Abstract
Herein we provide a review of the importance of social relationships on health and welfare of nonhuman primates. Social relationships are a key component of life for most primates. Sociality, however, comes with costs and benefits to health and welfare. When examining these benefits and costs we can look at two main types of primate relationships: dominance relationships/social status and affiliative relationships/social bonds. Over millions of years of evolution, many primate species experienced selection for larger brains (relative to body size) and living in cohesive social groups, which has resulted in a social life that is fundamentally linked to their welfare. These two evolutionary characteristics lead to complexity in both the dominance relationships and social bonds that develop in many primate societies. Individual dominance rank may be associated with differential risk of injury, exposure to stress, and other welfare-related outcomes because dominance relationships govern competitive interactions over access to resources and mating opportunities. Similarly, the affiliative social bonds between primates can also impact welfare because such interactions offer a way to cope with social stress yet increase risk of disease transmission via contact. Zoos, sanctuaries, research facilities, and other institutions that house nonhuman primates in captivity must take into consideration such social relationships in their management strategies and procedures to promote good welfare. Here we discuss these social relationships in relation to individual health, fitness, and well-being.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abbott DH, Keverne EB, Bercovitch FB et al (2003) Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm Behav 43(1):67–82. https://doi.org/10.1016/s0018-506x(02)00037-55
Adams MR, Kaplan JR, Clarkson TB, Koritnik DR (1985) Ovariectomy, social status, and atherosclerosis in cynomolgus monkeys. Arteriosclerosis 5(2):192–200. https://doi.org/10.1161/01.atv.5.2.192
Akinyi MY, Tung J, Jeneby M et al (2013) Role of grooming in reducing tick load in wild baboons (Papio cynocephalus). Anim Behav 85(3):559–568. https://doi.org/10.1016/j.anbehav.2012.12.012
Albert R, Jeong H, Barabasi AL (2000) Error and attack tolerance of complex networks. Nature 406:378–381. https://doi.org/10.1038/35019019
Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Syst 5:324–382. https://doi.org/10.1146/annurev.es.05.110174.001545
Alford PL, Bloomsmith MA, Keeling ME, Beck TF (1995) Wounding aggression during the formation and maintenance of captive, multimale chimpanzee groups. Zoo Biol 14(4):347–359. https://doi.org/10.1002/zoo.1430140406
Anderson JR, Chamove AS (1980) Self-aggression and social aggression in laboratory-reared macaques. J Abnorm Psychol 89(4):539–550. https://doi.org/10.1037/0021-843X.89.4.539
Archie EA, Altmann J, Alberts SC (2014) Costs of reproduction in a long-lived female primate: injury risk and wound healing. Behav Ecol Sociobiol 68(7):1183–1193. https://doi.org/10.1007/s00265-014-1729-4
Association for Assessment and Accreditation of Laboratory Animal Care Internatonal (2015) Position statements: social housing. https://www.aaalac.org/accreditation-program/position-statements/
Aureli F, Preston SD, de Waal FBM (1999) Heart rate responses to social interactions in free-moving rhesus macaques (Macaca mulatta): A pilot study. J Comp Psychol 113(1):59–65. https://doi.org/10.1037/0735-7036.113.1.59
Baker KC, Bloomsmith MA, Oettinger BC et al (2012) Benefits of pair housing are consistent across a diverse population of rhesus macaques. Appl Anim Behav Sci 137(3–4):148–156. https://doi.org/10.1016/j.applanim.2011.09.010
Balasubramaniam KN, Beisner BA, Vandeleest JJ et al (2016) Social buffering and contact transmission: network connections have beneficial and detrimental effects on Shigella infection risk among captive rhesus macaques. Peer J 4:e2630. https://doi.org/10.7717/peerj.2630
Barrett GM, Shimizu K, Bardi M et al (2002) Endocrine correlates of rank, reproduction, and female-directed aggression in male Japanese macaques (Macaca fuscata). Horm Behav 42(1):85–96. https://doi.org/10.1006/hbeh.2002.1804
Barton RA, Whiten A (1993) Feeding competition among female olive baboons, Papio anubis. Anim Behav 46(4):777–789. https://doi.org/10.1006/anbe.1993.1255
Barton RA, Byrne RW, Whiten A (1996) Ecology, feeding competition and social structure in baboons. Behav Ecol Sociobiol 38(5):321–329
Beisner B, Isbell LA (2008) Ground substrate affects activity budgets and hair loss in outdoor captive groups of rhesus macaques (Macaca mulatta). Am J Primatol 70(12):1160–1168. https://doi.org/10.1002/ajp.20615
Beisner BA, Isbell LA (2011) Factors affecting aggression among females in captive groups of rhesus macaques (Macaca mulatta). Am J Primatol 73(11):1152–1159. https://doi.org/10.1002/ajp.20982
Beisner BA, McCowan B (2013) Policing in nonhuman primates: partial interventions serve a prosocial conflict management function in rhesus macaques. PLoS One 8(10):e77369. https://doi.org/10.1371/journal.pone.0077369
Beisner BA, McCowan B (2014) Signaling context modulates social function of silent bared teeth displays in rhesus macaques (Macaca mulatta). Am J Primatol 76(2):111–121. https://doi.org/10.1002/ajp.22214
Beisner BA, Jackson ME, Cameron A, McCowan B (2012) Sex ratio, conflict dynamics and wounding in rhesus macaques (Macaca mulatta). Appl Anim Behav Sci 137(3–4):137–147. https://doi.org/10.1016/j.applanim.2011.07.008
Beisner BA, Hannibal DL, Finn KR et al (2016) Social power, conflict policing, and the role of subordination signals in rhesus macaque society. Am J Phys Anthropol 160(1):102–112. https://doi.org/10.1002/ajpa.22945
Bercovitch FB, Clarke AS (1995) Dominance rank, cortisol concentrations, and reproductive maturation in male rhesus macaques. Physiol Behav 58(2):215–221. https://doi.org/10.1016/0031-9384(95)00055-N
Bercovitch FB, Strum SC (1993) Dominance rank, resource availability, and reproductive maturation in female savanna baboons. Behav Ecol Sociobiol 33:313–318. https://doi.org/10.1007/bf00172929
Bernstein I, Gordon TP (1974) The function of aggression in primate societies. Am Sci 62:304–311
Bertram BCR (1978) Living in groups: predators and prey. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach. Blackwell, Oxford, pp 64–96
Boccia ML, Laudenslager M, Reite M (1988) Food distribution, dominance, and aggressive behaviors in bonnet macaques. Am J Primatol 16(2):123–130. https://doi.org/10.1002/ajp.1350160203
Boccia ML, Reite M, Laudenslager M (1989) On the physiology of grooming in a pigtail macaque. Physiol Behav 45(3):667–670. https://doi.org/10.1016/0031-9384(89)90089-9
Bradbury JW, Vehrencamp SL (1976) Social organization and foraging in emballonurid bats. Behav Ecol Sociobiol 1:337–381. https://doi.org/10.1007/BF00299284
Brennan J, Anderson JR (1988) Varying responses to feeding competition in a group of rhesus monkeys (Macaca mulatta). Primates 29:353–360. https://doi.org/10.1007/bf02380958
Byrne RW, Whiten A (1988) Machiavellian intelligence. Oxford University Press, Oxford
Byrne GD, Abbott KM, Suomi SJ (1996) Reorganization of dominance rank among adult males in a captive group of tufted capuchins (Cebus apella). Lab Primate Newsl 35:1–4
Cacioppo JT, Hawkley LC, Thisted RA (2010) Perceived social isolation makes me sad: 5-year cross-lagged analyses of loneliness and depressive symptomatology in the Chicago Health, Aging, and Social Relations Study. Psychol Aging 25(2):453–463. https://doi.org/10.1037/a0017216
Campbell CJ, Fuentes A, MacKinnon KC et al (2011) Primates in perspective. Oxford University Press, Oxford
Capitanio JP, Cole SW (2015) Social instability and immunity in rhesus monkeys: the role of the sympathetic nervous system. Philos Trans R Soc B Biol Sci 370(1669):20140104. https://doi.org/10.1098/rstb.2014.0104
Capitanio JP, Mendoza SP, Lerche NW (1998) Individual differences in peripheral blood immunological and hormonal measures in adult male rhesus macaques (Macaca mulatta): Evidence for temporal and situational consistency. Am J Primatol 44(1):29–41. https://doi.org/10.1002/(sici)1098-2345(1998)44:1<29::aid-ajp3>3.0.co;2-z
Capitanio JP, Mendoza SP, Lerche NW, Mason WA (1998) Social stress results in altered glucocorticoid regulation and shorter survival in simian acquired immune deficiency syndrome. Proc Natl Acad Sci U S A 95(8):4714–4719. https://doi.org/10.1073/pnas.95.8.4714
Capitanio JP, Hawkley LC, Cole SW, Cacioppo JT (2014) A behavioral taxonomy of loneliness in humans and rhesus monkeys (Macaca mulatta). PLoS One 9(10):e110307. https://doi.org/10.1371/journal.pone.0110307
Capitanio JP, Vandeleest J, Hannibal DL (2022) Physiological measures of welfare. In: Robinson LM, Weiss A (eds) Nonhuman primate welfare: from history, science, and ethics to practice. Springer, Cham, pp 231–254
Cavigelli SA (1999) Behavioural patterns associated with faecal cortisol levels in free-ranging female ring-tailed lemurs, Lemur catta. Anim Behav 57(4):935–944. https://doi.org/10.1006/anbe.1998.1054
Cavigelli SA, Caruso MJ (2015) Sex, social status and physiological stress in primates: the importance of social and glucocorticoid dynamics. Philos Trans R Soc B Biol Sci 370(1669):20140103. https://doi.org/10.1098/rstb.2014.0103
Chamove AS, Anderson JR, Morgan-Jones SC, Jones SP (1982) Deep woodchip litter: hygiene, feeding, and behavioral enhancement in eight primate species. Int J Study Anim Probl 3(4):308–318
Chancellor RL, Isbell LA (2009) Food site residence time and female competitive relationships in wild gray-cheeked mangabeys (Lophocebus albigena). Behav Ecol Sociobiol 63(10):1447–1458. https://doi.org/10.1007/s00265-009-0805-7
Chapman CA, Chapman LJ (2000) Constraints on group size in red colobus and red-tailed guenons: Examining the generality of the ecological constraints model. Int J Primatol 21:565–585. https://doi.org/10.1023/A:1005557002854
Cheney D, Seyfarth R (1990) Attending to behaviour versus attending to knowledge: examining monkeys’ attribution of mental states. Anim Behav 40(4):742–753. https://doi.org/10.1016/S0003-3472(05)80703-1
Christley RM, Pinchbeck GL, Bowers RG et al (2005) Infections in social networks: using network analysis to identify high-risk individuals. Am J Epidemiol 162(10):1024–1031. https://doi.org/10.1093/aje/kwi308
Clarke AS, Czekala NM, Lindburg DG (1995) Behavioral and adrenocortical responses of male cynomolgus and lion-tailed macaques to social stimulation and group formation. Primates 36:41–56. https://doi.org/10.1007/bf02381914
Clutton-Brock TH (1974) Primate social organisation and ecology. Nature 250:539–542. https://doi.org/10.1038/250539a0
Coe CL (1993) Psychosocial factors and immunity in nonhuman-primates: a review. Psychosom Med 55(3):298–308. https://doi.org/10.1097/00006842-199305000-00007
Coe CL, Mendoza SP, Levine S (1979) Social status constrains the stress response in the squirrel monkey. Physiol Behav 23(4):633–638. https://doi.org/10.1016/0031-9384(79)90151-3
Cohen S, Kaplan JR, Cunnick JE et al (1992) Chronic social stress, affiliation, and cellular immune-response in nonhuman primates. Psychol Sci 3(5):301–304. https://doi.org/10.1111/j.1467-9280.1992.tb00677.x
Cohen S, Line S, Manuck SB et al (1997) Chronic social stress, social status, and susceptibility to upper respiratory infections in nonhuman primates. Psychosom Med 59(3):213–221. https://doi.org/10.1097/00006842-199705000-00001
Cohen S, Janicki-Deverts D, Miller GE (2007) Psychological stress and disease. JAMA 298(14):1685–1687. https://doi.org/10.1001/jama.298.14.1685
Corner LAL, Pfeiffer DU, Morris RS (2003) Social-network analysis of Mycobacterium bovis transmission among captive brushtail possums (Trichosurus vulpecula). Prev Vet Med 59(3):147–167. https://doi.org/10.1016/S0167-5877(03)00075-8
Cowlishaw G, Dunbar RIM (1991) Dominance rank and mating success in male primates. Anim Behav 41(6):1045–1056. https://doi.org/10.1016/S0003-3472(05)80642-6
Creel S (2001) Social dominance and stress hormones. Trends Ecol Evol 16(9):491–497. https://doi.org/10.1016/S0169-5347(01)02227-3
Creel S, Dantzer B, Goymann W, Rubenstein DR (2013) The ecology of stress: effects of the social environment. Funct Ecol 27(1):66–80. https://doi.org/10.1111/j.1365-2435.2012.02029.x
Crockford C, Wittig RM, Whitten PL et al (2008) Social stressors and coping mechanisms in wild female baboons (Papio hamadryas ursinus). Horm Behav 53(1):254–265. https://doi.org/10.1016/j.yhbeh.2007.10.007
Darwin C (1871) The descent of man and selection in relation to sex. John Murray, London
Deutsch JC, Lee PC (1991) Dominance and feeding competition in captive rhesus monkeys. Int J Primatol 12:615–628. https://doi.org/10.1007/bf02547673
Dhabhar FS (2014) Effects of stress on immune function: the good, the bad, and the beautiful. Immunol Res 58(2–3):193–210. https://doi.org/10.1007/s12026-014-8517-0
Drewe JA, Perkins SE (2015) Disease transmission in animal social networks. In: Krause J, James R, Croft DP (eds) Animal social networks. Oxford University Press, Oxford, pp 95–110
Dunbar RIM (1988) Primate social systems. Chapman & Hall, London
Dunbar RIM (1991) Functional significance of social grooming in primates. Folia Primatol 57:121–131. https://doi.org/10.1159/000156574
Dunbar RIM (1998) The social brain hypothesis. Evol Anthropol 6(5):178–190. https://doi.org/10.1002/(SICI)1520-6505(1998)6:5%3C178::AID-EVAN5%3E3.0.CO;2-8
Eaton GG, Kelley ST, Axthelm MK et al (1994) Psychological well-being in paired adult female rhesus (Macaca mulatta). Am J Primatol 33(2):89–99. https://doi.org/10.1002/ajp.1350330204
Ehardt CL, Bernstein IS (1992) Conflict intervention behavior by adult male macaques: structural and functional aspects. In: Harcourt AH, De Waal FBM (eds) Coalitions and alliances in humans and other animals. Oxford University Press, Oxford, pp 83–111
Erwin J (1977) Factors influencing aggressive-behavior and risk of trauma in pigtail macaque (Macaca nemestrina). Lab Anim Sci 27:541–547
Erwin J, Anderson B, Erwin N et al (1976) Aggression in captive pigtail monkey groups: effects of provision of cover. Percept Mot Skills 42(1):319–324. https://doi.org/10.2466/pms.1976.42.1.319
Estep DQ, Baker SC (1991) The effects of temporary cover on the behavior of socially housed stumptailed macaques (Macaca arctoides). Zoo Biol 10(6):465–472. https://doi.org/10.1002/zoo.1430100605
Ethun K, Dicker S, Hughes B et al (2015) Use of novel automated feeders to control obesity of socially housed rhesus macaques. J Am Assoc Lab Anim Sci 54:661
European Commission (2010) Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes OJL276/33
Fairbanks LA, McGuire MT (1984) Determinants of fecundity and reproductive success in captive vervet monkeys. Am J Primatol 7(1):27–38. https://doi.org/10.1002/ajp.1350070106
Fairbanks LA, McGuire TM, Kerber W (1978) Effects of group-size, composition, introduction technique and cage apparatus on aggression during group formation in rhesus-monkeys. Psychol Rep 42(1):327–333. https://doi.org/10.2466/pr0.1978.42.1.327
Flack JC, de Waal FBM (2007) Context modulates signal meaning in primate communication. Proc Natl Acad Sci 104(5):1581–1586. https://doi.org/10.1073/pnas.0603565104
Flack JC, Krakauer DC (2006) Encoding power in communication networks. Am Nat 168(3):E87–E102. https://doi.org/10.1086/506526
Flack JC, de Waal FBM, Krakauer DC (2005a) Social structure, robustness, and policing cost in a cognitively sophisticated species. Am Nat 165(5):E126–E139. https://doi.org/10.1086/429277
Flack JC, Krakauer DC, de Waal FBM (2005b) Robustness mechanisms in primate societies: a perturbation study. Proc R Soc B Biol Sci 272(1568):1091–1099. https://doi.org/10.1098/rspb.2004.3019
Flack JC, Girvan M, de Waal FBM, Krakauer DC (2006) Policing stabilizes construction of social niches in primates. Nature 439:426–429. https://doi.org/10.1038/nature04326
Foerster S, Kithome K, Cords M, Monfort SL (2015) Social status and helminth infections in female forest guenons (Cercopithecus mitis). Am J Phys Anthropol 158(1):55–66. https://doi.org/10.1002/ajpa.22764
Fontenot MB, Wilkes MN, Lynch CS (2006) Effects of outdoor housing on self-injurious and stereotypic behavior in adult male rhesus macaques (Macaca mulatta). J Am Assoc Lab Anim Sci 45(5):35–43
Freeland WJ (1976) Pathogens and the evolution of primate sociality. Biotropica 8(1):12–24. https://doi.org/10.2307/2387816
Fushing H, Jordà Ò, Beisner B, McCowan B (2014) Computing systemic risk using multiple behavioral and keystone networks: The emergence of a crisis in primate societies and banks. Int J Forecast 30(3):797–806. https://doi.org/10.1016/j.ijforecast.2013.11.001
Gesquiere LR, Learn NH, Simao MCM et al (2011) Life at the top: rank and stress in wild male baboons. Science 333(6040):357–360. https://doi.org/10.1126/science.1207120
Gilbert MH, Baker KC (2011) Social buffering in adult male rhesus macaques (Macaca mulatta): effects of stressful events in single vs. pair housing. J Med Primatol 40(2):71–78. https://doi.org/10.1111/j.1600-0684.2010.00447.x
Goldberg JL, Grant JWA, Lefebvre L (2001) Effects of the temporal predictability and spatial clumping of food on the intensity of competitive aggression in the Zenaida dove. Behav Ecol 12(4):490–495. https://doi.org/10.1093/beheco/12.4.490
Gordon TP, Gust DA, Wilson ME et al (1992) Social separation and reunion affects immune-system in juvenile rhesus monkeys. Physiol Behav 51(3):467–472. https://doi.org/10.1016/0031-9384(92)90166-y
Gottlieb DH, Capitanio JP, McCowan BJ (2013) Risk factors for stereotypic behavior and self-biting in rhesus macaques (Macaca mulatta): animal’s history, current environment, and personality. Am J Primatol 75(10):995–1008. https://doi.org/10.1002/ajp.22161
Griffin RH, Nunn CL (2012) Community structure and the spread of infectious disease in primate social networks. Evol Ecol 26:779–800. https://doi.org/10.1007/s10682-011-9526-2
Gust DA, Gordon TP, Wilson ME et al (1991) Formation of a new social group of unfamiliar female rhesus monkeys affects the immune and pituitary adrenocortical systems. Brain Behav Immun 5(3):296–307. https://doi.org/10.1016/0889-1591(91)90024-5
Gust DA, Gordon TP, Wilson ME et al (1992) Removal from natal social group to peer housing affects cortisol levels and absolute numbers of T cell subsets in juvenile rhesus monkeys. Brain Behav Immun 6(2):189–199. https://doi.org/10.1016/0889-1591(92)90018-j
Gust D, Gordon TP, Hambright MK, Wilson ME (1993) Relationship between social factors and pituitary-adrenocortical activity in female rhesus monkeys (Macaca mulatta). Horm Behav 27(3):318–331. https://doi.org/10.1006/hbeh.1993.1024
Gust DA, Gordon TP, Brodie AR, McClure HM (1994) Effect of a preferred companion in modulating stress in adult female rhesus monkeys. Physiol Behav 55(4):681–684. https://doi.org/10.1016/0031-9384(94)90044-2
Habig B, Archie EA (2015) Social status, immune response and parasitism in males: a meta-analysis. Philos Trans R Soc B Biol Sci 370(1669):20140109. https://doi.org/10.1098/rstb.2014.0109
Hannibal D, Bliss-Moreau E, Vandeleest JJ et al (2017) Laboratory rhesus macaque social housing and social changes: implications for research. Am J Primatol 79(1):e22528. https://doi.org/10.1002/ajp.22528
Harcourt AH (1987) Dominance and fertility among female primates. J Zool Soc Lond 213(3):471–487. https://doi.org/10.1111/j.1469-7998.1987.tb03721.x
Harlow HF, Harlow MK (1962) Social deprivation in monkeys. Sci Am 207:136–146
Hausfater G, Watson DF (1976) Social and reproductive correlates of parasite ova emissions by baboons. Nature 262:688–689. https://doi.org/10.1038/262688a0
Heesen M, Rogahn S, Ostner J, Schülke O (2013) Food abundance affects energy intake and reproduction in frugivorous female Assamese macaques. Behav Ecol Sociobiol 67:1053–1066. https://doi.org/10.1007/s00265-013-1530-9
Hinde RA (1976) Interactions, relationships, and social structure. Man 11(1):1–17
Holt-Lunstad J, Smith TB, Layton JB (2010) Social relationships and mortality risk: a meta-analytic review. PLoS Med 7(7):e1000316. https://doi.org/10.1371/journal.pmed.1000316
Hooper LV, Littman DR, Macpherson AJ (2012) Interactions between the microbiota and the immune system. Science 336(6086):1268–1273. https://doi.org/10.1126/science.1223490
House JS, Landis KR, Umberson D (1988) Social relationships and health. Science 241(4865):540–545. https://doi.org/10.1126/science.3399889
Isbell LA (1991) Contest and scramble competition: patterns of female aggression and ranging behavior among primates. Behav Ecol 2(2):143–155. https://doi.org/10.1093/beheco/2.2.143
Isbell LA (2004) Is there no place like home? Ecological bases of female dispersal and philopatry and their consequences for the formation of kin groups. In: Chapais B, Berman CM (eds) Kinship and behavior in primates. Oxford University Press, Oxford, pp 71–108
Isbell LA, Pruetz JD, Lewis M, Young TP (1999) Rank differences in ecological behavior: a comparative study of patas monkeys (Erythrocebus patas) and vervets (Cercopithecus aethiops). Int J Primatol 20:257–272. https://doi.org/10.1023/A:1020574504017
Janson CH, Goldsmith ML (1995) Predicting group size in primates: foraging costs and predation risks. Behav Ecol 6(3):326–336. https://doi.org/10.1093/beheco/6.3.326
Kapsalis E, Berman C (1996) Models of affiliative relationships among free-ranging rhesus monkeys (Macaca mulatta). 2. Testing predictions for three hypothesized organizing principles. Behaviour 133(15/16):1235–1263
Kay RF, Plavcan JM, Glander KE, Wright PC (1988) Sexual selection and canine dimorphism in New World monkeys. Am J Phys Anthropol 77(3):385–397. https://doi.org/10.1002/ajpa.1330770311
Kempes MM, Gulickx MMC, van Daalen HJC et al (2008) Social competence is reduced in socially deprived rhesus monkeys (Macaca mulatta). J Comp Psychol 122(1):62–67. https://doi.org/10.1037/0735-7036.122.1.62
Keverne EB, Eberhart JA, Yodyingyuad U, Abbott DH (1984) Social influences on sex differences in the behaviour and endocrine state of talapoin monkeys. Prog Brain Res 61:331–347. https://doi.org/10.1016/S0079-6123(08)64445-3
Keverne EB, Martensz ND, Tuite B (1989) Beta-endorphin concentrations in cerebrospinal fluid of–monkeys are influenced by grooming relationships. Psychoneuroendocrinology 14(1–2):155–161. https://doi.org/10.1016/0306-4530(89)90065-6
Kikusui T, Winslow JT, Mori Y (2006) Social buffering: relief from stress and anxiety. Philos Trans R Soc B Biol Sci 361(1476):2215–2228. https://doi.org/10.1098/rstb.2006.1941
Kummer H (1967) Tripartite relations in hamadryas baboons. In: Altmann SA (ed) Social communication among primates. University of Chicago Press, Chicago, pp 113–121
Lankau EW, Turner PV, Mullan RJ, Galland GG (2014) Use of nonhuman primates in research in North America. J Am Assoc Lab Anim Sci 53(3):278–282
Lehmann J, Korstjens AH, Dunbar RIM (2007) Group size, grooming and social cohesion in primates. Anim Behav 74(6):1617–1629. https://doi.org/10.1016/j.anbehav.2006.10.025
Leigh SR (1994) Relations between captive and noncaptive weights in anthropoid primates. Zoo Biol 13(1):21–43. https://doi.org/10.1002/zoo.1430130105
Lutz CK, Novak MA (2005) Environmental enrichment for nonhuman primates: Theory and application. ILAR J 46(2):178–191. https://doi.org/10.1093/ilar.46.2.178
Lyons DM, Parker KJ (2007) Stress inoculation-induced indications of resilience in monkeys. J Trauma Stress 20(4):423–433. https://doi.org/10.1002/jts.20265
MacIntosh AJJ, Jacobs A, Garcia C et al (2012) Monkeys in the middle: parasite transmission through the social network of a wild primate. PLoS One 7(12):e51144. https://doi.org/10.1371/journal.pone.0051144
Majolo B, Lehmann J, Vizioli AD, Schino G (2012) Fitness-related benefits of dominance in primates. Am J Phys Anthropol 147(4):652–660. https://doi.org/10.1002/ajpa.22031
Manogue KR (1975) Dominance status and adrenocortical reactivity to stress in squirrel monkeys (Saimiri sciureus). Primates 14:457–463. https://doi.org/10.1007/BF02382742
Marmot M, Sapolsky RM (2014) Of baboons and men: Social circumstances, biology, and the social gradient in health. In: Weinstein M, Lane MA (eds) Sociality, hierarchy, health: comparative biodemography: a collection of papers. The National Academies Press, Washington, DC, pp 365–388
Mathy JW, Isbell LA (2001) The relative importance of size of food and interfood distance in eliciting aggression in captive rhesus macaques (Macaca mulatta). Folia Primatol 72(2):268–277. https://doi.org/10.1159/000049948
McCowan B, Anderson K, Heagarty A, Cameron A (2008) Utility of social network analysis for primate behavioral management and well-being. Appl Anim Behav Sci 109(2–4):396–405. https://doi.org/10.1016/j.applanim.2007.02.009
McCowan B, Beisner BA, Capitanio JP et al (2011) Network stability is a balancing act of personality, power, and conflict dynamics in rhesus macaque societies. PLoS ONE 6(8):e22350. https://doi.org/10.1371/journal.pone.0022350
McCowan B, Beisner BA, Bliss-Moreau E et al (2016) Connections matter: social networks and lifespan health in primate translational models. Front Psychol 7:433. https://doi.org/10.3389/fpsyg.2016.00433
McEwen BS (1998) Stress, adaptation, and disease: allostasis and allostatic load. Ann N Y Acad Sci 840(1):33–44. https://doi.org/10.1111/j.1749-6632.1998.tb09546.x
McKenna P, Hoffmann C, Minkah N et al (2008) The macaque gut microbiome in health, lentiviral infection, and chronic enterocolitis. PLoS Pathog 4(2):e20. https://doi.org/10.1371/journal.ppat.0040020
Melfi V, Poyser F (2007) Trichuris burdens in zoo-housed Colobus guereza. Int J Primatol 28:1449–1456. https://doi.org/10.1007/s10764-007-9206-9
Modlmeier AP, Keiser CN, Watters JV et al (2014) The keystone individual concept: an ecological and evolutionary overview. Anim Behav 89:53–62. https://doi.org/10.1016/j.anbehav.2013.12.020
Morimura N, Hirata S, Matsuzawa T (2022) Challenging cognitive enrichment: examples from caring for the chimpanzees in the Kumamoto Sanctuary, Japan and Bossou, Guinea. In: Robinson LM, Weiss A (eds) Nonhuman primate welfare: from history, science, and ethics to practice. Springer, Cham, pp 489–516
Muehlenbein MP, Watts DP (2010) The costs of dominance: testosterone, cortisol and intestinal parasites in wild male chimpanzees. BioPsychoSocial Med 4:21. https://doi.org/10.1186/1751-0759-4-21
Muller MN, Wrangham RW (2004) Dominance, cortisol, and stress in wild chimpanzees (Pan troglodytes). Behav Ecol Sociobiol 55:332–340. https://doi.org/10.1007/s00265-003-0713-1
National Research Council (2011) Guide for the care and use of laboratory animals, 8th edn. The National Academies Press, Washington, DC
NC3Rs (2006) NC3Rs guidelines: Primate accomodations, care and use. National Center for the Replacement, Refinement and Reduction of Animals in Research, London
Novak MA, Suomi SJ (1988) Psychological well-being of primates in captivity. Am Psychol 43(10):765–773. https://doi.org/10.1037/0003-066X.43.10.765
Oates-O’Brien RS, Farver TB, Anderson-Vicino KC et al (2010) Predictors of matrilineal overthrows in large captive breeding groups of rhesus macaques (Macaca mulatta). J Am Assoc Lab Anim Sci 49(2):196–201
Office of Laboratory Animal Welfare (2015). http://grants.nih.gov/grants/olaw/faqs.htm#1655
Ostner J, Heistermann M, Schülke O (2008) Dominance, aggression, and physiological stress in wild male Assamese macaques (Macaca assamensis). Horm Behav 54(5):613–619. https://doi.org/10.1016/j.yhbeh.2008.05.020
Perret M (1992) Environmental and social determinants of sexual function in the male lesser mouse lemur (Microcebus murinus). Folia Primatol 59(1):1–25. https://doi.org/10.1159/000156637
Petit O, Thierry B (1994) Aggressive and peaceful interventions in conflicts in Tonkean macaques. Anim Behav 48(6):1427–1436. https://doi.org/10.1006/anbe.1994.1378
Preuschoft S (1992) “Laughter” and “smile” in Barbary macaques (Macaca sylvanus). Ethology 91(3):220–236. https://doi.org/10.1111/j.1439-0310.1992.tb00864.x
Pusey A, Williams J, Goodall J (1997) The influence of dominance rank on the reproductive success of female chimpanzees. Science 277(5327):828–831. https://doi.org/10.1126/science.277.5327.828
Ray JC, Sapolsky RM (1992) Styles of male social behavior and their endocrine correlates among high-ranking wild baboons. Am J Primatol 28(4):231–250. https://doi.org/10.1002/ajp.1350280402
Rimbach R, Bisanzio D, Galvis N et al (2015) Brown spider monkeys (Ateles hybridus): a model for differentiating the role of social networks and physical contact on parasite transmission dynamics. Philos Trans R Soc Lond B Biol Sci 370(1669):20140110. https://doi.org/10.1098/rstb.2014.0110
Rowell TE (1974) The concept of social dominance. Behav Biol 11(2):131–154. https://doi.org/10.1016/S0091-6773(74)90289-2
Ruehlmann TE, Bernstein IS, Gordon TP, Balcaen P (1988) Wounding patterns in three species of captive macaques. Am J Primatol 14(2):125–134. https://doi.org/10.1002/ajp.1350140203
Rukstalis M, French JA (2005) Vocal buffering of the stress response: exposure to conspecific vocalizations moderates urinary cortisol excretion in isolated marmosets. Horm Behav 47(1):1–7. https://doi.org/10.1016/j.yhbeh.2004.09.004
Runcie DE, Wiedmann RT, Archie EA et al (2013) Social environment influences the relationship between genotype and gene expression in wild baboons. Philos Trans R Soc Lond B Biol Sci 368(1618):20120345. https://doi.org/10.1098/rstb.2012.0345
Saito C (1996) Dominance and feeding success in female Japanese macaques, Macaca fuscata: effects of food patch size and inter-patch distance. Anim Behav 51(5):967–980. https://doi.org/10.1006/anbe.1996.0100
Salathe M, Jones JH (2010) Dynamics and control of diseases in networks with community structure. PLoS Comput Biol 6(4):e1000736. https://doi.org/10.1371/journal.pcbi.1000736
Saltzman W, Schultz-Darken NJ, Wegner FH et al (1998) Suppression of cortisol levels in subordinate female marmosets: reproductive and social contributions. Horm Behav 33(1):58–74. https://doi.org/10.1006/hbeh.1998.1436
Santiago ML, Range F, Keele BF et al (2005) Simian immunodeficiency virus infection in free-ranging sooty mangabeys (Cercocebus atys atys) from the Taï Forest, Côte d’Ivoire: implications for the origin of epidemic human immunodeficiency virus type 2. J Virol 79(19):12515–12527. https://doi.org/10.1128/jvi.79.19.12515-12527.2005
Sapolsky RM (1982) The endocrine stress-response and social status in the wild baboon. Horm Behav 16(3):279–292. https://doi.org/10.1016/0018-506X(82)90027-7
Sapolsky RM (1983) Endocrine aspects of social instability in the olive baboon (Papio anubis). Am J Primatol 5(4):365–379. https://doi.org/10.1002/ajp.1350050406
Sapolsky RM (1992) Cortisol concentrations and the social significance of rank instability among wild baboons. Psychoneuroendocrinology 17(6):701–709. https://doi.org/10.1016/0306-4530(92)90029-7
Sapolsky RM (2005) The influence of social hierarchy on primate health. Science 308(5722):648–652. https://doi.org/10.1126/science.1106477
Sapolsky RM, Mott GE (1987) Social subordinance in wild baboons is associated with suppressed high density lipoprotein-cholesterol concentrations: the possible role of chronic social stress. Endocrinology 121(5):1605–1610. https://doi.org/10.1210/endo-121-5-1605
Sapolsky RM, Ray JC (1992) Styles of male social behavior and their endocrine correlates among high-ranking wild baboons. Am J Primatol 28(4):231–250. https://doi.org/10.1002/ajp.1350280402
Sapolsky RM, Share LJ (1994) Rank-related differences in cardiovascular function among wild baboons: role of sensitivity to glucocorticoids. Am J Primatol 32(4):261–268. https://doi.org/10.1002/ajp.1350320404
Sapolsky RM, Spencer E (1997) Insulin-like growth factor I is suppressed in socially subordinate male baboons. Am J Physiol 273(4):R1346–R1351. https://doi.org/10.1152/ajpregu.1997.273.4.R1346
Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21(1):55–89. https://doi.org/10.1210/edrv.21.1.0389
Schapiro SJ, Nehete PN, Perlman JE, Sastry KJ (2000) A comparison of cell-mediated immune responses in rhesus macaques housed singly, in pairs, or in groups. Appl Anim Behav Sci 68(1):67–84. https://doi.org/10.1016/s0168-1591(00)00090-3
Schoener TW (1971) Theory of feeding strategies. Annu Rev Ecol Syst 2:369–404. https://doi.org/10.1146/annurev.es.02.110171.002101
Schwitzer C, Kaumanns W (2001) Body weights of ruffed lemurs (Varecia variegata) in European zoos with reference to the problem of obesity. Zoo Biol 20(4):261–269. https://doi.org/10.1002/zoo.1026
Scott J, Lockard JS (2006) Captive female gorilla agonistic relationships with clumped defendable food resources. Primates 47:199–209. https://doi.org/10.1007/s10329-005-0167-3
Setchell JM, Smith T, Wickings EJ, Knapp LA (2008) Factors affecting fecal glucocorticoid levels in semi-free-ranging female mandrills (Mandrillus sphinx). Am J Primatol 70(11):1023–1032. https://doi.org/10.1002/ajp.20594
Shively CA, Clarkson TB (1994) Social status and coronary artery atherosclerosis in female monkeys. Arterioscler Thromb 14(5):721–726. https://doi.org/10.1161/01.ATV.14.5.721
Shively CA, Day SM (2015) Social inequalities in health in nonhuman primates. Neurobiol Stress 1:156–163. https://doi.org/10.1016/j.ynstr.2014.11.005
Shutt K, MacLarnon A, Heistermann M, Semple S (2007) Grooming in Barbary macaques: better to give than to receive? Biol Lett 3(3):231–233. https://doi.org/10.1098/rsbl.2007.0052
Sicotte P (1995) Interposition in conflicts between males in bimale groups of mountain gorillas. Folia Primatol 65(1):14–24. https://doi.org/10.1159/000156871
Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302(5648):1231–1234. https://doi.org/10.1126/science.1088580
Silk JB, Beehner JC, Bergman TJ et al (2009) The benefits of social capital: close social bonds among female baboons enhance offspring survival. Proc R Soc B Biol Sci 276(1670):3099–3104. https://doi.org/10.1098/rspb.2009.0681
Silk JB, Beehner JC, Bergman TJ et al (2010) Strong and consistent social bonds enhance the longevity of female baboons. Curr Biol 20(15):1359–1361. https://doi.org/10.1016/j.cub.2010.05.067
Small M (1981) Body fat, rank, and nutritional status in a captive group of rhesus macaques. Int J Primatol 2:91–95. https://doi.org/10.1007/BF02692303
Smith DG (2012) Taxonomy of nonhuman primates used in biomedical research. In: Abee C, Mansfield K, Tardif S, Morris T (eds) Nonhuman primates in biomedical research: biology and management, vol 1. Elsevier, New York, pp 57–85
Smith TE, French JA (1997) Social and reproductive conditions modulate urinary cortisol excretion in black tufted-ear marmosets (Callithrix kuhli). Am J Primatol 42(4):253–267. https://doi.org/10.1002/(sici)1098-2345(1997)42:4%3C253::aid-ajp1%3E3.0.co;2-w
Smuts BB, Cheney D, Seyfarth R et al (1987) Primate societies. University of Chicago Press, Chicago
Stahl D, Kaumanns W (2003) Food competition in captive female sooty mangabeys (Cercocebus torquatus atys). Primates 44(3):203–216. https://doi.org/10.1007/s10329-002-0012-x
Sterck EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291–309. https://doi.org/10.1007/s002650050390
Suomi SJ, Harlow HF, Kimball SD (1971) Behavioral effects of prolonged partial social isolation in the rhesus monkey. Psychol Rep 29(3):1171–1177. https://doi.org/10.2466/pr0.1971.29.3f.1171
Suomi SJ, Collins ML, Harlow HF (1973) Effects of permanent separation from mother on infant monkeys. Dev Psychol 9(3):376–384. https://doi.org/10.1037/h0034896
Tajiama T, Kurotori H (2010) Nonaggressive interventions by third parties in conflict among captive Bornean orangutans (Pongo pygmaeus). Primates 51(2):179–182. https://doi.org/10.1007/s10329-009-0180-z
The Commission of European Communities (2007) Commission recommendation of 18 June 2007 on guidelines for the accommodation and care of animals used for experimental and other scientific purposes. Off J Eur Union 30.7.2007:L197/1–L197/89. https://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2007:197:0001:0089:EN:PDF
Thierry B, Iwaniuk AN, Pellis SM (2000) The influence of phylogeny on the social behaviour of macaques (Primates: Cercopithedicdae, genus Macaca). Ethology 106(8):713–728. https://doi.org/10.1046/j.1439-0310.2000.00583.x
Thierry B, Singh M, Kaumanns W (2004) Macaque societies: a model for the study of social organization. Cambridge University Press, Cambridge
Tung J, Barreiro LB, Burns MB et al (2015) Social networks predict gut microbiome composition in wild baboons. Elife 4:e05224. https://doi.org/10.7554/eLife.05224
Turnbaugh PJ, Hamady M, Yatsunenko T et al (2009) A core gut microbiome in obese and lean twins. Nature 457:480–484. https://doi.org/10.1038/nature07540
U.S. Department of Agriculture (2013) Animal Welfare Act and Animal Welfare Regulations
van Noordwijk M, van Schaik CP (1999) The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques, Macaca fascicularis. Primates 40:105–130. https://doi.org/10.1007/BF02557705
van Schaik CP (1983) Why are diurnal primates living in groups? Behaviour 87(1/2):120–144
van Schaik CP (1989) The ecology of social relationships amongst female primates. In: Standen V, Foley RA (eds) Comparative socioecology: the behavioural ecology of humans and other mammals. Blackwell Scientific Publications, Oxford, pp 195–218
van Schaik CP, van Hooff JARAM (1983) On the ultimate causes of primate social systems. Behaviour 85(1/2):91–117
van Schaik CP, van Noordwijk M (1988) Scramble and contest in feeding competition among female long-tailed macaques (Macaca fascicularis). Behaviour 105(1/2):77–98. https://doi.org/10.1163/156853988X00458
Vandeleest JJ, McCowan BJ, Capitanio JP (2011) Early rearing interacts with temperament and housing to influence the risk for motor stereotypy in rhesus monkeys (Macaca mulatta). Appl Anim Behav Sci 132(1–2):81–89. https://doi.org/10.1016/j.applanim.2011.02.010
Vandeleest JJ, Beisner BA, Hannibal DL et al (2016) Decoupling social status and status certainty effects on health in macaques: a network approach. PeerJ 4:e2394. https://doi.org/10.7717/peerj.2394
Videan EN, Fritz J, Murphy J (2007) Development of guidelines for assessing obesity in captive chimpanzees (Pan troglodytes). Zoo Biol 26(2):93–104. https://doi.org/10.1002/zoo.20122
Vitone ND, Altizer S, Nunn CL (2004) Body size, diet and sociality influence the species richness of parasitic worms in anthropoid primates. Evol Ecol Res 6(2):183–199
von Rohr CR, Koski SE, Burkart JM et al (2012) Impartial third-party interventions in captive chimpanzees: a reflection of community concern. PLoS ONE 7(3):e32494. https://doi.org/10.1371/journal.pone.0032494
Weingrill T, Gray DA, Barrett L, Henzi SP (2004) Fecal cortisol levels in free-ranging female chacma baboons: relationship to dominance, reproductive state and environmental factors. Horm Behav 45(4):259–269. https://doi.org/10.1016/j.yhbeh.2003.12.004
Whitacre JM (2010) Degeneracy: a link between evolvability, robustness and complexity in biological systems. Theor Biol Med Model 7:6. https://doi.org/10.1186/1742-4682-7-6
Whitten PL (1983) Diet and dominance among female vervet monkeys (Cercopithecus aethiops). Am J Primatol 5(2):139–159. https://doi.org/10.1002/ajp.1350050205
Wilson ME, Fisher J, Fischer A et al (2008) Quantifying food intake in socially housed monkeys: social status effects on caloric consumption. Physiol Behav 94(4):586–594. https://doi.org/10.1016/j.physbeh.2008.03.019
Wittig RM, Crockford C, Lehmann J et al (2008) Focused grooming networks and stress alleviation in wild female baboons. Horm Behav 54(1):170–177. https://doi.org/10.1016/j.yhbeh.2008.02.009
Wrangham R (1980) An ecological model of female-bonded primate groups. Behaviour 75(3/4):262–300
Yodyingyuad U, de la Riva C, Abbott DH et al (1985) Relationship between dominance hierarchy, cerebrospinal fluid levels of amine transmitter metabolites (5-hydroxyindole acetic acid and homovanillic acid) and plasma cortisol in monkeys. Neuroscience 16(4):851–858. https://doi.org/10.1016/0306-4522(85)90099-5
Young C, Majolo B, Heistermann M et al (2014) Responses to social and environmental stress are attenuated by strong male bonds in wild macaques. Proc Natl Acad Sci U S A 111(51):18195–18200. https://doi.org/10.1073/pnas.1411450111
Zehr JL, Van Meter PE, Wallen K (2005) Factors regulating the timing of puberty onset in female rhesus monkeys (Macaca mulatta): role of prenatal androgens, social rank, and adolescent body weight. Biol Reprod 72(5):1087–1094. https://doi.org/10.1095/biolreprod.104.027755
Ziegler TE, Scheffler G, Snowdon CT (1995) The relationship of cortisol levels to social environment and reproductive functioning in female cotton-top tamarins, Saguinus oedipus. Horm Behav 29(3):407–424. https://doi.org/10.1006/hbeh.1995.1028
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2023 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Beisner, B.A., Hannibal, D.L., Vandeleest, J.J., McCowan, B. (2023). Sociality, Health, and Welfare in Nonhuman Primates. In: Robinson, L.M., Weiss, A. (eds) Nonhuman Primate Welfare. Springer, Cham. https://doi.org/10.1007/978-3-030-82708-3_18
Download citation
DOI: https://doi.org/10.1007/978-3-030-82708-3_18
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-82707-6
Online ISBN: 978-3-030-82708-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)