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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]
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Abstract

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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