Laboratory macaques: When to wean?

Applied Animal Behaviour Science

Volumn 138, Issue 1-2, 2012, Pages 194-207

  Prescott, Mark J ^a   Nixon, Mellissa E ^b   Farningham, David A H ^b   Naiken, Sandiren ^c   Griffiths, Mary Ann ^c  

^a National Centre for the Replacement   (United Kingdom)

^b Centre for Macaques   (United Kingdom)

^c Bioculture (Mauritius) Group Senneville   (Mauritius)

Author keywords

Animal welfare; Behaviour; Colony management; Development; Macaca; Weaning

Indexed keywords

ANIMAL WELFARE; BEHAVIOR; COLONY; DECISION MAKING; LABORATORY METHOD; LITERATURE REVIEW; MANAGEMENT PRACTICE; PRIMATE; REARING; WEANING; YOUNG POPULATION;

ANIMALIA; HAPLORHINI; MACACA; MACACA FASCICULARIS;

EID: 84859443104     PISSN: 01681591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.applanim.2011.11.001     Document Type: Article

References (189)

1. Ackerman S.H., Keller S.E., Schleifer S.J., Shindledecker R.D., Camerino M., Hofer M.A., Weiner H., Stein M. Premature maternal separation and lymphocyte function. Brain Behav. Immun. 1988, 2:161-165.
2. Altmann J., Altmann S.A., Hausfater G., McCuskey S.A. Life history of yellow baboons: physical development, reproductive parameters, and infant mortality. Primates 1977, 18:315-330.
3. Andrews M.W., Rosenblum L.A. Assessment of attachment in differentially reared infant monkeys (Macaca radiata): response to separation and a novel environment. J. Comp. Psychol. 1993, 107:84-90.
4. Animal Procedures Committee, 2006. Acceptance of Overseas Centre Supplying Non-human Primates to UK Laboratories: A Report by the Primates Sub-Committee of the Animal Procedures Committee. Animal Procedures Committee, London.
5. Barrett C.E., Noble P., Hanson E., Pine D.S., Winslow J.T., Nelson E.E. Early adverse rearing experiences alter sleep-wake patterns and plasma cortisol in juvenile rhesus monkeys. Psychoneuroendocrinology 2009, 34:1029-1040.
6. Baskerville M. Old World monkeys. UFAW Handbook on the Care and Management of Laboratory Animals, Volume 1-Terrestrial Vertebrates 1999, 611-635. Blackwell Science, Oxford. 7th edition. T. Poole (Ed.).
7. Bastian M.L., Sponberg A.C., Suomi S.J., Higley J.D. Long-term effects of infant rearing condition on the acquisition of dominance rank in juvenile and adult rhesus macaques (Macaca mulatta). Dev. Psychobiol. 2003, 42:44-51.
8. Bechard A., Mason G. Leaving home: a study of laboratory mouse pup independence. App. Anim. Behav. Sci. 2010, 125:181-188.
9. Becker M.L., Barr C.S., Gura T.L., Champoux M., Suomi S.J., Higley J.D. The relationships between distress vocalizations and cortisol response during stress are modulated by early rearing experience in rhesus macaques. Am. J. Primatol. 2002, 57(Suppl. 1):55-56.
10. Bellanca R.U., Crockett C.M. Factors predicting increased incidence of abnormal behaviour in male pigtailed macaques. Am. J. Primatol. 2002, 58:57-69.
11. Berman C.M. Mother-infant relationships among free-ranging rhesus monkeys on Cayo Santiago: a comparison with captive pairs. Anim. Behav. 1980, 28:860-873.
12. Bernstein I.S., Dobrofsky M. Compensatory social responses of older pigtailed monkeys to maternal separation. Dev. Psychobiol. 1981, 14:163-168.
13. Boccia M.L., Laudenslager M.L., Reite M.L. Individual differences in macaques' responses to stressors based on social and physiological factors: implications for primate welfare and research outcomes. Lab. Anim. 1995, 29:250-257.
14. Boccia M.L., Scanlan J.M., Laudenslager M.L., Berger C.L., Hijazi A.S., Reite M.L. Juvenile friends, behavior, and immune responses to separation in bonnet macaque infants. Physiol. Behav. 1997, 61:191-198.
15. Bourne G.H., Golarz de Bourne M.N. Breeding monkeys for biomedical research. The Rhesus Monkey 1975, vol. 2:261-276. Academic Press, New York.
16. Bowlby J. Attachment and Loss. Vol. 1. Attachment 1969, Basic, New York.
17. Boyce W.T., Champoux M., Suomi S.J., Gunnar M.R. Salivary cortisol in nursery-reared rhesus monkeys: reactivity to peer interactions and altered circadian activity. Dev. Psychobiol. 1995, 28:257-267.
18. Bradwell A. The benefits of hand-rearing in a colony of Macaca fascicularis. Congress of the Institute of Animal Technology 2001, 40. (abstracts).
19. Buchl S.J., Keeling M.E., Voss W.R. Establishing specific pathogen-free (SPF) nonhuman primate colonies. ILAR J. 1997, 38:22-27.
20. Caine N., Michell G. A review of play in the genus Macaca: social correlates. Primates 1979, 20:535-546.
21. Capitanio J.P. Behavioral pathology. Comparative Primate Biology, Vol. 2, Part A: Behavior, Conservation, and Ecology 1986, 411-454. Alan R. Liss, New York. G. Mitchell, J. Erwin (Eds.).
22. Capitanio J.P. Social experience and immune system measures in laboratory-housed macaques: implications for management and research. ILAR J. 1998, 39:12-20.
23. Capitanio J.P., Lerche N.W. Psychosocial factors and disease progression in simian AIDS: a preliminary report. AIDS 1991, 5:1103-1106.
24. Capitanio J.P., Reite M. The roles of early separation experience and prior familiarity in the social relations of pigtail macaques: a descriptive multivariate study. Primates 1984, 25:475-484.
25. Capitanio J.P., Mendoza S.P., Mason W.A., Maninger N. Rearing environment and hypothalamic-pituitary-adrenal regulation in young rhesus monkeys (Macaca mulatta). Dev. Psychbiol. 2005, 46:318-330.
26. Capitanio J.P., Kyes R.C., Fairbanks L.A. Considerations in the selection and conditioning of Old World monkeys for laboratory research: animals from domestic sources. ILAR J. 2006, 47:294-306.
27. Carlsson H.E., Schapiro S.J., Farah I., Hau J. Use of primates in research: a global overview. Am. J. Primatol. 2004, 63:225-237.
28. Chamove A.S., Rosenblum L.A., Harlow H.F. Monkeys (Macaca mulatta) raised only with peers: a pilot study. Anim. Behav. 1973, 21:316-325.
29. Champoux M., Suomi S.J. Behavioural and adrenocortical responses of rhesus macaque mothers to infant separation in an unfamiliar environment. Primates 1994, 35:191-202.
30. Champoux M., Coe C.L., Schanberg S.M., Kuhn C.M., Suomi S.J. Hormonal effects of early rearing conditions in the infant rhesus monkey. Am. J. Primatol. 1989, 19:111-117.
31. Champoux M., Byrne E., DeLizio R., Suomi S.J. Motherless mothers revisited: rhesus maternal behavior and rearing history. Primates 1992, 33:251-255.
32. Champoux M., Bennett A., Shannon C., Higley J.D., Lesch K.P., Suomi S.J. Serotonin transporter gene polymorphism, differential early rearing, and behavior in rhesus monkey neonates. Mol. Psychiatry 2002, 7:1058-1063.
33. Chapman K., Pullen N., Andrews L., Ragan I. The future of non-human primate use in mAb development. Drug Discov. Today 2010, 15:235-242.
34. Clarke A.S. Social rearing effects on HPA axis activity over early development and in response to stress in rhesus monkeys. Dev. Psychobiol. 1993, 26:433-446.
35. Coe C.L. Psychosocial factors and immunity in nonhuman primates: a review. Psychosom. Med. 1993, 55:298-308.
36. Coe C.L., Lubach G.R., Ershler W.B., Klopp R.G. Influence of early rearing on lymphocyte proliferation responses in juvenile rhesus monkeys. Brain Behav. Immun. 1989, 3:47-60.
37. Coe C.L., Lubach G.R., Schneider M.L., Dierschke D.J., Ershler W.B. Early rearing conditions alter immune responses in the developing infant primate. Pediatrics 1992, 90:505-509.
38. Coleman K., Tully L.A., McMillan J.L. Temperament correlates with training success in adult rhesus macaques. Am. J. Primatol. 2005, 65:63-71.
39. Council of Europe, 2006. Appendix A of the European Convention for the Protection of Vertebrate Animals Used for Experimental and Other Scientific Purposes (ETS No. 123), Guidelines for Accommodation and Care of Animals (Article 5 of the Convention), Approved by the Multilateral Consultation, 15 June 2006, Cons 123 (2006) 3. Council of Europe, Strasbourg, France. (accessed 20.10.10). http://www.coe.int/t/e/legal_affairs/legal_co-operation/biological_safety%2C_use_of_animals/laboratory_animals/2006/Cons123(2006)3AppendixA_en.pdf.
40. Curley J.P., Jordan E.R., Swaney W.T., Izraelit A., Kammel S., Champagne F.A. The meaning of weaning: influence of the weaning period on behavioral development in mice. Dev. Neurosci. 2009, 31:318-331.
41. Durham D.L., Newell-Morris L.L. Is it nutrients or nurturing? Comparison of the growth and development of mother-reared and laboratory-reared macaque infants (Macaca nemestrina). Nursery Rearing of Nonhuman Primates in the 21st Century 2006, 249-268. Springer, New York. G.P. Sackett, G.C. Ruppenthal, K. Elias (Eds.).
42. Elmore D.B., Anderson J.H., Hird D.W., Sanders K.D., Lerche N.W. Diarrhea rates and risk factors for developing chronic diarrhea in infant and juvenile rhesus monkeys. Lab. Anim. Sci. 1992, 42:356-359.
43. European Union, 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. Official J. Eur. Union, L 276/33. (accessed 22.10.10). http://eur-lex.europa.eu/LexUriServ/LexUriServ.do%3Furi=OJ%3AL%3A2010%3A276%3A0033%3A0079%3AEN%3APDF.
44. Evans G.J., Groves S.E. Handrearing rhesus macaques involving catering for individual needs whilst allowing a structured handrearing schedule. Anim. Technol. Welf. 2005, 4:109-111.
45. Fairbanks L.A., McGuire M.T. Age, reproductive value, and dominance related behaviour in vervet monkey females: cross-generational influences on social relationships and reproduction. Anim. Behav. 1986, 34:1710-1721.
46. Garner J.P. Stereotypies and other abnormal repetitive behaviors: potential impact on validity, reliability, and replicability of scientific outcomes. ILAR J. 2005, 46:106-117.
47. George J.W., Lerche N.W. Electrolyte abnormalities associated with diarrhea in rhesus monkeys: 100 cases (1986-1987). J. Am. Vet. Med. Assoc. 1990, 196:1654-1658.
48. Gluck J.P. The intellectual consequences of early social restriction in rhesus monkeys (Macaca mulatta). Nursery Care of Nonhuman Primates 1979, 253-267. Plenum Press, New York. G.C. Ruppenthal (Ed.).
49. Goin D.L., Gust D.A. Peer-rearing influences subsequent maternal behavior and infant survival in a newly formed herpes B-virus negative rhesus macaque group. Primates 1998, 39:539-543.
50. Goldfoot D.A. Rearing conditions which support or inhibit later sexual potential of laboratory-born rhesus monkeys: hypotheses and diagnostic behaviours. Lab. Anim. Sci. 1977, 27:548-556.
51. Golub M.S., Anderson J.H., Goo G.P., Sassenrath E.N. Plasma cortisol response to different methods of weaning in rhesus monkey (Macaca mulatta) infants. Lab. Anim. Sci. 1981, 31:400-402.
52. Goo G.P., Fugate J.K. Effects of weaning on age on maternal reproduction and offspring health in rhesus monkeys (M. mulatta). Lab. Anim. Sci. 1984, 34:66-69.
53. Goosen C. Influence of age of weaning on the behaviour and well-being of rhesus monkeys. Laboratory Animal Welfare Research-Primates 1989, Universities Federation for Animal Welfare, Potters Bar, England, pp. 17-22.
54. Gordon T.P., Gust D.A., Wilson M.E. Social separation and reunion affects immune system in juvenile rhesus monkeys. Physiol. Behav. 1992, 51:467-472.
55. Goy R.W., Wallen K. Experiential variables influencing play, foot-clasp mounting and adult sexual competence in male rhesus monkeys. Psychoneuroendocrinology 1979, 4:1-12.
56. Goy R.W., Wallen K., Goldfoot D.A. Social factors affecting the development of mounting behavior in male rhesus monkeys. Reproductive Behavior 1974, 223-247. Plenum Publishing Corp., New York. W. Montagna, W.A. Sadler (Eds.).
57. Gunnar M.R., Gonzalez C.A., Goodlin B.L., Levine S. Behavioral and pituitary-adrenal responses during a prolonged separation period in infant rhesus macaques. Psychoneuroendoncrinology 1981, 6:65-75.
58. Gunnar M.R., Gonzalez C.A., Levine S. The role of peers in modifying behavioural distress and pituitary-adrenal response to a novel environment in year-old rhesus monkeys. Physiol. Behav. 1980, 25:795-798.
59. Gust D.A., Gordon T.P., Wilson M.E., Brodie A., Ahmed-Ansari A., McClure H.M. Removal from natal social group to peer housing affects cortisol levels and absolute numbers of T cell subsets in juvenile rhesus monkeys. Brain, Behav. Immunol. 1992, 6:189-199.
60. Harlow H.F., Harlow M.K., Schlitz K.A., Mohr D.J. The effect of early adverse and enriched environments on the learning ability of rhesus monkeys. Cognitive Processes of Nonhuman Primates 1971, 121-148. Academic Press, New York. L.E. Jarrard (Ed.).
61. Harlow H.F., Suomi S.J. Induced depression in monkeys. Behav. Biol. 1974, 12:273-296.
62. Harvey P.H., Martin R.D., Clutton-Brock T.H. Life histories in comparative perspective. Primate Societies 1987, 181-186. University of Chicago Press, Chicago.B.B. Smuts, D.L. Cheyney, R.M. Seyfarth, R.W. Wrangham, T.T. Struhsaker (Eds.).
63. Hasegawa T., Hiraiwa M. Social interactions of orphans observed in a free-ranging troop of Japanese monkeys. Folia Primatol. 1980, 33:129-158.
64. Herbert T.B., Cohen S. Stress and immunity in humans: a meta-analytic review. Psychosom. Med. 1993, 55:364-379.
65. Hinde R.A., Spencer Booth Y. Effects of brief separation from mother on rhesus monkeys. Science 1971, 173:111-118.
66. Hiraiwa M. Maternal and alloparental care in a troop of free-ranging Japanese monkeys. Primates 1981, 22:309-329.
67. Home Office Code of Practice for the Housing and Care of Animals in Designated Breeding and Supplying Establishments 1995, Her Majesty's Stationery Office, London.
68. Honess P., Stanley-Griffiths M.A., Narainapoulle S., Naiken S., Andrianjazalahatra T. Selective breeding of primates for use in research: consequences and challenges. Anim. Welf. 2010, 19(Suppl.):57-65.
69. Hsu C.K., Jia R. Breeding and supply of Chinese macaques for biomedical research. Caring for Primates: Abstracts of the XIXth Congress of the International Primatological Society 2002, 188-189. Mammalogical Society of China, Beijing.
70. Institute for Laboratory Animal Research International perspectives: the future of nonhuman primate resources. Proceedings of the Workshop Held April 17-19, 2002 2003, National Academy Press, Washington, D.C.
71. Ismail I. Epidemiology of diarrhea-related morbidity and mortality in single birth cohort of rhesus macaques (Macaca mulatta). MPVM Research Project 1995, School of Veterinary Medicine, University of California, Davis.
72. Jennings, M., Prescott, M.J. (Eds.), 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. Lab. Anim. 43 (S1), 1-47.
73. Jones M.A., Mason G., Pillav N. Early social experience influences the development of stereotypic behaviour in captive-born striped mice Rhabdomys. App. Anim. Behav. Sci. 2010, 123:70-75.
74. Kaplan J.R. Psychological stress and behavior in nonhuman primates. Comparative Primate Biology, Vol. 2, Part A: Behavior, Conservation, and Ecology 1986, 455-492. Alan R. Liss, New York.
75. Kaufman I.C., Rosenblum L.A. Depression in infant monkeys separated from their mothers. Science 1967, 155:1030-1031.
76. Kotera S., Tanaka T., Tajima Y., Nomura T. Establishment of an island breeding colony of Japanese monkeys as a laboratory animal. Lab. Anim. Handbooks 1975, 6:95-105.
77. Kraemer G. Psychobiology of early social attachment in rhesus monkeys: clinical implications. Ann. N. Y. Acad. Sci. 1997, 807:408-418.
78. Kraemer G.W., Ebert M.H., Schmidt D.E., McKinney W.T. Strangers in a strange land: a psychobiological study of infant monkeys before and after separation from real or inanimate mothers. Child Dev. 1991, 62:548-566.
79. Kriete M.F., Champoux M., Suomi S.J. Development of iron deficiency anemia in infant rhesus macaques. Lab. Anim. Sci. 1995, 45:15-21.
80. Laboratory Animal Science Association, Medical Research Council, 2004. Principles of best practice in the breeding of macaques and marmosets for scientific purposes: a statement by the Laboratory Animal Science Association and the Medical Research Council. (accessed 22.10.10). http://www.lasa.co.uk/position_papers/LASACBPAR%20breeding%20of%20primates.pdf.
81. Latham N.R., Mason G.J. Maternal deprivation and the development of stereotypic behaviour. App. Anim. Behav. Sci. 2008, 110:84-108.
82. Laudenslager M.L. The psychobiology of loss. Lessons from humans and nonhuman primates. J. Soc. Issues 1988, 44:19-36.
83. Laudenslager M.L., Boccia M.L. Some observations on psychosocial stressors, immunity and individual differences in nonhuman primates. Am. J. Primatol. 1996, 39:205-221.
84. Laudenslager M.L., Capitanio J.P., Reite M.L. Possible effects of early separation experiences on subsequent immune function in adult macaque monkeys. Am. J. Psychiatry 1985, 142:862-864.
85. Laudenslager M.L., Held D.E., Boccia M.L., Reite M.L., Cohen J.J. Behavioral and immunological consequences of brief mother-infant separation: a species comparison. Dev. Psychobiol. 1990, 23:247-264.
86. Laudenslager M.L., Boccia M.L., Berger C.L., Gennaro-Ruggles M.M., McFerran B., Reite M.L. Total cortisol, free cortisol, and growth hormone with brief social separation experiences in young macaques. Dev. Psychobiol. 1995, 28:199-211.
87. Lee P.C. Comparative ecology of postnatal growth and weaning among haplorhine primates. Comparative Primate Socioecology 1999, 111-139. Cambridge University Press, Cambridge. P.C. Lee (Ed.).
88. Levine S., Johnson D.F., Gonzalez C.A. Behavioral and hormonal responses to separation in infant rhesus monkeys and mothers. Behav. Neurosci. 1985, 99:399-410.
89. Lindburg D.G. The rhesus monkey in north India: an ecological and behavioral study. Primate Behavior: Development in Field and Laboratory Research 1971, vol. 2:1-106. Academic Press, New York.
90. Lubach G.R., Coe C.L., Ershler W.B. Effects of early rearing environment on immune responses of infant rhesus monkeys. Brain Behav. Immun. 1995, 9:31-46.
91. Lutz C., Well A., Novak M. Stereotypic and self-injurious behavior in rhesus macaques: a survey and retrospective analysis of environment and early experience. Am. J. Primatol. 2003, 60:1-15.
92. Lutz C., Tiefenbacher S., Meyer J., Novak M. Extinction deficits in male rhesus macaques with a history of self-injurious behaviour. Am. J. Primatol. 2004, 63:41-48.
93. Lutz C.K., Davis E.B., Ruggiero A.M., Suomi S.J. Early predictors of self-biting in socially-housed rhesus macaques (Macaca mulatta). Am. J. Primatol. 2007, 69:584-590.
94. MacDonald Pavelka M.S., Fedigan L.M., Zohar S. Availability and adaptive value of reproductive and postreporoductive Japanese macaque mothers and grandmothers. Anim. Behav. 2002, 64:407-414.
95. Maestripieri D., Carroll K.A. Risk factors for infant abuse and neglect in group-living rhesus monkeys. Psychol. Sci. 1998, 9:143-145.
96. Maestripieri D., Carroll K.A. Behavioral and environmental correlates of infant abuse in group-living pigtail macaques. Infant Behav. Dev. 1998, 21:603-612.
97. Maestripieri D., Carroll K.A. Causes and consequences of infant abuse and neglect in monkeys. Aggress. Violent Behav. 2000, 5:245-254.
98. Maestripieri D., Wallen K., Carroll K.A. Infant abuse runs in families of group-living pigtailed macaques. Child Abuse Neglect 1997, 21:465-471.
99. Maninger N., Sackett G.P., Ruppenthal G.C. Weaning, body weight and postpartum amenorrhea duration in pigtailed macaques (Macaca nemestrina). Am. J. Primatol. 2000, 52:81-91.
100. Mansfield K. Development of specific pathogen free nonhuman primate colonies. The Laboratory Primate 2005, 229-239. Elsevier Academic Press, San Diego. S. Wolfe-Coote (Ed.).
101. Mansfield K.G., Kemnitz J.W. Challenges in microbial quality control for nonhuman primates. ILAR J. 2008, 49:133-136.
102. Mason G.J., Latham N.R. Can't stop, won't stop: is stereotypy a reliable animal welfare indicator?. Anim. Welf. 2004, 13:S57-S69.
103. Mason W.A. The effects of environmental restriction of social development on rhesus monkeys. Primate Social Behaviour 1963, 161-173. Van Nostrand Reinhold Co., New York. C.H. Southwick (Ed.).
104. Mason W.A. Effects of social interaction on well-being: developmental aspects. Lab. Anim. Sci. 1991, 41:323-328.
105. McCann, C., Buchanan-Smith, H.M., Farmer, K., Fitch-Snyder, H., Jones-Engel, L., Prescott, M., Taylor, S., 2007. IPS International Guidelines for the Acquisition, Care and Breeding of Nonhuman Primate, second edition. (accessed 22.10.10). http://www.internationalprimatologicalsociety.org/docs/IPS_International_Guidelines_for_the_Acquisition_Care_and_Breeding_of_Nonhuman_Primates_Second_Edition_2007.pdf.
106. Meishvili N.V., Chalyah V.G., Vancatova M.A. Mother-infant relationships in cynomolgus monkeys (Macaca fascicularis). Primate Rep. 1991, 29:41-46.
107. Melnick D.J., Pearl M.C., Richard A.F. Male migration and inbreeding avoidance in wild rhesus monkeys. Am. J. Primatol. 1984, 7:229-243.
108. Minami T. The behavioural development of mother-infant relations in the first six months of the infants' life in the Japanese monkey (Macaca fuscata fuscata). 1. Filial cling and maternal embrace and grooming. Annu. Anim. Psychol. 1974, 24:15-24.
109. Mineka S., Suomi S.J. Social separation in monkeys. Psychol. Bull. 1978, 8:1376-1400.
110. Mogi K., Nagasawa M., Kikusui T. Developmental consequences and biological significance of mother-infant bonding. Prog. Neuropsychopharmacol. Biol. Psychiatry 2011, 35:1232-1241.
111. Morton W.R., Agy M.B., Capuano S.V., Grant R.F. Specific pathogen-free macaques: definition, history, and current production. ILAR J. 2008, 49:137-144.
112. Muñoz-Zanzi C.M., Thurmond M.C., Hird D.W., Lerche N.W. Effect of weaning time and associated management practices on post-weaning chronic diarrhea in captive rhesus monkeys (Macaca mulatta). Lab. Anim. Sci. 1999, 49:617-621.
113. Nagarajan P., Venkatesan P., Kumar J.M., Majumdar S.S. Suppression of lactation in post-weaning Macaca radiata by bromocriptine under laboratory conditions. Lab. Primate Newslett. 2004, 43:12-13.
114. National Research Council, 1998. The Psychological Well-being of Nonhuman Primates: A Report of the Committee on Well-being of Nonhuman Primates. Institute for Laboratory Animal Research. Committee on Well-Being of Nonhuman Primates, Institute of Laboratory Animal Research, Commission on Life Sciences, National Research Council. National Academy Press, Washington, D.C.
115. Nicolson N.A. Infants, mothers, and other females. Primate Societies 1987, 330-342. University of Chicago Press, Chicago. B.B. Smuts, D.L. Cheney, R.M. Seyfarth, R.W. Wrangham, T.T. Struhsaker (Eds.).
116. Norikoshi K. The development of peer-mate relationships in Japanese macaque infants. Primates 1974, 15:39-46.
117. Novak M.A. Self-injurious behaviour in rhesus monkeys: new insights into its etiology, physiology, and treatment. Am. J. Primatol. 2003, 59:3-19.
118. Novak M.A., Suomi S.J. Social separation in monkeys. Psychol. Bull. 1988, 85:1376-1400.
119. Novak M.F., Sackett G.P. Pair-rearing infant monkeys (Macaca nemestrina) using a " rotating-peer" strategy. Am. J. Primatol. 1997, 41:141-149.
120. Parr L.A., Winslow J.T., Davis M. Rearing experience differentially affects somatic and cardiac startle responses in rhesus monkeys (Macaca mulatta). Behav. Neurosci. 2002, 116:378-386.
121. Platt D.M., Kinsey J.H., Jorgensen M.J., Novak M.A. Factors affecting the expression of self-injurious behavior in rhesus monkeys (Macaca mulatta). XVIth Congress of the International Primatological Society/XIXth Conference of the American Society of Primatologists, Abstract No. 768 1996.
122. Poole T. Happy animals make good science. Lab. Anim. 1997, 31:116-124.
123. Poole T., Thomas A.W. Primate Vaccine Evaluation Network: Recommendations, Guidelines and Information for Biomedical Research Involving Non-Human Primates with Emphasis on Health Problems of Developing Countries 1995, European Commission DG-XII, Brussels, Belgium.
124. Poole T.B., Costa P., Netto W.J., Schwartz K., Wechsler B., Whittaker D. Non-human primates. The Accommodation of Laboratory Animals in Accordance with Animal Welfare Requirements. Proceedings of an International Workshop held at Bundesgesundheitsamt 1994, 81-86. Bundesministerium für Ernährung, Landwirtshaft und Forsten, Bonn, Germany. P.N. O'Donoghue (Ed.).
125. Porton I., Niebruegge K. The changing role of hand rearing in zoo-based primate breeding programmes. Nursery Rearing of Nonhuman Primates in the 20th Century 2006, 21-31. Springer, New York. G.P. Sackett, G.C. Ruppenthal, K. Elias (Eds.).
126. Prescott M.J., Jennings M. Ethical and welfare implications of the acquisition and transport of non-human primates for use in research and testing. ATLA - Altern. Lab. Anim. 2004, 32(S1A):323-327.
127. Reinhardt V. Artificial weaning of Old World monkeys: benefits and costs. J. Appl. Anim. Welf. Sci. 2002, 5:151-156.
128. Reinhardt V. Common husbandry-related variables in biomedical research with animals. Lab. Anim. 2004, 38:213-235.
129. Reite M. Infant abuse and neglect: lessons from the primate laboratory. Child Abuse Neglect 1987, 11:347-355.
130. Reite M., Short R., Seiler C., Pauley D.J. Attachment, loss, and separation. J. Child Psychol. Psychiatry 1981, 22:141-169.
131. Rennie A.E., Buchanan-Smith H.M. Report on the extent and character of primate use in scientific procedures across Europe in 2001. Lab. Primate Newslett. 2005, 44:6-12.
132. Roberts J.A., Lerche N., Short J., Penedo C. Pedigreed specific pathogen free rhesus macaques, production and management. Caring for Primates, Abstracts of the XIXth Congress of the International Primatological Society 2002, 281. Mammalogical Society of China, Beijing, China.
133. Rommeck I., Gottlieb D.H., Strand S.C., McCowan B. The effects of four nursery rearing strategies on infant behavioral development in rhesus macaques (Macaca mulatta). J. Am. Assoc. Lab. Anim. Sci. 2009, 48:395-401.
134. Rommeck I., Anderson K., Heagerty A., Cameron A., McCowan B. Risk factors and remediation of self-injurious and self-abuse behaviour in rhesus macaques. J. Appl. Anim. Welf. Sci. 2009, 12:61-72.
135. Roonwal M.L., Mohnot S.M. Primates of South Asia: Ecology, Sociobiology and Behavior 1977, Harvard University Press, Cambridge, MA.
136. Rosenblum L.A., Kaufman I.C. Laboratory observations of early mother-infant relations in pigtail and bonnet macaques. Social Communication Among Primates 1967, 33-41. University of Chicago Press, Chicago. A.S. Altmann (Ed.).
137. Ross C. Life history patterns and ecology of macaque species. Primates 1992, 32:207-215.
138. Ruppenthal G.C., Arling G.L., Harlow H.F., Sackett G.P., Suomi S.J. A 10-year perspective of motherless-monkey behavior. J. Abnorm. Psychol. 1976, 85:341-349.
139. Ruppenthal G.C., Sackett G.P. Nursery care of at-risk nonhuman primates. Nursery Rearing of Nonhuman Primates in the 20th Century 2006, 371-390. Springer, New York. G.P. Sackett, G.C. Ruppenthal, K. Elias (Eds.).
140. Russell R.G., Rosenkranz S.L., Lee L.A., Howard H., DiGiacomo R.F., Bronsdon M.A., Blakley G.A., Tsai C.C., Morton W.R. Epidemiology and etiology of diarrhea in colony-born Macaca nemestrina. Lab. Anim. Sci. 1987, 37:309-316.
141. Russell W.M.S. The ill-effects of uncomfortable quarters. Comfortable Quarters for Laboratory Animals 2002, 1-5. Animal Welfare Institute, Washington, D.C. 9th edition. V. Reinhardt, A. Reinhardt (Eds.).
142. Sackett G.P., Ruppenthal G.C. Growth of nursery-reared Macaca nemestrina infants: effects of feeding schedules, sex and birth weight. Am. J. Primatol. 1992, 27:189-204.
143. Sackett G.P., Ruppenthal G.C., Elias K. Nursery Rearing of Nonhuman Primates in the 21st Century 2006, Springer, Chicago, IL.
144. Sackett G.P., Terao K. Separation stress in mother and nursery reared pigtailed monkey infants (M. nemestrina). XIVth Congress of the International Primatological Society, Strasbourg 1992, Abstract No. 0462 1992, 237. International Primatological Society.
145. Sackett G.P., Erwin J. Effects of weaning age on mortality of colony-born Macaca nemestrina. Theriogenology 1981, 15:505-511.
146. Sackett G.P., Ruppenthal G.C., Davis A.E. Survival, growth, health, and reproduction following nursery rearing compared with mother rearing in pigtailed monkeys (Macaca nemestrina). Am. J. Primatol. 2002, 56:165-183.
147. Sade D.S. Some aspects of parent-offspring and sibling relations in a group of rhesus monkeys, with a discussion of grooming. Am. J. Phys. Anthropol. 1965, 23:1-17.
148. Scientific Committee on Animal Health and Welfare, 2002. The welfare of non-human primates used in research. Report of the Scientific Committee on Animal Health and Welfare, Adopted on 17 December 2002. Health and Consumer Protection Directorate-General, European Commission, Brussels, Belgium. (accessed 22.10.10). http://ec.europa.eu/food/fs/sc/scah/out83_en.pdf.
149. Schapiro S.J. A few new developments in primate housing and husbandry. Scand. J. Lab. Anm. Sci. 2000, 27:103-110.
150. Schapiro S.J., Lee-Parritz D.E., Taylor L.L., Watson L., Bloomsmith M.A., Petto A. Behavioral management of specific pathogen-free rhesus macaques: group formation, reproduction, and parental competence. Lab. Anim. Sci. 1994, 44:229-234.
151. Schapiro S.J., Bloomsmith M.A., Suarez S.A., Porter L.M. Maternal behavior of primiparous rhesus monkeys: effects of limited social restriction and inanimate environmental enrichment. App. Anim. Behav. Sci. 1995, 45:139-149.
152. Schino G., Troisi A. Neonatal abandonment in Japanese macaques. Am. J. Phys. Anthropol. 2005, 126:447-452.
153. Seay B., Alexander B.K., Harlow H.F. Maternal behaviour of socially deprived rhesus monkeys. J. Abnorm. Soc. Psychol. 1964, 69:345-354.
154. Shannon C., Champoux M., Suomi S.J. Rearing condition and plasma cortisol in rhesus monkeys infants. Am. J. Primatol. 1998, 46:311-321.
155. Singh R. Ontogeny of play behavior in free-ranging rhesus macaques (Macaca mulatta). Proc. Indian Acad. Sci. (Anim. Sci.) 1986, 95:605-612.
156. Smith J.A., Boyd K.M. The Boyd Group Papers on the Use of Non-Human Primates in Research and Testing 2002, British Psychological Society, Southsea, U.K.
157. Smotherman W.P., Hunt L.E., McGinnis L.M., Levine S. Mother-infant separation in group-living rhesus macaques: a hormonal analysis. Dev. Psychobiol. 2004, 12:211-217.
158. Southey E.R., Baldwin C.M. Socialisation of rhesus macaques at CFM. Anim. Technol. Welf. 2006, 5:119-122.
159. Southwick C.H., Beg M.A., Siddiqi M.R. Rhesus monkeys in north India. Primate Behavior: Field Studies in Monkeys and Apes 1965, 111-159. Holt, Rinehart and Winston, New York. I. DeVore (Ed.).
160. Spencer-Booth Y., Hinde R.A. Effects of brief separations from mothers during infancy on behaviour or rhesus monkeys 6-24 months later. J. Child Psychol. Psychiatry 1971, 12:157-172.
161. Suomi S.J. Social interactions of monkeys reared in a nuclear family environment vs. monkeys reared with mothers and peers. Primates 1974, 15:311-320.
162. Suomi S.J. Maternal behaviour by socially incompetent monkeys: neglect and abuse of offspring. J. Pediatr. Psychol. 1978, 3:28-34.
163. Suomi S.J. Genetic, maternal, and environmental influences on social development in rhesus monkeys. Primate Behavior and Sociobiology 1981, 81-87. Springer-Verlag, New York. A.B. Chiarelli, R.S. Corruccini (Eds.).
164. Suomi S.J. Anxiety-like disorders in young nonhuman primates. Anxiety Disorders of Childhood 1986, 1-23. Guildford Press, New York. R. Gittelman (Ed.).
165. Suomi S.J. Uptight and laid-back monkeys: individual differences in the response to social challenges. Plasticity of Development 1991, 27-56. MIT Press, Cambridge. S.E. Brauth, W.S. Hall, R.J. Dooling (Eds.).
166. Suomi S.J. Developmental trajectories, early experiences, and community consequences: lessons from studies with rhesus monkeys. Developmental Health and Wealth of Nations: Social, Biological, and Educational Dynamics 1999, 185-200. Guilford Press, New York.D.P. Keating, C. Hertzman (Eds.).
167. Suomi S.J., Harlow H.F. The role and reason of peer relationships in rhesus monkeys. Orig. Behav. 1975, 4:153-185.
168. Suomi S.J., Ripp C. A history of motherless mother monkey mothering at the University of Wisconsin Primate Laboratory. Child Abuse: The nonhuman Primate Data 1983, 49-78. Alan R. Liss Inc., New York. M. Reite, N.G. Caine (Eds.).
169. Timmermans P.J.A. Development of maternal behaviour in monkeys: effects of rearing condition and motherhood on periparturitional behaviour. Folia Primatol. 1997, 67:212-213.
170. Timmermans P.J.A., Vossen J.M.H. The influence of rearing conditions on maternal behaviour in cynomolgus monkeys (Macaca fascicularis). Int. J. Primatol. 1996, 17:259-276.
171. Timmermans P.J.A., Roder E.L., Kemps A.M.L.J. Rearing cynomolgus monkeys (Macaca fascicularis) on surrogate mothers with bottle feeding. Lab. Anim. 1988, 22:229-234.
172. Timmermans P.J.A., Vochteloo J.D., Vossen J.M.H., Röder E.L., Duijghuisen J.A.H. Persistent neophobic behavior in monkeys: a habit or a trait?. Behav. Process. 1994, 31:177-196.
173. Tsuchida J., Yoshida T., Sankai T., Yasutomi Y. Maternal behaviour of laboratory-born, individually-reared long-tailed macaques (Macaca fascicularis). J. Am. Assoc. Lab. Anim. Sci. 2008, 47:29-34.
174. United States Department of Agriculture Animal and Plant Health Inspection Service, 1999. Draft Policy on Environmental Enhancement for Nonhuman Primates. 9 CFR Part 3. Federal Register, pp. 38145-38150.
175. Valentine B., Cary M., Stanley J., White G., Wallis J. The timing of mother-infant separation and its effect on postpartum estrus and subsequent conception in captive baboons. Am. J. Primatol. 1999, 49:110.
176. Valerio D.A., Darrow C.C., Martin I.I., Martin D.P. Rearing of infant simians in modified germ free isolators for oncogenic studies. Lab. Anim. Care 1970, 20:713-719.
177. Van Luijk I.A.F., Timmermans P.J.A., Sweep F., Willems J., Vossen J.M.H. Differences in behaviour and physiology between adult surrogate-reared and mother-reared cynomolgus monkeys (Macaca fascicularis). Folia Primatol. 2000, 71:201.
178. van Noordwijk M.A., Hemelrijk C.K., Herremans L., Sterck E.H.M. Spatial position and behavioral sex differences in juvenile long-tailed macaques. Juvenile Primates: Life History, Development and Behavior 1993, 77-85. Oxford University Press, New York. M.E. Pereira, L.A. Fairbanks (Eds.).
179. Wallen K. Nature needs nurture: the interaction of hormonal and social influences on the development of behavioural sex differences in rhesus monkeys. Horm. Behav. 1996, 30:364-378.
180. Wallen K., Goldfoot D.A., Goy R.W. Peer and maternal influences on the expression of foot-clasp mounting by juvenile male rhesus monkeys. Dev. Psychbiol. 1981, 14:299-309.
181. Wallis J., Valentine B. Early vs. natural weaning in captive baboons: the effect on timing of postpartum oestrus and next conception. Lab. Primate Newslett. 2001, 40:10-13.
182. Welshman M. Breeding macaques in source countries. The UFAW Handbook on the Care and Management of Laboratory Animals, Volume 1-Terrestrial Vertebrates 1999, 636-642. Blackwell Science, Oxford. 7th edition. T. Poole (Ed.).
183. Whitley R.J., Hilliard J. Cercopithecine herpes virus 1 (B virus). Fields Virology 2007, vol. 2:2889-2903. Lippincott, Williams and Wilkins, Philadelphia, P.A. 5th edition.
184. Wolfe L., Griesemer R., Rohovsky M. Germfree cynomolgus monkey. Lab. Anim. Care 1966, 16:364-368.
185. Wolfensohn S. Old World monkeys. The UFAW Handbook on the Care and Management of Laboratory and Other Research Animals 2010, 592-617. John Wiley and Sons Ltd., West Sussex. 8th edition. R. Hubrecht, J. Kirkwood (Eds.).
186. Wolfensohn S., Honess P. Handbook of Primate Husbandry and Welfare 2005, Blackwell Publisher, Ames, IA.
187. Worlein J.M., Sackett G.S. Social development in nursery-reared pigtailed macaques (Macaca nemestrina). Am. J. Primatol. 1997, 41:23-35.
188. Yasutomi Y. Establishment of specific pathogen-free macaque colonies in Tsukuba Primate Research Center of Japan for AIDS research. Vaccine 2010, 28(S2):B75-B77.
189. Zwartouw H.T., MacArthur J.H., Chamove Transmission of B virus infection between monkeys especially in relation to breeding colonies. Lab. Anim. 1984, 18:125-130.