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Environmental Enrichment For Nonhuman Primates Resource Guide: Social Housing

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Abney, D.M. and J.L. Weed (2006). Methods for successfully pair housing adult male rhesus macaques (Macaca mulatta). American Journal of Primatology 68(Suppl. 1): 59. DOI: 10.1002/ajp.20270

Alexander, S. and M. Fontenot (2003). Isosexual social group formation for environmental enrichment in adult male Macaca mulatta. Contemporary Topics in Laboratory Animal Science 42(4): 122.

Anonymous (2009). Social housing of nonhuman primates with cranial implants: a discussion. Laboratory Primate Newsletter 48(2): 1-2.
Online: https://www.brown.edu/Research/Primate/LPN48-2.html#implants

Augustsson, H. and J. Hau (1999). A simple ethological monitoring system to assess social stress in group-housed laboratory rhesus macaques. Journal of Medical Primatology 28(2): 84-90. 

Baker, K.C., M. Bloomsmith, K. Neu, C. Griffis, B. Oettinger, V. Schoof, A. Clay, and M. Maloney (2008). Benefits of isosexual pairing of rhesus macaques (Macaca mulatta) vary with sex and are limited by protected contact but not by frequent separation. American Journal of Primatology 70(Suppl. 1): 44. DOI: 10.1002/ajp.20556

Baker, K.C., M.A. Bloomsmith, B. Oettinger, K. Neu, C. Griffis, and V.A. Schoof (2014). Comparing options for pair housing rhesus macaques using behavioral welfare measures. American Journal of Primatology 76(1): 30-42. DOI: https://doi.org/10.1002/ajp.22190

Baker, K.C., C.M. Crockett, G.H. Lee, B.C. Oettinger, V. Schoof, and J.P. Thom (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(2): 126-143. DOI: https://doi.org/10.1080/10888705.2012.658330

Baker, K.C., E. Seres, F. Aureli, and F.B. De Waal (2000). Injury risks among chimpanzees in three housing conditions. American Journal of Primatology 51(3): 161-175.

Baker, K.C., M.A. Bloomsmith, B. Oettinger, K. Neu, C. Griffis, V. Schoof, and M. Maloney (2012). Benefits of pair housing are consistent across a diverse population of rhesus macaques. Applied Animal Behaviour Science 137(3-4): 148-156. DOI: 10.1016/j.applanim.2011.09.010

Beisner, B. A., Wooddell, L. J., Hannibal, D. L., Nathman, A., & McCowan, B. (2019). High rates of aggression do not predict rates of trauma in captive groups of macaques. Applied Animal Behaviour Science, 212, 82–89. DOI: https://doi.org/10.1016/j.applanim.2019.01.003

Benton, C.G., M.W. West, S.M. Hall, S.T. Marko, and J.C. Johnson (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(3): 240-246. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3690444/

Bloomsmith, M. A., Clay, A. W., Lambeth, S. P., Lutz, C. K., Breaux, S. D., Lammey, M. L., Franklin, A. N., Neu, K. A., Perlman, J. E., Reamer, L. A., Mareno, M. C., Schapiro, S. J., Vazquez, M., & Bourgeois, S. R. (2019). Survey of Behavioral Indices of Welfare in Research Chimpanzees ( Pan troglodytes ) in the United States. Journal of the American Association for Laboratory Animal Science : JAALAS, 58(2), 160–177. MEDLINE. DOI: https://doi.org/10.30802/AALAS-JAALAS-18-000034

Bloomsmith, M., K. Baker, C. Griffis, B. Oettinger, V. Schoof, A. Clay, and M. Maloney (2008). Behavioral benefits of pair housing in adult rhesus macaques (Macaca mulatta) do not depend on age, previous duration of single housing, or naturalistic rearing. American Journal of Primatology 70(Suppl. 1): 44. DOI: 10.1002/ajp.20556

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:e22464. DOI: 10.1002/ajp.22464.

Cassidy, L. C., Hannibal, D. L., 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). Scopus. DOI: https://doi.org/10.1002/ajp.23189

Claxton, A.M. (2011). The potential of the human-animal relationship as an environmental enrichment for the welfare of zoo-housed animals. Applied Animal Behaviour Science 133(1-2): 1-10. DOI: 10.1016/j.applanim.2011.03.002

De Filippis, B., F. Chiarotti, and A. Vitale (2009). Severe intragroup aggressions in captive common marmosets (Callithrix jacchus). Journal of Applied Animal Welfare Science 12(3): 214-222. 

Díaz, S., Sánchez, S., & Fidalgo, A. (2020). Coping Style and Early Life Vocalizations in the Common Marmoset (Callithrix jacchus). International Journal of Primatology, 41(3), 497–510. Scopus. DOI: https://doi.org/10.1007/s10764-020-00153-8

Dinklo, T., Garces, P., Chatham, C., Pouliot, M., & Authier, S. (2019). Non-human primate neuropharmacology refinement: Polysomnography and regional qEEG with social housing in ETS 123 compliant cages. Journal of Pharmacological and Toxicological Methods, 99. DOI: https://doi.org/10.1016/j.vascn.2019.05.069

DiVincenti Jr, L. and J.D. Wyatt (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.

DiVincenti, L., A. Rehrig, and J. Wyatt (2012). Interspecies pair housing of macaques in a research facility. Laboratory Animals: 1-3. 

Doyle, L.A., K.C. Baker, and L.D. Cox (2008). Physiological and behavioral effects of social introduction on adult male rhesus macaques. American Journal of Primatology 70(6): 542-550. DOI: 10.1002/ajp.20526

Egeler, J., S. Hoekwater, and H. Hoffman (2010). A novel approach for utilizing large group-housing style cages for nonhuman primates in toxicology studies. Journal of the American Association for Laboratory Animal Science 49(5): 716.

Farmer, H.L., A.B. Plowman, and L.A. Leaver (2011-). Role of vocalisations and social housing in breeding in captive howler monkeys (Alouatta caraya). Applied Animal Behaviour Science 134(3-4): 177-183. DOI: 10.1016/j.applanim.2011.07.005

Franz, C., S. Macherhammer, E. Kalcher, K. Crailsheim, and S. Preuschoft (2003). The influence of housing conditions on the performance of aberrant behaviours in former laboratory chimpanzees (Pan troglodytes): Association with social interactions. Folia Primatologica 74(4): 194.

Gaspari, F., G. Perretta, and G. Schino (2000). Effects of different housing systems on the behaviour of the common marmoset (Callithrix jacchus). Folia Primatologica 71(4): 291.

Gilbert, M.H. and K.C. Baker (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. DOI: 10.1111/j.1600-0684.2010.00447.x

Ha, J.C., R.L. Robinette, and G.P. Sackett (1999). Social housing and pregnancy outcome in captive pigtailed macaques. American Journal of Primatology 47(2): 153-163. 

Hannibal, D. L., Nathman, A. C., Beisner, B. A., Lin, N. S., & McCowan, B. (2019). INCREASED PRODUCE ENRICHMENT REDUCES TRAUMA IN SOCIALLY-HOUSED CAPTIVE RHESUS MACAQUES (Macaca mulatta). American Journal of Primatology, 81. DOI: https://dx.doi.org/10.1002%2Fajp.23073

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 79:e22528. DOI: 10.1002/ajp.22528.

Hartner, M., J. Hall, J. Penderghest, and L.P. Clark (2001). Group housing subadult male cynomolgus macaques in a pharmaceutical environment. Lab Animal 30(8): 53-57. 

Heagerty, A., Johnson, C., & Coleman, K. (2019). USE OF REGRESSION TREE MODELING TO PREDICT PAIR SUCCESS IN RHESUS MACAQUES (Macaca mulatta). American Journal of Primatology, 81. 

Hotchkiss, C.E. and M.G. Paule (2003). Effect of pair-housing on operant behavior task performance by rhesus monkeys. Contemporary Topics in Laboratory Animal Science 42(4): 38-41.

Janavaris, M., Bader, L., Coleman, K., & Kievit, P. (2020). Bedding as an enrichment strategy in group-housed Mauritian cynomolgus macaques (Macaca fascicularis). American Journal of Primatology, 82. DOI: https://doi.org/:/WOS:000519103100122

Jennings, M. and M. Prescott (2009). Refinements in husbandry, care and common procedures for non-human primates: Ninth report of the BVAAWF/FRAME/RSPCA/UFAW Joint Working Group on Refinement. Laboratory Animals 43(Suppl. 1): S1:1-S1:47. DOI: 10.1258/la.2008.007143

Jorgensen, MJ, Lambert, KR, Breaux, SD, Baker, KC, Snively, BM, Weed, JL. (2017). Pair housing of Vervets/African Green Monkeys for biomedical research. American Journal of Primatology 79:e22501. DOI: 10.1002/ajp.22501.

Kaiser, R.A., S.D. Tichenor, D.E. Regalia, K. York, and H.H. Holzgrefe (2015). Telemetric assessment of social and single housing: Evaluation of electrocardiographic intervals in jacketed cynomolgus monkeys. Journal of Pharmacological and Toxicological Methods. In press.
DOI: 10.1016/j.vascn.2015.05.001

Kutsukake, N., Teramoto, M., Honma, S., Mori, Y., Ikeda, K., Yamamoto, R., Ishida, T., & Hasegawa, T. (2019). Behavioural and hormonal changes during group formation by male chimpanzees. Behaviour, 156(2), 109–129. Environment Complete.

Lee, G.H., J.P. Thom, K.L. Chu, and C.M. Crockett (2012). Comparing the relative benefits of grooming-contact and full-contact pairing for laboratory-housed adult female Macaca fascicularis. Applied Animal Behaviour Science 137(3-4): 157-165. 
DOI: 10.1016/j.applanim.2011.08.013

Leonardi, R., H.M. Buchanan-Smith, V. Dufour, C. MacDonald, and A. Whiten (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(1): 33-47. DOI: https://doi.org/10.1002/ajp.20748

Majolo, B., H.M. Buchanan Smith, and K. Morris (2003). Factors affecting the successful pairing of unfamiliar common marmoset (Callithrix jacchus) females: Preliminary results. Animal Welfare 12(3): 327-337.

Marks, D., J. Kelly, T. Rice, S. Ames, R. Marr, J. Westfall, J. Lloyd, and C. Torres (2000). Utilizing restraint chair training to prepare primates for social housing. Laboratory Primate Newsletter 39(4): 9. https://www.brown.edu/Research/Primate/lpn39-4.html#chair

McCowan, B. and I. Rommeck (2006). Bioacoustic monitoring of aggression in group-housed rhesus macaques. Journal of Applied Animal Welfare Science 9(4): 261-268. DOI: http://www.tandfonline.com/doi/abs/10.1207/s15327604jaws0904_1

Medical Research Council (MRC) (n.d). Primates in medical research. London: Medical Research Council & Wellcome Trust. https://mrc.ukri.org/publications/browse/primates-in-medical-research/

Meguerditchian, A., Marie, D., Margiotoudi, K., Roth, M., Nazarian, B., Anton, J.-L., & Claidière, N. (2021). Baboons (Papio anubis) living in larger social groups have bigger brains. Evolution and Human Behavior, 42(1), 30–34. Scopus. DOI: https://doi.org/10.1016/j.evolhumbehav.2020.06.010

Morgan, D., K.A. Grant, O.A. Prioleau, S.H. Nader, J.R. Kaplan, and M.A. Nader (2000). Predictors of social status in cynomolgus monkeys (Macaca fascicularis) after group formation. American Journal of Primatology 52(3): 115-131. 

Neal Webb, S. J., Hau, J., & Schapiro, S. J. (2019). Does group size matter? Captive chimpanzee (Pan troglodytes) behavior as a function of group size and composition. American Journal of Primatology, 81(1), e22947. MEDLINE. DOI: https://doi.org/10.1002/ajp.22947

Niehoff, M., Bartko, T., Kremer, J., & Nichols, J. (2020). Evaluation of PhysioTel (TM) digital M11 cardiovascular telemetry implant in socially housed cynomolgus monkeys using etilefrine and moxifloxacin. Journal of Pharmacological and Toxicological Methods, 105. DOI: https://doi.org/10.1016/j.vascn.2020.106761

Niehoff, M.O., M. Bergmann, and G.F. Weinbauer (2010). Effects of social housing of sexually mature male cynomolgus monkeys during general and reproductive toxicity evaluation. Reproductive Toxicology 29(1): 57-67. DOI: 10.1016/j.reprotox.2009.09.007

Novak, M. A. (2020). Self-Injurious behavior in rhesus macaques: Issues and challenges. American Journal of Primatology. Scopus. DOI: https://doi.org/10.1002/ajp.23222

Novak, M.A., A.F. Hamel, B.J. Kelly, A.M. Dettmer, and J.S. Meyer (2012). Stress, the HPA axis, and nonhuman primate well-being: A review. Applied Animal Behaviour Science In Press. DOI: 10.1016/j.applanim.2012.10.012

Olsson, I.A.S. and K. Westlund (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(3-4): 229-254. DOI: 10.1016/j.applanim.2006.05.022(link is external)

Ottesen, J.L., A. Weber, H. Gurtler, and L.F. Mikkelsen (2004). New housing conditions: improving the welfare of experimental animals. Alternatives to Laboratory Animals 32(Suppl. 1B): 397-404.

Pahar, B., Baker, K. C., Jay, A. N., Russell-Lodrigue, K. E., Srivastav, S. K., Aye, P. P., Blanchard, J. L., & Bohm, R. P. (2020). Effects of Social Housing Changes on Immunity and Vaccine-Specific Immune Responses in Adolescent Male Rhesus Macaques. Frontiers in Immunology, 11. Scopus. https://doi.org/10.3389/fimmu.2020.565746

Prescott, M. J., Clark, C., Dowling, W. E., & Shurtleff, A. C. (2021). Opportunities for refinement of non-human primate vaccine studies. Vaccines, 9(3). Scopus. DOI: https://doi.org/10.3390/vaccines9030284

Reinhardt, V. (1999). Pair-housing overcomes self-biting behavior in macaques. Laboratory Primate Newsletter 38(1): 4-5. http://www.brown.edu/Research/Primate/lpn38-1.html

Reinhardt, V. (2005). Implementing housing refinements in a rhesus macaque colony. Contemporary Topics in Laboratory Animal Science 44(3): 76,78,80. 

Reinhardt, V. (2008). Taking Better Care of Monkeys and Apes: Refinement of Housing and Handling Practices for Caged Nonhuman Primates. Animal Welfare Institute: Washington, DC, 137 p. https://awionline.org/store/catalog/animal-welfare-publications/animals-...

Reinhardt, V. and A. Reinhardt (2000). Social enhancement for adult nonhuman primates in research laboratories: A review. Lab Animal 29(1): 34-41.

Reinhardt, V. and A. Reinhardt (2008). Environmental Enrichment and Refinement for Nonhuman Primates Kept in Research Laboratories: A Photographic Documentation and Literature Review, 3rd edition, Animal Welfare Institute: Washington, DC, 129 p. http://awionline.org/sites/default/files/uploads/legacy-uploads/documents/08-EnvironmentalEnrichmentFull.pdf

Rennie, A. and H. Buchanan Smith (2006). Refinement of the use of non-human primates in scientific research. II. Housing, husbandry and acquisition. Animal Welfare 15(3): 215-238. 

Roberts, S.J. and M.L. Platt (2005). Effects of isosexual pair-housing on biomedical implants and study participation in male macaques. Contemporary Topics in Laboratory Animal Science 44(5): 13-18.

Roder, E.L. and P.J.A. Timmermans (2002). Housing and care of monkeys and apes in laboratories: Adaptations allowing essential species-specific behaviour. Laboratory Animals 36(3): 221-242. DOI: https://dx.doi.org/10.1258/002367702320162360

Rox, A., van Vliet, A. H., Langermans, J. A. M., Sterck, E. H. M., & Louwerse, A. L. (2021). A Stepwise Male Introduction Procedure to Prevent Inbreeding in Naturalistic Macaque Breeding Groups. Animals, 11(2). DOI: https://doi.org/10.3390/ani11020545

Schapiro, S.J. (2000). A few new developments in primate housing and husbandry. Scandinavian Journal of Laboratory Animal Science 27(2): 103-110.

Schapiro, S.J. (2002). Effects of social manipulations and environmental enrichment on behavior and cell mediated immune responses in rhesus macaques. Pharmacology Biochemistry and Behavior 73(1): 271-278.

Schapiro, S.J., J.E. Perlman, and B.A. Boudreau (2001). Manipulating the affiliative interactions of group-housed rhesus macaques using positive reinforcement training techniques. American Journal of Primatology 55(3): 137-149.

Schapiro, S.J. and B.J. Bernacky (2011). Socialization strategies and disease transmission in captive colonies of nonhuman primates. American Journal of Primatology DOI: 10.1002/ajp.21001

Schrock, A. E., Leard, C., Lutz, M. C., Meyer, J. S., & Gazes, R. P. (2019). Aggression and social support predict long-term cortisol levels in captive tufted capuchin monkeys (Cebus Sapajus apella). American Journal of Primatology, 81(7), e23001–e23001.

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. 

Seier, J., C. de Villiers, J. van Heerden, and R. Laubscher (2011). The effect of housing and environmental enrichment on stereotyped behavior of adult vervet monkeys (Chlorocebus aethiops). Lab Animal 40(7): 218-224. DOI: 10.1038/laban0711-218

Seier, J.V., J. Loza, and L. Benjamin (2004). Housing and stereotyped behaviour: Some observations from an indoor colony of vervet monkeys (Chlorocebus aethiops). Folia Primatologica 75(Suppl. 1): 332.

Singh, P., El Amrani, A. I., Loriot, S., El Amrani-Callens, F., Duclos, M. E., & Forster, R. (2019). Comparison of single, paired and group housing effects on cardiovascular parameters and body temperature in telemetered cynomolgus monkeys. Toxicology Letters, 314, S257–S257.

Spratley, M. and K. Cork (2009). Continuous group housing standard for general toxicology studies as a form of environmental enrichment. Journal of the American Association for Laboratory Animal Science 48(5): 600.

Sterck, E. H. M., Zijlmans, D. G. M., de Vries, H., van den Berg, L. M., van Schaik, C. P., & Langermans, J. A. M. (2019). Determining overweight and underweight with a new weight-for-height index in captive group-housed macaques. American Journal of Primatology, 81(6), e22996. MEDLINE. DOI: https://doi.org/10.1002/ajp.22996

Stoinski, T.S., N. Czekala, K.E. Lukas, and T.L. Maple (2002). Urinary androgen and corticoid levels in captive, male Western lowland gorillas (Gorilla g. gorilla): Age and social group related differences. American Journal of Primatology 56(2): 73-87. 

Stow, R., Kendrick, J., Ibbotson, N., Adjin-tettey, G., Murphy, B., Trojca, R., Miller, J., Konradsen, G., Øvlisen, K., Helleberg, H., & Hansen, J. J. (2021). A new group housing approach for non-human primate metabolism studies. Journal of Pharmacological and Toxicological Methods, 107. Scopus. DOI: https://doi.org/10.1016/j.vascn.2020.106947

Tardif, S.D., D.A. Smucny, D.H. Abbott, K. Mansfield, N. Schultz Darken, and M.E. Yamamoto (2003). Reproduction in captive common marmosets (Callithrix jacchus). Comparative Medicine 53(4): 364-368.

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 79:e22485. DOI: 10.1002/ajp.22485.

Watson, L. (2003). Pair- and singly-housed adult male M. fascicularis' behavioral response to varying video tape subject matter. American Journal of Primatology 60 (Suppl. 1): 83.

Watson, L. (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. https://www.brown.edu/Research/Primate/LPN49-4.html#watson

Weed, J.L., K.J. McCollom, and F.A. Cisar (2000). Methods for socializing unfamiliar primates to provide environmental enrichment and promote psychological well-being. American Journal of Primatology 51(Suppl. 1): 98. 

Weed, J.L., P.O. Wagner, R. Byrum, S. Parrish, M. Knezevich, and D.A. Powell (2003). Treatment of persistent self-injurious behavior in rhesus monkeys through socialization: A preliminary report. Contemporary Topics in Laboratory Animal Science 42(5): 21-23. 

West, A.M., M. Carey, W. Wagner, and J. Erwin (2013). Full-contact social housing of non-human primates (Macaca mulatta and Macaca fascicularis) in a biomedical research facility: Initiation and Implementation. American Journal of Primatology 75(Suppl. 1: Program and Abstracts of the 36th Annual Meeting of the American Society of Primatologists June 19–22, 2013): 1-106. DOI: 10.1002/ajp.22188

Westergaard, G.C., M.K. Izard, J.H. Drake, S.J. Suomi, and J.D. Higley (1999). Rhesus macaque (Macaca mulatta) group formation and housing: wounding and reproduction in a specific pathogen free (SPF) colony. American Journal of Primatology 49(4): 339-347.

Whittaker, M. Managing Monkey Behavior: Advancing the Social Management of Old World Monkeys. Active Environments, Inc.  https://www.academia.edu/34493637/Managing_Monkey_Behavior_Advancing_the...

Williams, LE, Coke, C, Weed, J. Socialization of adult owl monkeys (Aotus sp.) in Captivity. (2017). American Journal of Primatology 79:e22521. DOI:10.1002/ajp.22521.

Williams, L.E., A. Steadman, and B. Kyser (2000). Increased cage size affects Aotus time budgets and partner distances. American Journal of Primatology 51(Suppl. 1): 98. 

Wolfensohn, S. (2004). Social housing of large primates: Methodology for refinement of husbandry and management. Alternatives to Laboratory Animals 32(Suppl. 1A): 149-151. 

Worlein, JM, Kroeker, R, Lee, GH, Thom, JP, Bellanca, RU, Crockett, CM. (2017). Socialization in pigtailed macaques (Macaca nemestrina). American Journal of Primatology 79:e22556. DOI:10.1002/ajp.22556.

Yamanashi, Y., Nemoto, K., & Alejandro, J. (2021). Social relationships among captive male pygmy slow lorises (Nycticebus pygmaeus): Is forming male same-sex pairs a feasible management strategy? American Journal of Primatology, 83(2), e23233. DOI: https://doi.org/10.1002/ajp.23233