Hostname: page-component-848d4c4894-8kt4b Total loading time: 0 Render date: 2024-06-22T02:52:55.678Z Has data issue: false hasContentIssue false
  • English
  • Français

Training laboratory-housed non-human primates, part 1: a UK survey

Published online by Cambridge University Press:  11 January 2023

MJ Prescott  and
HM Buchanan-Smith
MJ Prescott*
Affiliation:
National Centre for the Replacement, Refinement and Reduction of Animals in Research (NC3Rs), 20 Park Crescent, London W1B 1AL, UK
HM Buchanan-Smith
Affiliation:
Department of Psychology, University of Stirling, Stirling FK9 4LA, Scotland, UK
*
* Contact for correspondence and requests for reprints: mark.prescott@nc3rs.org.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

Training using positive reinforcement is increasingly recognised as a valuable tool for the humane and effective management and use of laboratory-housed non-human primates. We utilised a mixed-mode questionnaire to survey use of training and other learning processes (socialisation, habituation and desensitisation) in over half of UK establishments using and breeding primates. The survey demonstrated that there is widespread awareness of training as a refinement technique and appreciation of its diverse benefits, but training is not used as widely or as fully as it might be. This is due to real constraints (principally staff and time and a lack of confidence in ability to train), and perceived constraints (such as a supposed lack of published information on how to train and assessment of the benefits, and an overestimation of the time investment needed). There is also considerable variation between establishments in the purposes of training and techniques used, with a reliance on negative reinforcement in some. We conclude that there is opportunity for refinement of common scientific, veterinary and husbandry procedures (such as blood and urine collection, injection, capture from the group and weighing) through use of positive reinforcement training, especially when combined with appropriate socialisation, habituation and desensitisation. We end this paper with recommendations on best practice, training techniques and staff education.

Keywords

animal welfarehabituationpositive reinforcementrefinementsocialisationtraining
Type
Research Article
Information
Animal Welfare , Volume 16 , Issue 1 , February 2007 , pp. 21 - 36
Copyright
© 2007 Universities Federation for Animal Welfare

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adams, KM, Navarro, AM, Hutchinson, EK and Weed, JL 2004 A canine socialization and training program at the National Institutes of Health. Lab Animal 33: 32–36Google ScholarPubMed
Baker, KC 2004 Benefits of human interaction for socially housed chimpanzees. Animal Welfare 13: 239–245Google ScholarPubMed
Bassett, L, Buchanan-Smith, HM, McKinley, J and Smith, TE 2003 Effects of training on stress-related behavior of the common marmoset (Callithrix jacchus) in relation to coping with routine husbandry procedures. Journal of Applied Animal Welfare Science 6: 221–233CrossRefGoogle ScholarPubMed
Bayne, KA 2002 Development of the human-research animal bond and its impact on animal well-being. Institute for Laboratory Animal Research 43: 4–9CrossRefGoogle ScholarPubMed
Bayne, KA, Dexter, SL and Strange, GM 1993 The effects of food treat provisioning and human interaction on the behavioral well-being of rhesus monkeys (Macaca mulatta). Contemporary Topics in Laboratory Animal Science 32: 6–9Google Scholar
Biological Council 1992 Guidelines on the Handling and Training of Laboratory Animals. UFAW: Wheathampstead, Hertfordshire, UKGoogle Scholar
Bloomsmith, M 1992 Chimpanzee training and behavioral research: A symbiotic relationship. American Association of Zoological Parks and Aquariums Annual Conference Proceedings, pp 403–410. American Association of Zoological Parks and Aquariums: Toronto, Ontario, CanadaGoogle Scholar
Bloomsmith, MA, Lambeth, SP, Stone, AM and Laule, GE 1997 Comparing two types of human interaction as enrichment for chimpanzees. American Journal of Primatology 42: 96 (Abstract)Google Scholar
Bloomsmith, MA, Baker, KC, Ross, SK and Lambeth, SP 1999 Comparing animal training to non-training human interaction as environmental enrichment for chimpanzees. American Journal of Primatology 49: 35–36Google Scholar
Bourgeois, SR and Brent, L 2005 Modifying the behaviour of singly caged baboons: evaluating the effectiveness of four enrichment techniques. Animal Welfare 14: 71–81CrossRefGoogle Scholar
Bowell, V, Buchanan-Smith, HM and Morris, K 2004 The effect of animal age, sex and temperament on the time investment required for positive reinforcement training of common marmosets. Folia Primatologica 75(S1): 359–360Google Scholar
Boxall, J, Heath, S, Bate, S and Brautigam, J 2004 Modern concepts of socialisation for dogs: Implications for their behaviour, welfare and use in scientific procedures. Alternatives to Laboratory Animals 32(S2): 81–93 http://altweb.jhsph.edu/publications/journals/atla/32_sup/boxallp1.pdfCrossRefGoogle ScholarPubMed
Brockway, BP, Hassler, CR and Hicks, N 1993 Minimizing stress during physiological monitoring. In: Niemi, SM, Willson, JE (eds) Refinement and Reduction in Animal Testing pp 56–69. Scientists Center for Animal Welfare: Bethesda, MD, USAGoogle Scholar
Buchanan-Smith, HM, McKinley, J and Prescott, MJ 2003a Positive reinforcement training with New World primates. Joint LASA/LAVA Meeting: Animal Training as Refinement: Basis and Benefits. 27 June 2003, Ware, Hertfordshire, UKGoogle Scholar
Buchanan-Smith, HM, McKinley, J, Bassett, L, Morris, K, Rennie, A and Prescott, MJ 2003b The potential uses of positive reinforcement training in marmosets. European Marmoset Research Group, UK Meeting. 23-24 July 2003, Cambridge, UKGoogle Scholar
Coleman, K, Tully, LA and McMillan, JL 2005 Temperament correlates with training success in adult rhesus macaques. American Journal of Primatology 65: 63–71CrossRefGoogle ScholarPubMed
Desmond, T and Laule, G 1994 Use of positive reinforcement training in the management of species for reproduction. Zoo Biology 13: 471–477CrossRefGoogle Scholar
Elvidge, H, Challis, JRG, Robinson, JS, Roper, C and Thorburn, GD 1976 Influence of handling and sedation on plasma cortisol in rhesus monkeys (Macaca mulatta). Journal of Endocrinology 70: 325–326CrossRefGoogle ScholarPubMed
Hassimoto, M, Harada, T and Harada, T 2004 Changes in hematology, biochemical values, and restraint ECG of rhesus monkeys (Macaca mulatta) following 6-month laboratory acclimation. Journal of Medical Primatology 33: 175–186Google Scholar
Heath, M 1989 The training of cynomolgus monkeys and how the human-animal relationship improves with environmental enrichment. Animal Technology 40: 11–22. http://www.awionline.org/Lab_animals/biblio/at40heath.htmlGoogle Scholar
Heath, SE, Thomas, J and Deegan, C 2002 Preparing laboratory beagles for their life as a working dog. Fourth World Congress on Alternatives and Animal Use in the Life Sciences. 11-15 August 2002, New Orleans, Louisiana, USAGoogle Scholar
Home Office 1989 Code of Practice for the Housing and Care of Animals Used in Scientific Procedures. HMSO: London. http://scienceandresearch.homeoffice.gov.uk/animalresearch/publications/publications/code-of-practice/Google Scholar
Home Office 2000 Guidance on the Operation of the Animals (Scientific Procedures) Act 1986. The Stationary Office: London. http://www.archive.official-documents.co.uk/document/hoc/321/321-00.htmGoogle Scholar
Iliff, SA, Friscino, BH and Anderson, LC 2004 Refinements of study design using positive reinforcement training in macaques. Folia Primatologica 74(S1): 282–283Google Scholar
International Primatological Society 1989 IPS International guidelines for the acquisition, care and breeding of nonhuman primates. Primate Report 25: 3–27. http://www.enviro.co.za/vervet/care_and_breeding.htmGoogle Scholar
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. http://www.lasa.co.uk/position_papers/LASACBPAR%20breeding%20of%20primates.pdfGoogle Scholar
Lambeth, SP, Hau, J, Perlman, JE, Martino, MA, Bernacky, BJ and Schapiro, SJ 2004 Positive reinforcement training affects hematologic and serum chemistry values in captive chimpanzees (Pan troglodytes). American Journal of Primatology 62(S1): 37–38Google Scholar
Laule, G 1999 Training laboratory animals. In: Poole, T (ed) UFAW Handbook on the Care and Management of Laboratory Animals, Edition 7, Volume 1 – Terrestrial Vertebrates pp 21–27. Blackwell Science: Oxford, UKGoogle Scholar
Laule, GE, Thurston, RH, Alford, PL and Bloomsmith, MA 1996 Training to reliably obtain blood and urine samples from a diabetic chimpanzee (Pan troglodytes). Zoo Biology 15: 587–5913.0.CO;2-7>CrossRefGoogle Scholar
Laule, GE, Bloomsmith, MA and Schapiro, SJ 2003 The use of positive reinforcement training techniques to enhance the care, management, and welfare of laboratory primates. Journal of Applied Animal Welfare Science 6: 163–173CrossRefGoogle Scholar
Likert, R 1932 A technique for the measurement of attitudes. Archives of Psychology 140: 1–55Google Scholar
Luttrell, L, Acker, L, Urben, M and Reinhardt, V 1994 Training a large troop of rhesus macaques to co-operate during catching: Analysis of the time investment. Animal Welfare 3: 135–140. http://www.awionline.org/Lab_animals/biblio/aw5train.htmGoogle Scholar
Mann, WA, Welzel, G and Kinter, LB 1991 Determination of resting blood pressure in unrestrained cynomolgus monkeys using implanted telemetric transmitters. The Toxicologist 11: 335 (Abstract)Google Scholar
McKinley, J 2004 Training in a laboratory environment: Methods, effectiveness and welfare implications of two species of primate. Unpublished PhD thesis, University of Stirling, Scotland, UKGoogle Scholar
McKinley, J, Buchanan-Smith, HM, Bassett, L and Morris, K 2003 Training common marmosets (Callithrix jacchus) to co-operate during routine laboratory procedures: Ease of training and time investment. Journal of Applied Animal Welfare Science 6: 209–220CrossRefGoogle Scholar
Medical Research Council 2004 Best practice in the accommodation and care of primates used in scientific procedures. Medical Research Council: London, UK. http://www.mrc.ac.uk/Utilities/Documentrecord/index.htm?d=MRC002395Google Scholar
Mitchell, DS, Wigodsky, HS, Peel, HH and McCaffrey, TA 1980 Operant conditioning permits voluntary, non-invasive measurement of blood pressure in conscious unrestrained baboons (Papio cynocephalus). Behavior Research Methods and Instrumentation 12: 492–498CrossRefGoogle Scholar
Morrow-Tesch, JL, McGlone, JJ and Norman, RL 1993 Consequences of restraint stress on natural killer cell activity, behavior and hormone levels in rhesus macaques (Macaca mulatta). Psychoendocrinology 18: 383–395CrossRefGoogle ScholarPubMed
Moseley, JR and Davis, JA 1989 Psychological enrichment techniques and New World monkey restraint device reduce colony management time. Lab Animal 18: 31–33Google Scholar
National Research Council 1998 The Psychological Well-being of Nonhuman Primates. National Academy Press: Washington DC, USA. http://www.nap.edu/catalog/4909.html#tocGoogle Scholar
Prescott, MJ and Buchanan-Smith, HM 2003 Training non-human primates using positive reinforcement techniques: Guest editors' introduction. Journal of Applied Animal Welfare Science 6: 157–161Google Scholar
Prescott, MJ, Bowell, VA and Buchanan-Smith, HM 2005a Training laboratory-housed non-human primates, part 2: Resources for developing and implementing training programmes. Animal Technology and Welfare 4(3): 133–148Google Scholar
Prescott, MJ, Buchanan-Smith, HM and Rennie, A 2005b Training of laboratory-housed non-human primates in the UK. Anthrozoös 18(3): 288–303CrossRefGoogle Scholar
Pryor, K 2002 Don't Shoot the Dog: The new art of teaching and training, Revised Edition. Ringpress Books: Gloucestershire, UKGoogle Scholar
Reinhardt, V 1990 Avoiding undue stress: Catching individual animals in groups of laboratory rhesus monkeys. Lab Animal 19: 52–53. http://www.awionline.org/Lab_animals/biblio/la-avoid.htmGoogle Scholar
Reinhardt, V 1991 Impact of venipuncture on physiological research conducted in conscious macaques. Journal of Experimental Animal Science 34: 212–217. http://www.awionline.org/Lab_animals/biblio/es34-2~1.htmGoogle ScholarPubMed
Reinhardt, V 1992 Transport-cage training of caged rhesus macaques. Animal Technology 43: 57–61. http://www.awionline.org/Lab_animals/biblio/at57.htmGoogle Scholar
Reinhardt, V 1997 Training nonhuman primates to cooperate during handling procedures: A review. Animal Technology 48: 55–73. http://www.brown.edu/Research/Primate/lpn36-4.htmlGoogle Scholar
Reinhardt, V 2003 Working with rather than against macaques during blood collection. Journal of Applied Animal Welfare Science 6: 189–197. http://www.awionline.org/Lab_animals/biblio/jaaws11.htmlCrossRefGoogle ScholarPubMed
Reinhardt, V 2004 Common husbandry-related variables in bio-medical research with animals. Laboratory Animals 38: 213–235CrossRefGoogle Scholar
Reinhardt, V, Cowley, D, Scheffler, J, Vertein, R and Wegner, F 1990 Cortisol response of female rhesus monkeys to venipuncture in homecage versus venipuncture restraint apparatus. Journal of Medical Primatology 19: 601–606. http://www.awion-line.org/Lab_animals/biblio/jmp19.htmCrossRefGoogle ScholarPubMed
Reinhardt, V, Liss, C and Stephens, C 1995 Restraint methods of laboratory non-human primates: a review. Animal Welfare 4: 221–238CrossRefGoogle Scholar
Russell, WMS and Burch, RL 1959 The Principles of Humane Experimental Technique. Methuen: London, UK. http://altweb.jhsph.edu/publications/humane_exp/het-toc.htmGoogle Scholar
Sauceda, R and Schmidt, MG 2000 Refining macaque handling and restraint techniques. Lab Animal 29: 47–49Google Scholar
Savastano, G, Hanson, A and McCann, C 2003 The development of an operant conditioning training programme for New World primates at the Bronx Zoo. Journal of Applied Animal Welfare Science 6: 247–261CrossRefGoogle ScholarPubMed
Schapiro, SJ 2000 A few new developments in primate housing and husbandry. Scandinavian Journal of Laboratory Animal Science 27: 103–110. http://biomedicum.ut.ee/sjlas/27_2_103.pdfGoogle Scholar
Schapiro, SJ, Bloomsmith, MA and 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: 175–187CrossRefGoogle ScholarPubMed
Schapiro, SJ, Perlman, JE, Thiele, E and Lambeth, S 2005 Training nonhuman primates to perform behaviours useful in bio-medical research. Lab Animal 34: 37–42CrossRefGoogle Scholar
Scientific Committee on Animal Health and Welfare 2002 The Welfare on Non-Human Primates Used in Research. Health and Consumer Protection Directorate-General, European Commission: Brussels, Belgium. http://www.aisal.org/pages/doc_vari/out83_en.pdfGoogle Scholar
Schnell, CR and Gerber, P 1997 Training and remote monitoring of cardiovascular parameters in non-human primates. Primate Report 49: 61–70. http://www.awionline.org/Lab_animals/biblio/pr49-6~1.htm#Google Scholar
Scott, L 1990 Training non-human primates: meeting their behavioural needs. In: UFAW (ed) Animal training: A review and commentary pp 129–133. UFAW: Wheathampstead, Hertfordshire, UKGoogle Scholar
Scott, L 1991 Environmental enrichment for single housed common marmosets. In: Box, HO (ed) Primate Responses to Environmental Change pp 265–274. Chapman and Hall: London, UKCrossRefGoogle Scholar
Scott, L, Pearce, P, Fairhall, S, Muggleton, N and Smith, J 2003 Training nonhuman primates to cooperate with scientific procedures in applied biomedical research. Journal of Applied Animal Welfare Science 6: 199–207CrossRefGoogle ScholarPubMed
Smith, TE, McCallister, JM, Gordon, SJ and Whittikar, M 2004 Quantitative data on training New World primates to urinate. American Journal of Primatology 64: 83–93CrossRefGoogle ScholarPubMed
Swallow, J, Anderson, D, Buckwell, AC, Harris, T, Hawkins, P, Kirkwood, J, Lomas, M, Meacham, S, Peters, A, Owen, S, Prescott, M, Quest, R, Sutcliffe, R and Thompson, K 2005 Guidance for the transport of laboratory animals. Laboratory Animals 39: 1–39CrossRefGoogle ScholarPubMed
Videan, EN, Fritz, J, Murphy, J, Howell, S and Heward, CB 2005 Does training chimpanzees to present for injection lead to reduced stress? Laboratory Primate Newsletter 44: 1–2Google Scholar
Waitt, C, Buchanan-Smith, HM and Morris, K 2002 The effects of caretaker-primate relationships on primates in the laboratory. Journal of Applied Animal Welfare Science 5: 309–319CrossRefGoogle ScholarPubMed
Weiss, JM 1968 Effects of coping responses on stress. Journal of Comparative Physiology and Psychology 65: 251–260CrossRefGoogle ScholarPubMed
Wolfensohn, S and Honess, P 2005 Handbook of Primate Husbandry and Welfare. Blackwell Publishing Ltd: Oxford, UKCrossRefGoogle Scholar