Erwin, J, Maple, TL and Mitchell, G (eds) Captivity and Behavior pp 139–171. Van Nostrand: New York, USAGoogle Scholar
Erwin, N and Erwin, J 1976 Social density and aggression in captive groups of pigtail monkeys (Macaca nemestrina). Applied Animal Ethology 2: 265–269. https://doi.org/10.1016/0304-3762(76)90059-6CrossRefGoogle Scholar
Flack, JC, de Waal, FBM and Krakauer, DC 2005 Social structure, robustness, and policing cost in a cognitively sophisticated species. The American Naturalist 165: 129–139. https://doi.org/10.1086/429277Google Scholar
Flack, JC, Girvan, M, de Waal, FBM and Krakauer, DC 2006 Policing stabilises construction of social niches in primates. Nature 439: 426–429. https://doi.org/10.1038/nature04326CrossRefGoogle ScholarPubMed
Goldstein, SJ and Richard, AF 1989 Ecology of rhesus macaques (Macaca mulatta) in northwest Pakistan. International Journal of Primatology 10(6): 531–567. https://doi.org/10.1007/BF02739364Google Scholar
Goss-Custard, J, Clarke, R and Durell, S 1984 Rates of food intake and aggression of oystercatchers (Haematopus ostralegus) on the most and least preferred mussel (Mytilus edulis) beds of the Exe Estuary. Journal of Animal Ecology 53(1): 233. https://doi.org/10.2307/4354CrossRefGoogle Scholar
Grenier, D, Barrette, C and Crete, M 1999 Food access by white-tailed deer (Odocoileus virginianus) at winter feeding sites in Eastern Quebec. Applied Animal Behaviour Science 63(4): 323–337. https://doi.org/10.1016/S0168-1591(99)00017-9CrossRefGoogle Scholar
Ha, JC, Alloway, H and Sussman, A 2011 Aggression in pigtailed macaque (Macaca nemestrina) breeding groups affects pregnancy outcome. American Journal of Primatology 73: 1169–1175. https://doi.org/10.1002/ajp.20984CrossRefGoogle ScholarPubMed
Harcourt, AH 1987 Dominance and fertility among female pri-mates. Zoological Society of London 213: 471–487. https://doi.org/10.1111/j.1469-7998.1987.tb03721.xCrossRefGoogle Scholar
Herrington, JA, Del Rosso, LA and Capitanio, JP 2016 Biobehavioral consequences of prenatal exposure to a matrilineal overthrow and relocation in captive infant rhesus (Macaca mulat-ta) monkeys. American Journal of Primatology 78(9): 895–903. https://doi.org/10.1002/ajp.22557CrossRefGoogle ScholarPubMed
Jenkins, TM Jr, Diehl, S, Kratz, KW and Cooper, SD 1999 Effects of population density on individual growth of brown trout in streams. Ecology 80: 941–956. https://doi.org/10.1890/0012-9658(1999)080[0941:EOPDOI]2.0.CO;2Google Scholar
Jones, KE, Patel, NG, Levy, MA, Storeygard, A, Balk, D, Gittleman, JL and Daszak, P 2008 Global trends in emerging infectious diseases. Nature 451: 990–994. https://doi.org/10.1038/nature06536CrossRefGoogle ScholarPubMed
Judge, P and de Waal, FBM 1993 Conflict avoidance among rhe-sus monkeys: coping with short-term crowding. Animal Behaviour 46: 221–232. https://doi.org/10.1006/anbe.1993.1184CrossRefGoogle Scholar
Judge, P, de Waal, FBM, Paul, KS and Gordon, TP 1994 Removal of a trauma-inflicting alpha matriline from a group of rhe-sus macaques to control severe wounding. Laboratory Animal Science 44: 344–350Google ScholarPubMed
Kaplan, JR, Chen, H, Appt, SE, Lees, CJ, Franke, AA, Berga, SL, Wilson, ME, Manuck, SB and Clarkson, TB 2010 Impairment of ovarian function and associated health-related abnormalities are attributable to low social status in pre-menopausal monkeys and not mitigated by a high-isoflavone soy diet. Human Reproduction 25: 3083–3094. https://doi.org/10.1093/humrep/deq288CrossRefGoogle Scholar
Lindburg, DG 1971 The rhesus monkey in north India: an ecological and behavioral study. In: Rosenblum, LA (ed) Primate Behavior: Developments in Field and Laboratory Research pp 1–106. Academic Press: New York, USA. https://doi.org/10.1016/B978-0-12-534002-1.50007-9CrossRefGoogle Scholar
Liu, B-J, Wu, C-F, Garber, PA, Zhang, P and Li, M 2018 Effects of group size and rank on mother-infant relationships and repro-ductive success in rhesus macaques (Macaca mulatta). American Journal of Primatology 80: e22881. https://doi.org/10.1002/ajp.22881CrossRefGoogle Scholar
Makwana, SC 1978 Field ecology and behaviour of the rhesus macaque (Macaca mulatta): Group composition, home range, roosting sites, and foraging routes in the Asarori forest. Primates 19: 483–492. https://doi.org/10.1007/BF02373310Google Scholar
Manson, JH 1995 Do female rhesus macaques choose novel males? American Journal of Primatology 37: 285–296. https://doi.org/10.1002/ajp.1350370403CrossRefGoogle ScholarPubMed
Mathy, J and Isbell, L 2001 The relative importance of size of food and interfood distance in eliciting aggression in captive rhe-sus macaques (Macaca mulatta). Folia Primatologica 72(5): 268–277. https://doi.org/10.1159/000049948Google ScholarPubMed
McCowan, B, Beisner, BA, Capitanio, JP, Jackson, ME, Cameron, A, Seil, S, Atwill, ER and Fushing, H 2011 Network stability is a balancing act of personality, power, and conflict dynamics in rhesus macaque societies. PLoS One 6: e22350. https://doi.org/10.1371/journal.pone.0022350CrossRefGoogle ScholarPubMed
McCowan, B, Beisner, BA and Hannibal, D 2018 Social man-agement of laboratory rhesus macaques housed in large groups using a network approach: A review. Behavioral Processes 156: 77–82. https://doi.org/10.1016/j.beproc.2017.11.014CrossRefGoogle Scholar
McGuire, MT, Cole, SR and Crookshank, C 1978 Effects of social and spatial density changes in Cercopithecus aethiops sabaeus. Primates 19: 615–631. https://doi.org/10.1007/BF02373630CrossRefGoogle Scholar
National Institutes of Health Office of Research Infrastructure Programs 2018 Non-human primate evaluation and analysis: Part 2 Report of the Expert Panel Forum on Challenges in Assessing Nonhuman Primate Needs and Resources for Biomedical Research. https://orip.nih.gov/sites/default/files/NHP%20Evaluation%20and%20Analysis%20Final%20%20Report%20-%20Part%202%20Final%20508%2021Dec2018_002.pdfGoogle Scholar
Nieuwenhuijsen, K and de Waal, FBM 1982 Effects of spatial crowding on social behavior in a chimpanzee colony. Zoo Biology 1: 5–28. https://doi.org/10.1002/zoo.1430010103CrossRefGoogle Scholar
Novak, MA and Drewsen, KH 1989 Enriching the lives of captive primates: issues and problems. In: Segal, EF (ed) Segal Housing, Care and Psychological Wellbeing of Captive and Laboratory Primates pp 161–182. Noyes Publications: Park Ridge, New Jersey, USAGoogle Scholar
Oates-O’Brien, RS, Farver, TB, Anderson-Vicino, KC, McCowan, B and Lerche, NW 2010 Predictors of matrilineal overthrows in large captive breeding groups of rhesus macaques (Macaca mulatta). Journal of the American Association for Laboratory Animal Science 49: 196–201Google ScholarPubMed
Pettorelli, N, Gaillard, JM, Van Laere, G, Duncan, P, Kjellander, P, Liberg, O, Delorme, D and Maillard, D 2002 Variations in adult body mass in roe deer: the effects of population density at birth and of habitat quality. Proceedings of the Royal Society. London. B: Biological Sciences 269: 747–753. https://doi.org/10.1098/rspb.2001.1791Google ScholarPubMed
Sade, DS, Cushing, K, Cushing, P, Dunaif, J, Figueroa, A and Kaplan, JR 1976 Population dynamics in relation to social structure on Cayo Santiago. Yearbook of Physical Anthropology 20: 253–262Google Scholar
Sahi, DN and Sharma, S 2004 An ecological and behavioural study on Macaca mulatta. In: Jammu, JK, Gupta, VK and Verma, AK (eds) Perspectives in Animal Ecology and Reproduction pp 201–213. Daya Publishing House: New Delhi, IndiaGoogle Scholar
Sanchez, DM, Herman, R and Wallen, K 2014 Matrilineal over-throws in captive groups of rhesus macaques (Macaca mulatta): a retrospective analysis. 37th Meeting of the American Society of Primatologists. 12-17 September 2014, Decatur, GA, USAGoogle Scholar
Sannen, A, Elsacker, LV and Eens, M 2004 Effect of spatial crowding on aggressive behavior in a bonobo colony. Zoo Biology 23: 383–395. https://doi.org/10.1002/zoo.20024CrossRefGoogle Scholar
Seth, PK and Seth, S 1985 Ecology and feeding behavior of the free ranging rhesus monkeys in India. Indian Anthropologist 15: 51–62Google Scholar
Singh, SD and Gupta, BS 1980 Xenophobic reactions of free-ranging rhesus infant groups raised in natural habitat. Primates 21: 492–497. https://doi.org/10.1007/BF02373837Google Scholar
Southwick, C, Beg, MA and Siddiqi, MR 1965 Rhesus monkeys in North India. In: DeVore, I (ed) Primate Behavior. Holt, Rinehart, and Winston: New York, USAGoogle Scholar
Southwick, CH 1967 An experimental study of intragroup ago-nistic behavior in rhesus monkeys (Macaca mulatta). Behaviour 28: 182–209. https://doi.org/10.1163/156853967X00235CrossRefGoogle ScholarPubMed
Southwick, CH 1969 Aggressive behaviour of rhesus monkeys in natural and captive groups. In: Garattini, S and Sigg, EB (eds) Sigg Aggressive Behavior pp 32–43. John Wiley: New York, USAGoogle Scholar
Southwick, CH, Beg, MA and Siddiqi, MR 1961 A population survey of rhesus monkeys in India: transportation routes and for-est areas. Ecology 42: 698–710. https://doi.org/10.2307/1933499CrossRefGoogle Scholar
Stavisky, RC, Ramsey, JK, Meeker, T, Stovall, M and Crane, MM 2018 Trauma rates and patterns in specific pathogen free (SPF) rhesus macaque (Macaca mulatta) groups. American Journal of Primatology 80(3): e22742. https://doi.org/10.1002/ajp.22742CrossRefGoogle ScholarPubMed
Steenbeek, R and van Schaik, CP 2001 Competition and group size in Thomas's langurs (Presbytis thomasil): The folivore paradox revisited. Behavioral Ecology and Sociobiology 49: 100–110. https://doi.org/10.1007/s002650000286CrossRefGoogle Scholar
Teas, J, Richie, T, Taylor, H and Southwick, CH 1980 Population patterns and behavioral ecology of rhesus monkeys in Nepal. In: Lindburg, DG (ed) The Macaques: Studies in Ecology, Behavior, and Evolution pp 247–262. Van Nostrand Reinhold Company: New York, USAGoogle Scholar
Vogel, ER, Much, S and Janson, CH 2007 Understanding esca-lated aggression over food resources in white-faced capuchin monkeys. Animal Behaviour 74(1): 71–80. https://doi.org/10.1016/j.anbehav.2007.02.003CrossRefGoogle Scholar
Weir, L and Grant, JW 2004 The causes of resource monopoli-sation: Interaction between resource dispersion and mode of competition. Ethology 110(1): 63–74. https://doi.org/10.1046/j.1439-0310.2003.00948.xCrossRefGoogle Scholar
Zumpe, D and Michael, RP 1987 Relation between the domi-nance rank of female rhesus monkeys and their access to males. American Journal of Primatology 13: 155–196. https://doi.org/10.1002/ajp.1350130206CrossRefGoogle Scholar