Hostname: page-component-84b7d79bbc-l82ql Total loading time: 0 Render date: 2024-07-26T17:51:26.074Z Has data issue: false hasContentIssue false

Refinement of the use of non-human primates in scientific research. Part I: the influence of humans

Published online by Cambridge University Press:  11 January 2023

AE Rennie
Affiliation:
Department of Psychology, University of Stirling, Stirling FK9 4LA, Scotland, UK
HM Buchanan-Smith*
Affiliation:
Department of Psychology, University of Stirling, Stirling FK9 4LA, Scotland, UK
*
* Contact for correspondence and requests for reprints: h.m.buchanan-smith@stir.ac.uk

Abstract

The welfare of non-human primates used in scientific research must be safeguarded to promote scientific validity and for ethical reasons. Welfare can be improved by the refinement of practice, particularly if these refinements are applied to every aspect of the life of an animal used in the laboratory, from birth to death with the aim of both minimising harm and maximising well-being. Many refinement methods have been described in nationally and internationally accepted guidelines on laboratory practice, but awareness of these guidelines is not universal. In Part I of this review, we examine the influence of humans on non-human primates and summarise and evaluate methods of refinement that are or could be used to reduce suffering and improve welfare. In particular we focus on staff selection, education and training, human–animal bonds, staff communication, and training primates. In Parts II and III, refinements of housing, husbandry and experimental procedures are reviewed.

Type
Research Article
Copyright
© 2006 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

Anon 1997 The Experiments on Animals Act. The Hague, The NetherlandsGoogle Scholar
Arluke, A and Sanders, CR 1996 Regarding Animals. Temple University Press: Philadelphia, USAGoogle Scholar
Baker, KC 2004 Benefits of positive human interaction for socially housed chimpanzees. Animal Welfare 13: 239245CrossRefGoogle ScholarPubMed
Bassett, L and Buchanan-Smith, HM in press Effects of predictability on the welfare of captive animals. In: Swaisgood RR (ed) Animal Behaviour, Conservation and Enrichment. Applied Animal Behaviour ScienceGoogle Scholar
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: 221233CrossRefGoogle ScholarPubMed
Bayne, K 2002 Development of the human-research animal bond and its impact on animal well-being. Institute of Laboratory Animal Research Journal 43: 49Google ScholarPubMed
Bayne, KAL, Dexter, SL and Strange, GM 1993 The effects of food treat and provisioning and human interaction on the behavioural well-being of rhesus monkeys (Macaca mulatta). Contemporary Topics in Laboratory Animal Science 32: 69Google Scholar
Bloomsmith, MA, Baker, KC, Lambeth, SP, Ross, SK and Schapiro, SJ 2001 Is giving chimpanzees control over environmental enrichment a good idea? In: The Apes: Challenges for the 21st Century pp 8889. Chicago Zoological Society: Chicago, USAGoogle 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: 3536 (Abstract)Google 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, Laule, GE, Alford, PL and Thurston, RH 1994 Using training to moderate chimpanzee aggression during feeding. Zoo Biology 13: 557566CrossRefGoogle Scholar
Bloomsmith, MA, Stone, AM and Laule, GE 1998 Positive reinforcement training to enhance the voluntary movement of group-housed chimpanzees within their enclosures. Zoo Biology 17: 3333413.0.CO;2-A>CrossRefGoogle Scholar
Bowell, VA, Buchanan-Smith, HM and Morris, K 2005 Training marmosets to cooperate with aversive laboratory procedures. Primate Eye 86: 24Google Scholar
Box, HO 1991 Responsiveness to environmental change: interrelationships among parameters. In: Box, HO (ed) Primate Responses to Environmental Change pp 5774. Chapman and Hall: London, UKCrossRefGoogle Scholar
Buchanan-Smith, HM, Rennie, AE, Vitale, A, Pollo, S, Prescott, MJ and Morton, DB 2005 Harmonising the definition of refinement. Animal Welfare 14: 379384CrossRefGoogle Scholar
Chang, FT and Hart, LA 2002 Human-animal bonds in the laboratory: how animal behavior affects the perspective of care-givers. Institute of Laboratory Animal Research Journal 43: 1018Google Scholar
Colahan, H and Breder, C 2003 Primate training at Disney's Animal Kingdom. Journal of Applied Animal Welfare Science 6: 235246CrossRefGoogle ScholarPubMed
Crofts, HS, Muggleton, NG, Bowditch, AP, Pearce, PC, Nutt, DJ and Scott, EAM 1999 Home cage presentation of complex discrimination tasks to marmosets and rhesus monkeys. Laboratory Animals 33: 207214CrossRefGoogle ScholarPubMed
Cross, N, Pines, MK and Rogers, LJ 2004 Saliva sampling to assess cortisol levels in unrestrained common marmosets and the effects of behavioural stress. American Journal of Primatology 62: 107114CrossRefGoogle Scholar
Davis, H 2002 Prediction and preparation: Pavlovian implications of research animals discriminating among humans. Institute of Laboratory Animal Research Journal 43: 1926Google ScholarPubMed
Desmond, T and Laule, G 1994 Use of positive reinforcement training in the management of species for reproduction. Zoo Biology 13: 471477CrossRefGoogle Scholar
European Commission (EC) 2002 The Welfare of Non-Human Primates used in Research. Scientific Committee on Animal Health and Animal Welfare, European CommissionGoogle Scholar
European Union (EU) 1986 Council Directive 86/609/EEC. Paris, FranceGoogle Scholar
Garcia, J and Koelling, RA 1966 Relation of cue to consequence in avoidance learning. Psychonomic Science 4: 123124CrossRefGoogle Scholar
Hart, LA 1996 The human/animal relationship in the research setting. In: Krulisch, L, Mayer, S and Simmonds, RC (eds) The Human/Research Animal Relationship pp 2534. Scientists Centre for Animal Welfare: Maryland, USAGoogle Scholar
Hau, J 1999 Humane endpoints and the importance of training. In: Hendriksen, CFM and Morton, DB (eds) Humane Endpoints in Animals Experiments for Biomedical Research pp 7174. Proceedings of the International Conference. Royal Society of Medicine Press: London, UKGoogle Scholar
Heath, M 1989 The training of cynomolgus monkeys and how the human/animal relationship improves with environmental and mental enrichment. Animal Technology 40: 1122Google Scholar
Herzog, H 2002 Ethical aspects of relationships between humans and research animals. Institute of Laboratory Animal Research Journal 43: 2732Google ScholarPubMed
Home Office 1986a Animals (Scientific Procedures) Act 1986. London, UKGoogle Scholar
Home Office 1986b Code of Practice for the Housing of Animals in Designated Breeding and Supplying Establishments. HMSO: Cambridge, UKGoogle Scholar
International Primatological Society (IPS) 1993 IPS International Guidelines for the Acquisition, Care and Breeding of Non-Human Primates. Poole TB and Schwibbe M (eds). Erich Goltze GmbH and Co: KG, Gottingen, GermanyGoogle Scholar
Kiley-Worthington, M 1990 Animals in Circuses and Zoos: Chiron's World? Little Eco-Farms Publishing: Essex, UKGoogle Scholar
Klein, HJ and Murray, KA 1995 Restraint. In: Bennett BT (ed) Non-Human Primates in Biomedical Research pp. 286-297. Academic Press: San Diego, USACrossRefGoogle Scholar
Laule, G 1993 The use of behavioral management techniques to reduce or eliminate abnormal behavior. Animal Welfare Information Centre Newsletter 4: 12, 8-11Google Scholar
Laule, G 1999 Training laboratory animals. In: Poole, T (ed) The UFAW Handbook on the Care and Management of Laboratory Animals pp 2127. Blackwell Science Ltd: Oxon, UKGoogle Scholar
Laule, G and Desmond, T 1998 Positive reinforcement training as an enrichment strategy. In: Sheperdson, DH, Mellen, JD and Hutchins, M (eds) Second Nature: Environmental Enrichment for Captive Animals pp 302313. Smithsonian Institute Press: Washington DC, USAGoogle 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: 5875913.0.CO;2-7>CrossRefGoogle Scholar
Luttrell, L, Acker, L, Urben, M and Reinhardt, V 1994 Training a large troop of rhesus macaques to cooperate during catching: analysis of the time investment. Animal Welfare 3: 135140CrossRefGoogle Scholar
Lutz, CK, Tiefenbacher, S, Jorgensen, MJ, Meyer, JS and Novak, MA 2000 Techniques for collecting saliva from awake, unrestrained, adult monkeys for cortisol assay. American Journal of Primatology 52: 93993.0.CO;2-B>CrossRefGoogle ScholarPubMed
Markowitz, H 1982 Behavioral Enrichment in the Zoo. Van Nostrand Reinhold, New York, USAGoogle Scholar
Markowitz, H and Line, S 1989 Primate research models and environmental enrichment. In: Segal, EF (ed) Housing, Care and Psychological Well-being of Captive and Laboratory Primates pp 203212. Noyes Publications Inc: New Jersey, USAGoogle Scholar
Mason, GJ 1991 Stereotypies and suffering. Behavioural Processes 25: 103115CrossRefGoogle ScholarPubMed
Mason, G and Mendl, M 1993 Why is there no simple way of measuring animal welfare? Animal Welfare 2: 301319CrossRefGoogle Scholar
McKinley, J 2004 Training in a Laboratory Environment: Methods, Effectiveness and Welfare Implications for Two Species of Primate. Unpublished PhD Thesis, University of Stirling, UKGoogle Scholar
McKinley, J, Buchanan-Smith, HM, Bassett, L and Morris, K 2003 Training common marmosets (Callithrix jacchus) to cooperate during routine laboratory procedures: ease of training and time investment. Journal of Applied Animal Welfare Science 6: 209220CrossRefGoogle ScholarPubMed
Moseley, JR and Davis, JA 1989 Psychological enrichment techniques and new world monkey restraint device reduce colony management time. Laboratory Animals 18: 3133Google Scholar
Nevalainen, T, Berge, E, Gallix, P, Jilge, B, Melloni, E, Thomann, P, Waynforth, B, van Zutphen, LFM 1999 FELASA guidelines for education of specialists in laboratory animal science. Laboratory Animals 33: 115CrossRefGoogle ScholarPubMed
Nevalainen, T, Dontas, I, Forslid, A, Howard, BR, Klusa, V, Kaserman, HP, Melloni, E, Nebendahl, K, Stafleu, FR, Vergara, P and Verstegen, J 2000 FELASA recommendations for the education and training of persons carrying out animal experiments (Category B). Laboratory Animals 34: 229235CrossRefGoogle ScholarPubMed
Petto, A, Russell, K, Watson, L and Lareau-Alves, M 1992 Promoting psychological well-being in a biomedical research facility: sheep in wolves' clothing. Humane Innovations and Alternatives 6: 366370Google Scholar
Philipp, C 1995 Operant conditioning with the great apes. Proceedings of the National Conference of the American Association of Zoo Keepers 22: 156163Google Scholar
Philipp, C, Breder, C and MacPhee, M 2001 Maternal care and infant training of a western lowland gorilla (Gorilla gorilla gorilla). In: The Apes: Challenges for the 21st Century pp 135136. Chicago Zoological Society: Chicago, USAGoogle Scholar
Phillippi-Falkenstein, K and Clarke, MR 1992 Procedure for training corral-living rhesus-monkeys for fecal and blood-sample collection. Laboratory Animal Science 42: 8385Google ScholarPubMed
Poole, T 1999 The UFAW Handbook on the Care and Management of Laboratory Animals. Blackwell Science Ltd: Oxon, UKGoogle Scholar
Poole, T, Hubrecht, R and Kirkwood, JK 1999 Marmosets and tamarins. In: Poole, T (ed) The UFAW Handbook on the Care and Management of Laboratory Animals pp 559574. Blackwell Science Ltd: Oxon, UKGoogle Scholar
Prescott, M J and Buchanan-Smith, H M 1999 Intra- and inter-specific stimulus enhancement in two species of tamarin. International Journal of Comparative Psychology 12: 7192CrossRefGoogle Scholar
Prescott, MJ and Buchanan-Smith, HM 2003 Training nonhuman primates using positive reinforcement techniques. Journal of Applied Animal Welfare Science 6: 157162CrossRefGoogle ScholarPubMed
Prescott, MJ, Buchanan-Smith, HM and Rennie, AE 2005 Training of laboratory-housed non-human primates in the UK. Anthrozoos 18: 288303.CrossRefGoogle Scholar
Priest, GM 1990 The use of operant conditioning to facilitate better care for captive exotic animals. In: Proceedings of the American Association of 16th Zoo Keepers. pp 94-108 National Conference, Louisiana, USAGoogle Scholar
Priest, GM 1991 Training a diabetic drill (Mandrillus leucophaeus) to accept insulin injections and venipuncture. Laboratory Primate Newsletter 30: 14Google Scholar
Reinhardt, V 1991 Training adult male rhesus monkeys to actively cooperate during in-homecage venipuncture. Animal Technology 42: 1117Google Scholar
Reinhardt, V 1992a Improved handling of experimental rhesus monkeys. In: Davis, H and Balfour, AD (eds) The Inevitable Bond: Examining Scientist-Animal Interactions pp 171177. Cambridge University Press: Cambridge, UKGoogle Scholar
Reinhardt, V 1992b Voluntary progression order in captive rhesus macaques. Zoo Biology 11: 6166CrossRefGoogle Scholar
Reinhardt, V 1997a Refining the traditional housing and handling of laboratory rhesus macaques improves scientific methodology. Primate Report 49: 93112Google Scholar
Reinhardt, V 1997b Training non-human primates to cooperate during blood collection: a review. Animal Technologist 48: 5573Google Scholar
Reinhardt, V 2002 The myth of the aggressive monkey. Journal of Applied Animal Welfare Science 5: 321330CrossRefGoogle ScholarPubMed
Reinhardt, V 2003 Working with rather than against macaques during blood collection. Journal of Applied Animal Welfare Science 6: 189198CrossRefGoogle ScholarPubMed
Reinhardt, V and Cowley, D 1991 Training stumptailed monkeys (Macaca arctoides) to cooperate during in-homecage treatment. Laboratory Primate Newsletter 29: 910Google Scholar
Reinhardt, V, Liss, C and Stevens, C 1995 Restraint methods of laboratory non-human primates: a critical review. Animal Welfare 4: 221238CrossRefGoogle Scholar
Rennie, AE and Buchanan-Smith, HM 2005 Report on the extent and character of primate use in scientific procedures across Europe in 2001. Laboratory Primate Newsletter 44: 612Google Scholar
Rennie, AE and Buchanan-Smith, HM 2006 Refinement of the use of non-human primates in scientific research. Part III: refinement of procedures. Animal Welfare 15: 239261CrossRefGoogle Scholar
Roder, EL and Timmermans, PJA 2002 Housing and care of monkeys and apes in laboratories: adaptations allowing essential species-specific behaviour. Laboratory Animals 36: 221242CrossRefGoogle ScholarPubMed
Roper, TJ 1983 Learning as a biological phenomenon. In: Halliday, TR and Slater, PJB (eds) Animal Behaviour: Genes, Development and Learning pp 178212. Blackwell Science Publications: Oxford, UKGoogle Scholar
Russell, WMS and Burch, RL 1992 The Principles of Humane Experimental Technique. Universities Federation for Animal Welfare: Herts, UKGoogle Scholar
Sands, SF and Wright, AA 1982 Monkey and human pictorial memory scanning. Science 216: 13331334CrossRefGoogle ScholarPubMed
Savastano, G, Hanson, A and McCann, C 2003 The development of an operant conditioning training program for the New World primates at the Bronx zoo. Journal of Applied Animal Welfare Science 6: 247261CrossRefGoogle ScholarPubMed
Schapiro, SJ 2000 A few new developments in primate housing and husbandry. Scandinavian Journal of Laboratory Animal Science 27: 103110Google Scholar
Schapiro, SJ, Bloomsmith, MA and Laule, GE 2003 Positive reinforcement training as a technique to alter non-human primate behavior: Quantitative assessments of effectiveness. Journal of Applied Animal Welfare Science 6: 175188CrossRefGoogle Scholar
Schapiro, SJ, Perlman, JE and Boudreau, BA 2001 Manipulating the affiliative interactions of group-housed rhesus macaques using positive reinforcement training techniques. American Journal of Primatology 55: 137149CrossRefGoogle ScholarPubMed
Schapiro, SJ, Perlman, JE, Thiele, E and Lambeth, S 2005 Training nonhuman primates to perform behaviours useful in bio-medical research. Laboratory Animal Europe 5: 1926Google Scholar
Schnell, C R and Gerber, P 1997 Training and remote monitoring of cardiovascular parameters in non-human primates. Primate Report 49: 6170Google Scholar
Scott, L 1990 Training non-human primates: meeting their behavioural needs. In: UFAW (ed) Animal Training: A Review and Commentary pp 129133. Universities Federation for Animal Welfare: Herts, UKGoogle Scholar
Scott, L 1991 Environmental enrichment for single housed common marmosets. In: Box, HO (ed) Primate Responses to Environmental Change pp 265274. Chapman and Hall: London, UKCrossRefGoogle Scholar
Scott, L, Pearce, P, Fairhall, S, Muggleton, N and Smith, J 2003 Training nonhuman primates to co-operate with scientific procedures in applied biomedical research. Journal of Applied Animal Welfare Science 6: 199208CrossRefGoogle Scholar
Segal, EF 1989 Housing, Care and Psychological Well-Being of Captive and Laboratory Primates. Noyes Publications: New Jersey, USAGoogle Scholar
Smith, JA and Boyd, KM 2002 The Use of Non-human Primates in Research and Testing. The British Psychological Society Scientific Affairs Board Standing Advisory Committee on The Welfare of Animals in Psychology: Leicester, UKGoogle Scholar
Smith, TE, McGreer-Whitworth, B and French, JA 1998 Close proximity of the heterosexual partner reduces the physiological and behavioral consequences of novel-cage housing in black tufted-ear marmosets (Callithrix kuhli). Hormones and Behavior 34: 211222CrossRefGoogle ScholarPubMed
The Biological Council Animal Research & Welfare Panel 1992 Guidelines on the Handling and Training of Laboratory Animals. Universities Federation for Animal Welfare: Herts, UKGoogle Scholar
Stone, AM, Bloomsmith, MA, Laule, GE and Alford, PL 1994 Documenting positive reinforcement training for chimpanzee urine collection. American Journal of Primatology 33: 242Google Scholar
Videan, EN, Fritz, J, Murphy, J, Borman, R, Howell, S and Heward, CB 2005a Does training chimpanzees to present for injection lead to reduced stress? Laboratory Primate Newsletter 44: 12Google Scholar
Videan, EN, Fritz, J, Murphy, J, Borman, R, Smith, HF and Howell, S 2005b Training captive chimpanzees to cooperate for an anaesthetic injection. Laboratory Animal Europe 5: 2834Google Scholar
Visalberghi, E and Anderson, JR 1999 Capuchin monkeys. In: Poole, T (ed) The UFAW Handbook on the Care and Management of Laboratory Animals pp 601610. Blackwell Science Ltd: Oxon, UKGoogle Scholar
Waitt, C, and 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: 309319CrossRefGoogle ScholarPubMed
Weiss, JM 1968 Effects of coping response on stress. Journal of Comparative Physiology and Psychology 65: 251260Google ScholarPubMed
Wilson, MS, Berge, E, Maess, J, Mahouy, G, Natoff, I, Nevalainen, T, Van Zutphen, LFM, Zaninelli, P, Fosse, RT, Bonnod, J, Hau, J, Leyten, R, O'Donoghue, PN, Sabourdy, M, Schwartz, K and Thomann, P 1995 FELASA recommendations on the education and training of persons working with laboratory animals: category A and category C reports of the Federation-of-European-Laboratory-Animal-Science-Associations Working Group on Education accepted by the FELASA Board of Management. Laboratory Animals 29: 121131Google Scholar
Wolfle, TL 2002 Introduction. Institute of Laboratory Animal Research Journal 43: 13Google Scholar
Wolfensohn, S and Honess, P 2005 Handbook of Primate Husbandry and Welfare. Blackwell, Oxford, UKCrossRefGoogle Scholar
Young, RJ and Cipreste, CF 2004 Applying animal learning theory: training captive animals to comply with veterinary and husbandry procedures. Animal Welfare 13: 225232CrossRefGoogle Scholar