Introduction to the social housing of primates

One of the most important forms of enrichment that can be provided for any captive, gregarious primate species is social housing. Primate social housing can consist of groupings of two to 100 or more members; captive housing composition should be guided by the species’ typical social structure found in the wild. Knowledge of the natural behavior of individual species is crucial in proper captive management of nonhuman primates (see Primate Info Net Factsheets for species-specific information).

The implementation of a social housing program for facilities with nonhuman primates, including laboratories, zoos, and sanctuaries, requires special attention to ensure the successful formation and maintenance of social groups. Social housing should be overseen by individuals with expertise in nonhuman primate behavior as animals housed socially require ongoing monitoring to ensure compatibility and to reduce the possibility of injury or distress. 

Scientific studies have shown that captive primates who are housed socially exhibit higher levels of species-appropriate behavior, lower levels of stress (both behavioral and physiological indices of stress) and, overall, demonstrate well-being that is superior to that of their singly-housed counterparts.

American Society of Primatologists Policy Statement
Social Housing for Nonhuman Primates Used in Biomedical or
Behavioral Research in the United States

Background: The following policy statement was formulated by the ASP Primate Care Committee for the purpose of providing a public document regarding the ASP’s stance on the use of social housing for nonhuman primates used in research. There is considerable scientific literature on the topic of social housing in laboratory primates, and best practices will continue to evolve over time. Therefore, this policy statement does not address specific scientific findings, rather it articulates general principles held by the society. Since there is variation across practices and regulatory requirements internationally, the scope of this policy is on primates in the United States. These guidelines build upon the ASP’s 2001 Policy Statement “Principles for the Ethical Treatment of Non-Human Primates” which states that ASP members “should make use of information on a species’ natural history to improve management and enrich environments, because physical and psychological well-being are essential not only to the health of the animal but also to the validity of the research results.”

Policy Statement: The ASP endorses social housing as the foundation of welfare for captive nonhuman primates who are members of species that live socially in the wild. (We recognize that social housing may not be appropriate for the very few, more solitary primate species.) The position that social housing should be the default housing for nonhuman primates is based upon the scientific literature, which establishes that socially-housed primates demonstrate wellbeing that is superior to that of their singly-housed counterparts, and that introduction of singly housed primates into a compatible social setting improves their welfare by a variety of behavioral and physiological measures. For example, social housing reduces the expression of species-inappropriate behaviors, promotes species-appropriate activities and can buffer individuals from stress. 

This endorsement is consistent with the positions of the United State Department of Agriculture (USDA), the Office of Laboratory Animal Welfare (OLAW), and the Association for Assessment and Accreditation of Laboratory Animal Care International (AAALAC). The USDA Animal Welfare Act regulation 9 CFR 3.81, states that plans for environmental enhancement must “address the social needs of nonhuman primates of species known to exist in social groups in nature” (USDA, 2013, p. 100). Public Health Service Policy (2002) states that, “The living conditions of animals should be appropriate for their species and contribute to their health and comfort” (OLAW, 2002, p. 5). OLAW has articulated its view on nonhuman primate housing in a policy statement affirming that “like all social animals, nonhuman primates should be socially housed”. Furthermore, AAALAC endorses social housing as the default approach, accrediting only those facilities that meet the standards outlined in The Guide for the Care and Use of Laboratory Animals, i.e., “Social animals should be housed in stable pairs or groups of compatible individuals unless they must be housed alone for experimental reasons or because of social incompatibility” (National Research Council, 2011, p. 64).

To this end, implementing a social housing program for laboratory primates requires special attention to overcome challenges and obstacles encountered in a research setting. The ASP concurs with the following statements:

  1. Appropriately implemented social housing should be guided by species-typical social structure, but may also be beneficial in configurations that do not replicate social groupings in the wild. Ideal configurations may not be feasible given the number or age/sex class of research subjects, or because of constraints related to study design, available housing, or clinical condition. However, the form of housing that involves the least restriction to social experience should be employed whenever practical. This practice is in line with the view that increased social and environmental complexity is associated with increased wellbeing. Even social housing for some portions of time or providing a limited degree of social contact should generally be seen as superior to individual housing.
  2. Housing must be guided by the research use of individual nonhuman primates. Institutional Animal Care and Use Committees (IACUCs) play a pivotal role in this process and are charged with ensuring that scientific justifications for restricted social housing are robust and evidence based. Therefore, it is critical that IACUCs have access to the necessary expertise by including on the committee at least one member with advanced training (i.e., Ph.D.-level expertise) in nonhuman primate behavior and management. The composition of social groups and changes in social setting may be determined by the timeline and experimental design of research projects with justification for restricted social contact during certain phases of a research project. In this case, single housing or restricted contact (including part-time social housing, or tactile contact through a barrier which prevents entry into a partner’s enclosure) should be limited to study phases in which scientific justification for the social restriction applies. The implementation of social housing requires close coordination between research personnel and individuals who are responsible for behavioral and clinical management of the primates. 
  3. Formation and maintenance of social groupings can involve risks to animal health and wellbeing, and should be overseen by individuals with expertise in nonhuman primate behavior and awareness of the relevant aspects of a research protocol’s study design. Animals housed socially require ongoing monitoring to ensure compatibility and reduce the possibility of injury or distress, as initial compatibility may not continue over time. For example, social compatibility may be impacted by changes in study procedures, maturation, aging, clinical impacts of the research procedures or environmental factors. However, it is recognized that even experienced personnel may not be able to manage social interactions in such a way as to avoid all conflict or injury among the animals. 
  4. The need for single housing should not be assumed in research involving the application of experimental appliances (e.g., telemetry implants, head caps, eye coils, tethers), the administration of substances exerting psychosocial effects, or use of restricted/controlled diets. Such research has been successfully performed on socially housed subjects. The potential need for single housing or restriction in social housing should be evaluated using available literature, or, where lacking, awareness of practices and outcomes across facilities. 
  5. The AWA exemption from social housing relating to individuals exhibiting ‘vicious or overly aggressive behavior’ or debilitation should not be applied to broad classes of individuals or species unless supported by published literature or other performance outcomes. Objective criteria should be established for deeming individual animals exempt for these reasons.
  6. Anticipated financial constraints or lack of resources such as appropriate caging are not a sufficient reason to fail to provide social housing. Furthermore, when assessing the potential financial impact of social housing, one should realize the impact that the prolonged use of single housing can have on the costs of lifetime care. Single housing may lead to the need for increased behavioral management and veterinary services to address compromised wellbeing, treatment of behavioral abnormalities that may develop, and adverse impact on research if behavioral abnormalities are severe.

References

National Research Council. The Guide for the Care and Use of Laboratory Animals, 2011.

Office of Laboratory Animal Welfare position statement on nonhuman primate housing. Retreived from http://grants.nih.gov/grants/olaw/positionstatement_guide.htm#nonhuman June 2, 2014.

Public Health Service Policy on Humane Care and Use of Laboratory Animals. United States Department of Health and Human Services, Washington, DC, 1986; amended 2002.

U. S. Department of Agriculture. Animal Welfare Act and Animal Welfare Regulations. Section 3.81 – Environmental enhancement to promote psychological well-being. Animal Welfare Act and Animal Welfare Regulations (“Blue Book”) 2013.

There are workshops available that include curriculum regarding social housing techniques and management practices for nonhuman primates. These workshops are not endorsed by the American Society of Primatologists, but they may be useful to those trying to learn more about introduction methodologies and group management.

Annual

Benefits of Social Housing

Baker KC, Bloomsmith MA, Oettinger B, Neu K, Griffis C, Schoof V, Maloney M. 2012. Benefits of pair housing are consistent across a diverse population of rhesus macaques. Applied Animal Behaviour Science 137(3):148-156.

DiVincenti Jr L, Wyatt JD. 2011. Pair housing of macaques in research facilities: a science-based review of benefits and risks. Journal of the American Association for Laboratory Animal Science 50(6):856-863.

Doyle LA, Baker KC, Cox LD. 2008. Physiological and behavioral effects of social introduction on adult male rhesus macaques. American Journal of Primatology 70(6):542-550.

Gilbert MH, Baker KC. 2011. Social buffering in adult male rhesus macaques (Macaca mulatta): Effects of stressful events in single vs. pair housing. Journal of Medical Primatology 40(2):71-78.

Kessel A, Brent L. 2001. The rehabilitation of captive baboons. Journal of Medical Primatology 30(2):71-80.

Mallapur A, Waran N, Sinha A. 2005. Factors influencing the behaviour and welfare of captive lion-tailed macaques in Indian zoos. Applied Animal Behaviour Science 91(3–4):337-353.

Olsson IAS, Westlund K. 2007. More than numbers matter: The effect of social factors on behaviour and welfare of laboratory rodents and non-human primates. Applied Animal Behaviour Science 103(3):229-254.

Weed JL, Wagner PO, Byrum R, Parrish S, Knezevich M, Powell DA. 2003. Treatment of persistent self-injurious behavior in rhesus monkeys through socialization: A preliminary report. Journal of the American Association for Laboratory Animal Science 42(5):21-23.

General Considerations for Social Housing

Bloomsmith MA, Baker KC. 2001. Social management of captive chimpanzees. In: Brent L, editor. The Care and Management of Captive Chimpanzees. San Antonio, TX: American Society of Primatologists. p 205-242.

Bloomsmith MA, Else JG. 2005. Behavioral management of chimpanzees in biomedical research facilities: The state of the science. ILAR Journal 46(2):192-201.

Brent L. 2007. Life-long well being: Applying animal welfare science to nonhuman primates in sanctuaries. Journal of Applied Animal Welfare Science 10(1):55-61.

Buchanan-Smith HM. 1997. Considerations for the housing and handling of New World primates in the laboratory.  In: Reinhardt V, editor. Comfortable Quarters for Laboratory Animals. Washington, DC: Animal Welfare Institute. p 75-84.

Coe CL. 1991. Is social housing of primates always the optimal choice? In: Novak MA, Petto AJ, editors. Through the Looking Glass: Issues of Psychological Well-Being in Captive Nonhuman Primates. Washington, DC: APA. p 69-77.

Crest J, Bloomsmith MA, Jonesteller T. 2015. Effects of changing housing conditions on mangabey behavior (Cercocebus atys): Spacial density, housing quality, and novelty effects. American Journal of Primatology 77(9).

Dolotovskaya S, Walker S, Heymann EW. 2020. What makes a pair bond in a Neotropical primate: female and male contributions. Royal Society Open Science 7(1):191489.

Hannibal DL, Bliss-Moreau E, Vandeleest J, McCowan B, Capitanio J. 2017. Laboratory rhesus macaque social housing and social changes: Implications for research. American Journal of Primatology DOI: 10.1002/ajp.22528.

Hosey GR. 2005. How does the zoo environment affect the behaviour of captive primates? Applied Animal Behaviour Science 90(2):107-129.

Jorgensen MJ, Lamberg KR, Breaux SD, Baker KC, Snively BM, Weed JL. 2015. Pair housing of vervets/African green monkeys for biomedical research. American Journal of Primatology DOI: 10.1002/ajp.22501.

Novak M. 2004. Housing for captive nonhuman primates: the balancing act. In: Institute for Laboratory Animal Research, editors. The Development of Science-Based Guidelines for Laboratory Animal Care: Proceedings of the November 2003 International Workshop. Washington, DC: National Academies Press. p 79-85.

Rennie AE, Buchanan-Smith HM. 2006. Refinement of the use of non-human primates in scientific research. Part II: Housing, husbandry, and acquisition. Animal Welfare 15:215-238.

Reinhardt V, Liss C, Stevens C. 1995. Social housing of previously single-caged macaques: What are the options and the risks. Animal Welfare 4(4):307-328.

Seelig, D. 2007. A tail of two monkeys: social housing for nonhuman primates in the research laboratory setting. Journal of Applied Animal Welfare Science 10(1):21-30.

Truelove MA, Martin AL, Perlman JE, Wood JS, Bloomsmith MA. 2017. Pair housing of macaques: a review of partner selection, introduction techniques, monitoring for compatibility, and methods for long-term maintenance of pairs. American Journal of Primatology DOI: 10.1002/ajp.22485.

Impacts of Social Housing on Development

Andrews MW, Rosenblum LA. 1994. The development of affiliative and agonistic social patterns in differentially reared monkeys. Child Development 65(5):1398-1404.

Bard KA, Gardner KH. 1996. Influences on development in infant chimpanzees: enculturation, temperament, and cognition. In: Russon AE, Bard KA, Parker ST, editors. Reaching into thought: the minds of the great apes. Cambridge: Cambridge University Press. p 235-255.

Bellanca RU, Crockett CM. 2002. Factors predicting increased incidence of abnormal behavior in male pigtailed macaques. Amercian Journal of Primatology 58(2):57-69.

Bloomsmith MA, Baker KC, Ross SR, Lambeth SP. 2006. Early rearing conditions and captive chimpanzee behavior: Some surprising findings. In: Sackett GP, Ruppenthal GC, Elias K, editors. Nursery Rearing of Nonhuman Primates in the 21st Century. New York: Springer. p. 289-312.

Bloomsmith MA, Pazol KA, Alford PL. 1994. Juvenile and adolescent chimpanzee behavioral development in complex groups. Applied Animal Behavior Science 39:73-87.

Chamove AS. 1973. Rearing infant rhesus together. Behaviour 47:48-66.

Chamove AS, Rosenblum LA, Harlow HF. 1973. Monkeys (Macaca mulatta) raised only with peers. A pilot study. Animal Behaviour 21(2):316-325.

Clay AW, Bard KA, Bloomsmith MA. 2018. Effects of sex and early rearing condition on adult behavior, health, and well-being in captive chimpanzees (Pan troglodytes). Behavioural Processes 156:58-76.

Cocks, L. 2007. Factors influencing the well-being and longevity of captive female orangutans. International Journal of Primatology 28(2):429-440.

Conti G, Hansman C, Heckman JJ, Novak MF, Ruggiero A, Suomi SJ. 2012. Primate evidence on the late health effects of early-life adversity. Proceedings of the National Academy of Sciences 109(23):8866-8871.

Crockett CM. 2006. Animal welfare regulations and nursery rearing. In: Sackett GP, Ruppenthal GC, Elias K, editors. Nursery Rearing of Nonhuman Primates in the 21st Century. New York: Springer. p 33-48.

Davenport RK, Rogers CM, Rumbaugh DM. 1973. Long-term cognitive deficits in chimpanzees associated with early impoverished rearing. Developmental Psychology 9(3):343-347.

Goosen C, Schrama A, Brinkhof H, Schonk J, van Hoek LA. 1983. Housing conditions and breeding success of chimpanzees at the primate center TNO. Zoo Biology 2(4):295-302.

Hennessy MB, Kaplan JN, Mendoza SP, Lowe EL, Levine S. 1979. Separation distress and attachment in surrogate-reared squirrel monkeys. Physiology & Behavior 23(6):1017-1023.

Higley JD, Hopkins WD, Thompson WW, Byrne EA, Hirsch RM, Suomi SJ. 1992. Peers as primary attachment sources in yearling rhesus monkeys (Macaca mulatta). Developmental Psychology 28(6):1163-1171.

Horvat JR, Kraemer HC. 1981. Infant socialization and maternal influence in chimpanzees. Folia Primatolgica 36:99-100.

King NE, Mellen JD. 1994. The effects of early experience on adult copulatory behavior in zoo-born chimpanzees (Pan troglodytes). Zoo Biology 13(1):51-59.

Lubach GR, Coe CL, Ershler WB. 1995. Effects of early rearing environment on immune-responses of infant Rhesus monkeys.  Brain, Behavior, and Immunity 9(1):31-46.

Lutz CK, Davis EB, Ruggiero AM, Suomi SJ. 2007. Early predictors of self-biting in socially-housed rhesus macaques (Macaca mulatta). American Journal of Primatology 69(5):584-590.

Maki S, Fritz J, England N. 1993. An assessment of early differential rearing conditions on later behavioral development in captive chimpanzees. Infant Behavioral Development 16:373-381.

Markham RJ. 1990. Breeding orangutans at Perth Zoo: Twenty years of appropriate husbandry. Zoo Biology 9(2):171-182.

Markus N, Croft D. 1995. Play behaviour and its effects on social development of common chimpanzees (Pan troglodytes). Primates 36(2):213-225.

Marriner LM, Drickamer LC. 1994. Factors influencing stereotyped behavior of primates in a zoo. Zoo Biology 13(3):267-275.

Martin JE. 2002. Early life experiences: Activity level and abnormal behaviours in resocialised chimpanzees. Animal Welfare 11(4):419-436.

Mason WA. 1991. Effects of social interaction on well-being: developmental aspects. Laboratory Animal Science 41(4):323-328.

Mineka S, Gunnar M, Champoux M. 1986. Control and early socioemotional development: Infant rhesus monkeys reared in controllable versus uncontrollable environments. Child Development 57(5):1241-1256.

Meder, A. 1989. Effects of hand-rearing on the behavioral development of infant and juvenile gorillas (Gorilla g. gorilla). Developmental Psychobiology 22(4):357-376.

Menzel Jr EW. 1964. Patterns of responsiveness in chimpanzees reared through infancy under conditions of environmental restriction. Psychologische Forschung 27(4):337-365.

Mulholland MM, Williams LE, Abee CR. 2020. Rearing condition may alter neonatal development of captive Bolivian squirrel monkeys (Saimiri boliviensis boliviensis). Developmental Psychobiology 62(7):909-919.

Murrey LE. 1998. The effects of group structure and rearing strategy on personality in chimpanzees (Pan troglodytes) at Chester, London, ZSL and Twycross Zoos. International Zoo Yearbook 36:97-108.

Novak MA & Harlow HF. 1975. Social recovery of monkeys isolated for the first year of life: I. Rehabilitation and therapy. Developmental Psychology 11(4):453-465.

Novak MF, Sackett GP. 1997. Pair-rearing infant monkeys (Macaca nemestrina) using a “rotating- peer” rearing strategy. American Journal of Primatology 41(2):141-149.

Parker KJ, Buckmaster CL, Hyde SA, Schatzberg AF, Lyons DM. 2019. Nonlinear relationship between early life stress exposure and subsequent resilience in monkeys. Scientific Reports 9(1):1-8.

Pazol KA, Bloomsmith MA. 1993. The development of stereotyped body rocking in chimpanzees (Pan troglodytes) reared in a variety of nursery settings. Animal Welfare2:113-129.

Porton I, Niebruegge K. 2006. The Changing Role of Hand Rearing in Zoo-Based Primate Breeding Programs. In: Sackett G, Ruppentahal G, Elias K, editors. Nursery Rearing of Nonhuman Primates in the 21st Century. New York: Springer. p 21-31.

Rommeck I, Gottlieb DH, Strand SC, McCowan B. 2009. The effects of four nursery rearing strategies on infant behavioral development in rhesus macaques (Macaca mulatta). Journal of the American Association for Laboratory Animal Science 48(4):395-401.

Russell JL, Lyn H, Schaeffer JA, Hopkins WD. 2011. The role of socio-communicative rearing environments in the development of social and physical cognition in apes. Developmental Science 14(6):1459-1470.

Ryan S, Thompson SD, Roth AM, Gold KC. 2002. Effects of hand-rearing on the reproductive success of western lowland gorillas in North America. Zoo Biology 21(4):389-401.

Sackett GP. 1965. Effects of rearing conditions upon the behavior of rhesus monkeys (Macaca mulatta). Child Development 36(4):855-868.

Sackett GP, Ruppenthal GC, Davis AE. 2002. Survival, growth, health , and reproduction following nursery rearing compared with mother rearing in pigtailed monkeys (Macaca nemestrina). American Journal of Primatology 56(3):165-183.

Sackett GP, Ruppenthal G, Elias K. eds. 2006.  Nursery Rearing of Nonhuman Primates in the 21st Century. New York: Springer.

Stevens HE, Leckman JF, Coplan JD, Suomi SJ. 2009. Risk and resilience: early manipulation of macaque social experience and persistent behavioral and neurophysiological outcomes. Journal of the American Academy of Child & Adolescent Psychiatry 48(2):114-127.

Suomi SJ, Harlow HF, Novak MA. 1974. Reversal of social deficits produced by isolation rearing in monkeys. Journal of Human Evolution 3(6):527-528.

Walsh S, Bramblett CA, Alford PL. 1982. A vocabulary of abnormal behaviors in restrictively reared chimpanzees. American Journal of Primatology 3:315-319.

Worlein JM, Sackett G P. 1997. Social development in nursery-reared pigtailed macaques (Macaca nemestrina).  American Journal of Primatology 41(1):23-35.

Introduction Strategies

Alford PL, Bloomsmith MA, Keeling ME, Beck TF. 1995. Wounding aggression during the formation and maintenance of captive, multimale chimpanzee groups. Zoo Biology 14(4):347-359.

Bailey KL, Young LA, Long CE, Remillard CM, Moss SE, Meeker TL, Bloomsmith MA. 2021. Use of introduction enclosures to integrate multimale cohorts into groups of female rhesus macaques (Macaca mulatta). Journal of the American Association for Laboratory Animal Science60(1):103–111(9).

Bernstein I. 1969. Introductory techniques in the formation of pigtail monkey troops. Folia Primatologica 10(1-2):1-19.

Bernstein IS. 1971. The influence of introductory techniques on the formation of captive mangabey groups. Primates 12(1):33-44.

Bloomsmith MA, Baker KC, Ross SK, Lambeth SP. 1999. Chimpanzee behavior during the process of social introductions. In: American Zoo and Aquarium Association (AZA) Annual Conference Proceedings , p 270-273.

Brent L, Kessel AL, Barrera H. 1997. Evaluation of introduction procedures in captive chimpanzees. Zoo Biology,16(4):335-342.

Capitanio JP, Blozis SA, Snarr J, Steward A, McCowan BJ. 2017. Do “birds of a feather flock together” or do “opposites attract”? Behavioral responses and temperament predict success in pairings of rhesus monkeys in a laboratory setting. American Journal of Primatology 79(1).

DiVincenti Jr L, Rehrig A, Wyatt J. 2012. Interspecies pair housing of macaques in a research facility. Laboratory Animals 46(2):170-172.

Ekanayake-Alper DK, Wilson SR, Scholz JA. 2018. Retrospective review of surgical outcomes and pair-housing success in vasectomized rhesus macaques (Macaca mulatta). Comparative Medicine 68(2):168-176.

Fragaszy D, Baer J, Adams-Curtis L. 1994. Introduction and integration of strangers into captive groups of tufted capuchins (Cebus apella). International Journal of Primatology 15(3):399-420.

Fritz J, Howell S. 2001. Captive chimpanzee social group formation. In: Brent L, editor. The Care and Management of Captive Chimpanzees. San Antonio, TX: American Society of Primatologists.

Lynch R. 1998. Successful pair-housing of male macaques (Macaca fascicularis). Laboratory Primate Newsletter 37:4-5.

MacAllister RP, Heagerty A, Coleman K. 2020. Behavioral predictors of pairing success in rhesus macaques (Macaca mulatta). American Journal of Primatology 82(1):p.e23081.

Majolo B, Buchanan-Smith HM, Morris K. 2003. Factors affecting the successful pairing of unfamiliar common marmoset (Callithrix jacchus) females: Preliminary results. Animal Welfare 12:327-337.

Pomerantz O, Baker KC. 2017. Higher levels of submissive behaviors at the onset of the pairing process of rhesus macaques (Macaca mulatta) are associated with lower risk of wounding following introduction. American Journal of Primatology 79(8).

Reinhardt V. 1994. Continuous pair-housing of caged Macaca mulatta: Risk evaluation. Laboratory Primate Newsletter 33(1):1-4.

Reinhardt V. 1994. Pair-housing rather than single-housing for laboratory rhesus macaques. Journal of Medical Primatology 23(8):426-431.

Rox A, van Vliet AH, Sterck EH, Langermans JA, Louwerse AL. 2019. Factors determining male introduction success and long-term stability in captive rhesus macaques. PLOS ONE 14(7):p.e0219972.

Vermeer J. 1997. The formation of a captive squirrel monkey group. International Zoo News 146-149.

Watson LM. 2002. A successful program for same-and cross-age pair-housing adult and subadult male Macaca fascicularis. Laboratory Primate Newsletter 41(2):6-9.

Williams LE, Abee CR. 1988. Aggression with mixed age-sex groups of Bolivian squirrel monkeys following single animal introductions and new group formations. Zoo Biology 7(2):139-145.

Williams LE, Coke CS, Weed JL. 2017. Socialization of adult owl monkeys (Aotus sp.) in Captivity. American Journal of Primatology 79(1).

Wojciechowski S. 2004. Introducing a fourth primate species to an established mixed-species exhibit of African monkeys. Zoo Biology 23(2):95-108.

Worlein JM, Kroeker R, Lee GH, Thom JP, Bellanca RU, Crockett CM. 2017. Socialization in pigtailed macaques (Macaca nemestrina). American Journal of Primatology 79(1).

Alternative Indoor Caging Social Housing Options

Baker KC, Bloomsmith MA, Oettinger B, Neu K, Griffis C, Schoof VAM. 2014. Comparing options for pair housing rhesus macaques using behavioral welfare measures. American Journal of Primatology 76:30-42.

Baker, KC Crockett, CM, Lee GH, Oettingerb BC, Schoof V, Thom JP. 2012. Pair housing for female longtailed and rhesus macaques in the laboratory: Behavior in protected contact versus full contact. Journal of Applied Animal Welfare Science 15:126-143.

Bayne K. 1991. Alternatives to continuous social housing. Laboratory Animal Science 41(4):355-359.

Cassidy LC, Hannibal DL, Semple S, McCowan B. 2020. Improved behavioral indices of welfare in continuous compared to intermittent pair‐housing in adult female rhesus macaques (Macaca mulatta). American Journal of Primatology 82(10):e23189.

Crockett CM, Bellanca RU, Bowers CL, Bowden DM. 1997. Grooming-contact bars provide social contact for individually-caged laboratory macaques. Contemporary Topics in Laboratory Animal Science 36:53-60.

Hannibal DL, Cassidy LC, Vandeleest J, Semple S, Barnard A, Chun K, Winkler S, McCowan B. 2018. Intermittent pair‐housing, pair relationship qualities, and HPA activity in adult female rhesus macaques. American Journal of Primatology 80(5):e22762.

Lee GH, Thom JP, Chu KL, Crockett CM. 2012. Comparing the relative benefits of grooming contact and full-contact pairing for laboratory-housed adult female Macaca fascicularis. Applied Animal Behaviour Science 137:157-165.

Watson LM. 2010. Effectiveness of perforated plexiglass dividers as social grooming devices between neighboring, individually housed adult male Macaca fascicularis. Laboratory Primate Newsletter 49(4):1-5.

Group Composition and Maintenance in Captivity

Augustsson A, Hau J. 1999. A simple ethological monitoring system to assess social stress in group-housed laboratory rhesus macaques. Journal of Medical Primatology 28:84-90.

Anzenberger G, Falk B. 2012. Monogamy and family life in callitrichid monkeys: deviations, social dynamics and captive management. International Zoo Yearbook 46(1):109-122.

Baker KC, Seres M, Aureli F, DeWaal FBM. 2000. Injury risks among chimpanzees in three housing conditions. American Journal of Primatology 51:151-175.

Beisner BA, Jackson ME, Cameron A, McCowan B. 2012. Sex ratio, conflict dynamics, and wounding in rhesus macaques (Macaca mulatta). Applied Animal Behaviour Science 137:137-147.

Beisner BA, Wooddell LJ, Hannibal DL, Nathman A, McCowan B. 2019. High rates of aggression do not predict rates of trauma in captive groups of macaques. Applied Animal Behaviour 212:82-89.

Bloomstrand A, Maple T. 1987. Management and husbandry of African monkeys in captivity. In: Zucker EL, editor. Comparative behavior of African monkeys. New York: Alan R. Liss, Inc. p 197-234.

Coleman K. 2012. Individual differences in temperament and behavioral management practices for nonhuman primates. Applied Animal Behavior Science 137(3):106-113.

Duarte RB, Maior RS, Barros M. 2018. Behavioral and cortisol responses of adult marmoset monkeys (Callithrix penicillata) to different home-cage social disruption intervals. Applied Animal Behaviour Science 201:117-124.

Fitch AL, Merhalski JJ, Bloomsmith MA. 1989. Social housing for captive adult male chimpanzees: Comparing single-male and multi-male social groups.  American Journal of Primatology Supplement 1:87-91.

Gartland K, McDonald M, Braccini Slade S, White F, Sanz C. 2018. Behavioral changes following alterations in the composition of a captive bachelor group of western lowland gorillas (Gorilla gorilla gorilla). Zoo Biology 37(6):391-398.

Leonardi R, Buchanan-Smith HM, Dufour V, MacDonald C, Whiten A. 2010. Living together: behavior and welfare in single and mixed species groups of capuchin (Cebus apella) and squirrel monkeys (Saimiri sciureus). American Journal of Primatology 72:33-47.

Macedonia JM. 1987. Effects of housing differences upon activity budgets in captive sifakas (Propithecus verreauxi). Zoo Biology 6(1):55-67.

McCowan B, Beisner BA, Capitanio JP, Jackson ME, Cameron AN, Seil S, Atwill ER, Fushing H. 2011. Network stability is a balancing act of personality, power, and conflict dynamics in rhesus macaque societies. PloS One 6(8):e22350.

McCowan B, Beisner B, Hannibal D. 2018. Social management of laboratory rhesus macaques housed in large groups using a network approach: A review. Behavioral Processes 156:77-82.

Oates-O’Brien RS, Farver TB, Anderson-Vicino KC, McCowan B, Lerche NW. 2010. Predictors of matrilineal overthrows in large captive breeding groups of rhesus macaques (Macaca mulatta). Journal of the American Association of Laboratory Animal Science 49:196-201.

Pinheiro T, Lopes MA. 2018. Hierarchical structure and the influence of individual attributes in the captive squirrel monkey (Saimiri collinsi). Primates 59(5):475-482.

Price EE, Stoinski TS. 2007. Group size: Determinants in the wild and implications for the captive housing of wild mammals in zoos.  Applied Animal Behaviour Science 103(3):255-264.

Reinhardt V, Dan Houser W, Eisele SG, Champoux M. 1987. Social enrichment of the environment with infants for singly caged adult rhesus monkeys. Zoo Biology 6(4):365-371.

Ross SR, Bloomsmith MA, Bettinger TL, Wagner KE. 2009. The influence of captive adolescent male chimpanzees on wounding: Management and welfare implications. Zoo Biology 28:623-634.

Wiley JN, Leeds A, Carpenter KD, Kendall CJ. 2018. Patterns of wounding in hamadryas baboons (Papio hamadryas) in North American zoos. Zoo Biology 37(2):74-79.

Social Housing and Positive Reinforcement Training

Desmond T, Laule G, McNary J. 1987. Training to enhance socialization and reproduction in drills. In: Proceedings of the American Association of Zoological Parks and Aquariums [AAZPA] Western Regional Conference. Wheeling, WV. p 435-441.

Pomerantz O, Terkel J. 2009. Effects of positive reinforcement training techniques on the psychological welfare of zoo-housed chimpanzees (Pan troglodytes). American Journal of Primatology 71(8):687-695.

Schapiro SJ, Perlman JE, Boudreau BA. 2001. Manipulating the affiliative interactions of group-housed rhesus macaques using positive reinforcement training techniques. American Journal of Primatology 55:137–149.

Schapiro SJ, Bloomsmith MA, Laule GE. 2003. Positive reinforcement training as a technique to alter nonhuman primate behavior: quantitative assessments of effectiveness. Journal of Applied Animal Welfare Science 6(3):175-187.

Veeder CL, Bloomsmith MA, McMillan JL, Perlman JE, Martin AL. 2009. Positive reinforcement training to enhance the voluntary movement of group-housed sooty mangabeys (Cercocebus atys atys).  Journal of the American Association of Laboratory Animal Science 48(2):192-195.

Social Housing and Impacts on Immunity, Physiology, and Disease

Armstrong DM, Santymire RM. 2013. Hormonal and behavioral variation in pied tamarins housed in different management conditions. Zoo Biology 32(3):299-306.

Balasubramaniam KN, Beisner BA, Hubbard JA, Vandeleest JJ, Atwill ER, McCowan B. 2019.

Affiliation and disease risk: social networks mediate gut microbial transmission among rhesus macaques. Animal Behaviour 151:131-143.

Benton CG, West MW, Hall SM, Marko ST, Johnson JC. 2013. Effect of short-term pair housing of juvenile rhesus macaques (Macaca mulatta) on immunologic parameters. Journal of the American Association for Laboratory Animal Science 52:240-246.

Capitanio JP. 1998. Social experience and immune system measures in laboratory-housed macaques: Implications for management and research. ILAR Journal 39(1):12-20.

Coe CL. 1993. Psychosocial factors and immunity in nonhuman primates: a review. Psychosomatic Medicine 55(3):298-308.

Coelho AM, Carey KD, Shade RE. 1991. Assessing the effects of social environment on blood pressure and heart rates of baboons. American journal of primatology 23(4):257-267.

Mendoza SP. 1991. Sociophysiology of well-being in nonhuman primates. Laboratory Animal Science 41(4):344-349.

Pahar B, Baker KC, Jay AN, Russell-Lodrigue KE, Srivastav SK, Aye PP, Blanchard JL, Bohm RP. 2020. Effects of social housing changes on immunity and vaccine-specific immune responses in adolescent male rhesus macaques. Frontiers in Immunology, 11, 565746.

Schapiro SJ. 2002. Effects of social manipulations and environmental enrichment on behavior and cell-mediated immune responses in rhesus macaques. Pharmacology, Biochemistry and Behavior 73:271–278.

Schapiro SJ, Bernacky BJ. 2012. Socialization strategies and disease transmission in captive colonies of nonhuman primates. American Journal of Primatology 74:518-527.

Smith AS, Birnie AK, French JA. 2011. Social isolation affects partner-directed social behavior and cortisol during pair formation in marmosets, Callithrix geoffroyi. Physiology & Behavior 104(5):955-961.

Other Social Housing Resources

Carlson J. 2008. Safe pair housing of macaques. Animal Welfare Institute, Washington, D.C.

Social Housing of Laboratory Animals Selected Citations (2014). Retrieved 3 March 2021, from http://enrichmentrecord.com/wp-content/uploads/2014/03/Social-Housing-Laboratory-Animals.pdf