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Cage sizes for tamarins in the laboratory

Published online by Cambridge University Press:  11 January 2023

MJ Prescott*
Affiliation:
Research Animals Department, Royal Society for the Prevention of Cruelty to Animals, Wilberforce Way, Southwater, Horsham, West Sussex RHI3 9RS, UK
HM Buchanan-Smith
Affiliation:
Department of Psychology, University of Stirling, Stirling FK9 4LA, UK
*
* Contact for correspondence and requests for reprints: [email protected]

Abstract

Provision of adequate space for captive animals is essential for good welfare. It affects not only their behaviour but also determines whether there is sufficient room for appropriate environmental enrichment. Most importantly, appropriate cage size permits captive animals to be housed in socially harmonious groups and to fulfil their reproductive potential. For animals used in the laboratory, the environment can be an additional source of suffering and distress. If they can be better housed and cared for to reduce the overall impact of experiments upon them, then we are obliged to do so for ethical, legal and scientific reasons. Practically all current guidelines specify minimum cage sizes for laboratory primates based on unit body weight. We believe that no single factor is sufficient to determine minimum cage sizes for primates, and that instead a suite of characteristics should be used, including morphometric, ecological, social and behavioural characteristics. Here we explore the relevant differences between tamarins (Saguinus labiatus and S. oedipus) and marmosets (Callithrix jacchus) that have a bearing on setting minimum cage sizes. These include: body size; arboreality and cage use; home range size, mean daily path length and stereotypic behaviour; breeding success in the laboratory; and species predisposition and aggression. We conclude that it is even more important to provide tamarins with a good quantity of space in the laboratory than it is marmosets if well-being and breeding success are to be maximised.

Type
Research Article
Copyright
© 2004 Universities Federation for Animal Welfare

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References

Alonso, C and Langguth, A 1989 Ecology and behavior of Callithrix jacchus (Primates: Callitrichidae) living on an Atlantic forest island. Revista Nordestina de Biologia 6: 105137Google Scholar
Bardi, M and Petto, A J 1999 Parental care in captive common marmosets (Callithrix jacchus) and cotton-top tamarins (Saguinus oedipus). American Journal of Primatology 49: 3132 (Abstract)Google Scholar
Bardi, M and Petto, A J 2002 Parental failure in captive common marmosets (Callithrix jacchus): a comparison with tamarins. Folia Primatologica 73: 4648CrossRefGoogle ScholarPubMed
Bardi, M, Petto, A J and Lee-Parritz, D E 2001 Parental failure in captive cotton-top tamarins (Saguinus oedipus). American Journal of Primatology 54: 159169CrossRefGoogle ScholarPubMed
Berkson, G, Goodrich, J and Kraft, I 1966 Abnormal stereotyped movements of marmosets. Perceptual and Motor Skills 23: 491 -498CrossRefGoogle Scholar
Box, H O 1977 Social interactions in family groups of captive marmosets (Callithrixjacchus). In: Kleiman, D G (ed) The Biology and Conservation of the Callitrichidae pp 239249. Smithsonian Institution Press: Washington, DC, USAGoogle Scholar
Box, H O 1988 Behavioural responses to environmental change. Observations on captive marmosets and tamarins. Animal Technology 39: 916Google Scholar
Box, H O 1995 Biological propensities of the Callitrichidae: a much used — little known group. Laboratory Animals 29: 237243CrossRefGoogle ScholarPubMed
Box, H O 1997 Callitrichid social biology and its significance for captive management. In: Pryce C, Scott L and Schnell C (eds) Marmosets and Tamarins in Biological and Biomedical Research: Proceedings of a Workshop Organised by the European Marmoset Research Group pp 111118. DSSD Imagery: Salisbury, UKGoogle Scholar
Box, H O and Hubrecht, R C 1987 Long-term data on the reproduction and maintenance of a colony of common marmosets (Callithrix jacchus jacchus) 1972-1983. Laboratory Animals 21: 249260CrossRefGoogle ScholarPubMed
Box, H O and Rohrhuber, B 1993 Differences in behaviour among adult male, female pairs of cotton-top tamarins (Saguinus oedipus) in different conditions of housing. Animal Technology 44: 1930Google Scholar
Brand, H M 1981 Husbandry and breeding of a newly established colony of cotton-topped tamarins (Saguinus oedipus oedipus). Laboratory Animals 15: 711CrossRefGoogle ScholarPubMed
Bruhin, H 1979 Callithrix jacchus, marmoset: new lab animal, review. Zeitschrift Fuer Versuchstierkunde 21: 209221Google Scholar
Buchanan-Smith, H M 1991 A field study on the red-bellied tamarin, Saguinus l. labiatus, in Bolivia. International Journal of Primatology 12: 259276CrossRefGoogle Scholar
Buchanan-Smith, H M 2001 Species-specific housing and husbandry for marmosets and tamarins (Callitrichinae). In: Hare, V J, Worley, K E and Myers, K (eds) Proceedings of the 4th International Conference on Environmental Enrichment pp 95105. The Shape of Enrichment: San Diego, USAGoogle Scholar
Buchanan-Smith, H M, Shand, C and Morris, K 2002 Cage use and feeding height preferences of captive common marmosets (Callithrix jacchus) in two-tier cages. Journal of Applied Animal Welfare Science 5: 139149CrossRefGoogle ScholarPubMed
Caine, N G 1993 Flexibility and co-operation as unifying themes in Saguinus social organization and behaviour: the role of predation pressures. In: Rylands A B (ed) Marmosets and Tamarins: Systematics, Behaviour, and Ecology pp 200219. Oxford University Press: Oxford, UKGoogle Scholar
Caine N G and O'Boyle V J Jr 1992 Cage design and forms of play in red-bellied tamarins, Saguinus labiatus. Zoo Biology II: 215220CrossRefGoogle Scholar
Caine, N G, Potter, MP and Mayer, K E 1992 Sleeping site selection by captive tamarins (Saguinus labiatus). Ethology 90: 6371CrossRefGoogle Scholar
Carroll, J B 1997 A comparative summary of the nutritional adaptations and needs of callitrichids and application to captive management. In: Pryce C, Scott L and Schnell C (eds) Marmosets and Tamarins in Biological and Biomedical Research: Proceedings of a Workshop Organised by the European Marmoset Research Group pp 7077. DSSD Imagery: Salisbury, UKGoogle Scholar
Chamove, A S 1989a Assessing the welfare of captive primates — a critique. Laboratory Animal Welfare Research — Primates: Proceedings of a Symposium Organised by Universities Federation for Animal Welfare pp 3949. Universities Federation for Animal Welfare: Wheathampstead, Hertfordshire, UKGoogle Scholar
Chamove, A S 1989b Environmental enrichment: a review. Animal Technology 40: 155178Google Scholar
Chamove, A S and Anderson, J R 1989 Examining environmental enrichment. In: Segal, E F (ed) Housing, Care and Psychological Well-being of Captive and Laboratory Primates pp 183202. Noyes Publications: Park Ridge, New Jersey, USAGoogle Scholar
Chamove, A S and Rohrhuber, B 1989 Moving callitrichid monkeys from cages to outside areas. Zoo Biology 8: 151163CrossRefGoogle Scholar
Clarke, J M 1994 The common marmoset, Callithrix jacchus. ANZCCART News 7: 18Google Scholar
Cleveland, J and Snowdon, C T 1984 Social development during the first twenty weeks in the cotton-top tamarin (Saguinus o. oedipus). Animal Behaviour 32: 432444CrossRefGoogle Scholar
Clubb, R and Mason, G 2003 Captivity effects on wide-ranging carnivores. Nature 425: 473474CrossRefGoogle ScholarPubMed
Council of Europe 1986 European Convention for the Protection of Vertebrate Animals Used for Experimental and Other Scientific Purposes, ETS No. 123. Council of Europe: Strasbourg, FranceGoogle Scholar
Draper, W A and Bernstein, I S 1963 Stereotyped behaviour and cage size. Perceptual and Motor Skills 16: 231234CrossRefGoogle Scholar
Ely, A, Freer, A, Windle, C and Ridley, R M 1998 Assessment of cage use by laboratory-bred common marmosets (Callithrix jacchus). Laboratory Animals 32: 427433CrossRefGoogle ScholarPubMed
Epple, G 1967 Comparative investigation of the sexual and social behavior of marmosets (Hapalidae). Folia Primatologica 7: 3765CrossRefGoogle Scholar
Erwin, J 1977 Factors influencing aggressive behavior and risk of trauma in the pigtail macaque (Macaca nemestrina). Laboratory Animal Science 27: 541547Google ScholarPubMed
European Community 1986 Council Directive 86/609/EEC on the Approximation of Laws, Regulations and Administrative Provisions of the Member States Regarding the Protection of Animals Used for Experimental and Other Scientific Purposes. Official Journal of the European Communities L358.Google Scholar
Evans, S 1984 Captive management of marmosets and tamarins. In: Laboratory Animal Science Association and Universities Federation for Animal Welfare (eds) Standards in Laboratory Animal Management pp 250252. Universities Federation for Animal Welfare: Wheathampstead, Hertfordshire, UKGoogle Scholar
Ferrari, S F 1993 Ecological differentiation in the Callitrichidae. In: Rylands A B (ed) Marmosets and Tamarins: Systematics, Behaviour, and Ecology pp 314328. Oxford University Press: Oxford, UKGoogle Scholar
Ferrari, S F and Lopes Ferrari, M A 1989 A re-evaluation of the social organization of the Callitrichidae, with reference to the ecological differences between genera. Folia Primatologica 52: 132147CrossRefGoogle Scholar
Garber, P A 1993 Feeding ecology and behaviour of the genus Saguinus. In: Rylands A B (ed) Marmosets and Tamarins: Systematics, Behaviour, and Ecology pp 273295. Oxford University Press: Oxford, UKGoogle Scholar
Gaspari, F, Perretta, G and Schino, G 2000 Effects of different housing systems on the behaviour of the common marmoset (Callithrix jacchus). Folia Primatologica 71: 291Google Scholar
Glatston, A R, Geilvoet-Soeteman, E, Hora-Pecek, E and van Hooff, J A R A M 1984 The influence of the zoo environment on social behavior of groups of cotton-topped tamarins (Saguinus oedipus oedipus). Zoo Biology 3: 241253CrossRefGoogle Scholar
Hampton, J K Jr, Hampton, S H and Landwehr, B T 1966 Observations on a successful breeding colony of the marmoset, Oedipomidas oedipus. Folia Primatologica 4: 265287CrossRefGoogle ScholarPubMed
Hearn, J P, Abbott, D H, Chambers, P C, Hodges, J K and Lunn, S F 1978 Use of the common marmoset, Callithrix jacchus, in reproductive research. Primates in Medicine 10: 4049Google ScholarPubMed
Hershkovitz, P 1977 Living New World Monkeys (Platyrrhini), with an Introduction to Primates, Volume I. University of Chicago Press: Chicago, USAGoogle Scholar
Home Office 1989 Code of Practice for the Housing and Care of Animals Used in Scientific Procedures. Her Majesty's Stationery Office: London, UKGoogle Scholar
Home Office 1995 Code of Practice for the Housing and Care of Animals in Designated Breeding and Supplying Establishments. Her Majesty's Stationery Office: London, UKGoogle Scholar
Hubrecht, R C 1985 Home-range size and use and territorial behavior in the common marmoset, Callithrix jacchus jacchus, at the Tapacura Field Station, Recife, Brazil. International Journal of Primatology 6: 533550CrossRefGoogle Scholar
Hubrecht, R C 1995 Housing, Husbandry and Welfare Provision for Animals Used in Toxicology Studies: Results of a UK Questionnaire on Current Practice (1994). Universities Federation for Animal Welfare: Wheathampstead, Hertfordshire, UKGoogle Scholar
Ingram, J C 1977 Parent-infant interactions in the common marmoset (Callithrix jacchus). In: Kleiman, D G (ed) The Biology and Conservation of the Callitrichidae pp 281297. Smithsonian Institution Press: Washington, DC, USAGoogle Scholar
Institute of Laboratory Animal Resources 1996 Guide for the Care and Use of Laboratory Animals. National Academy Press: Washington, DC, USAGoogle Scholar
International Primatological Society 1993 IPS International guidelines for the acquisition, care and breeding of nonhuman primates. Primate Report 35 (Special issue)Google Scholar
Izawa, K 1975 Foods and feeding behavior of monkeys in the upper Amazon basin. Primates 16: 295316CrossRefGoogle Scholar
Kerl, J and Rothe, H 1996 Influence of cage size and cage equipment on physiology and behavior of common marmosets (Callithrix jacchus). Laboratory Primate Newsletter 35: 1013Google Scholar
Kilborn, J A, Sehgal, P, Johnson, L D, Beland, M and Bronson, R T 1983 A retrospective study of infant mortality of cotton-top tamarins (Saguinus oedipus) in captive breeding. Laboratory Animal Science 33: 168171Google ScholarPubMed
Kingston, W R 1969 Marmosets and tamarins. Laboratory Animal Handbooks 4: 243250Google Scholar
Kingston, W R 1975 The breeding of endangered species of marmosets and tamarins. In: Martin, R D (ed) Breeding Endangered Species in Captivity pp 213222. Academic Press: London, UKGoogle Scholar
Kirkwood, J K, Epstein, M A and Terlecki, A J 1983 Factors influencing population growth of a colony of cotton-top tamarins. Laboratory Animals 17: 3541CrossRefGoogle ScholarPubMed
Kirkwood, J K and Stathatos, K 1992 Biology, Rearing, and Care of Young Primates. Oxford University Press: Oxford, UKGoogle Scholar
Kitchen, A M and Martin, A A 1996 The effects of cage size and complexity on the behaviour of captive common marmosets, Callithrix jacchus jacchus. Laboratory Animals 30: 317326Google ScholarPubMed
Maier, W, Alonso, C and Langguth, A 1982 Field observations on Callithrix jacchus jacchus L. Zeitschrift Fuer Saeugetierkunde 47: 334346Google Scholar
Maninger, N, Kim, J H and Ruppenthal, G C 1998 The presence of visual barriers decreases agonism in group housed pigtail macaques (Macaca nemestrina). American Journal of Primatology 45: 193194Google Scholar
McGrew, W C and Webster, J 1995 Birth seasonality in cotton-top tamarins (Saguinus oedipus) despite constant food supply and body weight. Primates 36: 241248CrossRefGoogle Scholar
McKenzie, S M, Chamove, A S and Feistner, A T C 1986 Floor-coverings and hanging screens alter arboreal monkey behaviour. Zoo Biology 5: 339348CrossRefGoogle Scholar
Molzen, E M and French, J A 1989 The problems of foraging in captive callitrichid primates: behavioral time budgets and foraging skills. In: Segal, E F (ed) Housing, Care and Psychological Well-being of Captive and Laboratory Primates pp 89101. Noyes Publications: Park Ridge, New Jersey, USAGoogle Scholar
National Research Council 1998 The Psychological Well-Being of Nonhuman Primates: A Report of the Committee on Well-Being of Nonhuman Primates. National Academy Press: Washington, DC, USAGoogle Scholar
Neyman, P F 1977 Aspects of the ecology and social organization of free-ranging cotton-top tamarins (Saguinus oedipus) and the conservation status of the species. In: Kleiman, D G (ed) The Biology and Conservation of the Callitrichidae pp 3971. Smithsonian Institution Press: Washington, DC, USAGoogle Scholar
Neyman, P F 1980 Ecology and social organization of the cotton-top tamarin. PhD Thesis, University of California, Berkeley, USAGoogle Scholar
Ogden, J D and Wolfe, L G 1979 Reproduction of wild-caught marmosets (Saguinus labiatus labiatus) under laboratory conditions. Laboratory Animal Science 29: 545546Google ScholarPubMed
Paulk, H H, Dienske, H and Ribbens, L G 1977 Abnormal behavior in relation to cage size in rhesus monkeys. Journal of Abnormal Psychology 86: 8792CrossRefGoogle ScholarPubMed
Peres, C A 1992 Consequences of joint-territoriality in a mixed-species group of tamarin monkeys. Behaviour 123: 220246CrossRefGoogle Scholar
Pook, A G and Pook, G 1982 Polyspecific association between Saguinus fuscicollis, Saguinus labiatus, Callimico goeldii and other primates in north-western Bolivia. Folia Primatologica 38: 196216CrossRefGoogle ScholarPubMed
Poole, T B 1988 Normal and abnormal behaviour in captive primates. Primate Report 22: 312Google Scholar
Poole, T B and Evans, R G 1982 Reproduction, infant survival and productivity of a colony of common marmosets (Callithrix jacchus jacchus). Laboratory Animals 16: 8897CrossRefGoogle ScholarPubMed
Poole, T B, Costa, P, Netto, W J, Schwartz, K, Wechsler, B and Whittaker, D 1994 Non-human primates. In: O'Donoghue P N (ed) The Accommodation of Laboratory Animals in Accordance with Animal Welfare Requirements. Proceedings of an International Workshop held at Bundesgesundheitsamt, Berlin, 17-19th May 1993 pp 81-86. Bundesministerium für Ernährung, Landwirtshaft und Forsten: Bonn, GermanyGoogle Scholar
Poole, T, Hubrecht, R and Kirkwood, J K 1999 Marmosets and tamarins. In: Poole T and English P (eds) The UFAW Handbook on the Care and Management of Laboratory Animals, 7th Edition, Volume 1: Terrestrial Vertebrates pp 559-573. Blackwell Science: Oxford, UKGoogle Scholar
Poole, T and Thomas, A W 1995 Primate Vaccine Evaluation Network: Recommendations, Guidelines and Information for Biomedical Research Involving Non-Human Primates with Emphasis on Health Problems of Developing Countries. European Commission DG-XII: Brussels, BelgiumGoogle Scholar
Prescott, M J and Buchanan-Smith, H M 2002 Predation sensitive foraging in captive tamarins. In: Miller, L (ed) Eat or Be Eaten: Predation Sensitive Foraging Among Primates pp 4457. Cambridge University Press: Cambridge, UKCrossRefGoogle ScholarPubMed
Price, E C and McGrew, W C 1990 Cotton-top tamarins (Saguinus (o.) oedipus) in a semi-naturalistic captive colony. American Journal of Primatology 20: 112Google Scholar
Reinhardt, V and Reinhardt, A 1991 Impact of a privacy panel on the behaviour of caged female rhesus monkeys living in pairs. Journal of Experimental Animal Science 34: 5558Google ScholarPubMed
Reinhardt, V and Reinhardt, A 2001 Legal space requirement stipulations for animals in the laboratory: are they adequate? Journal of Applied Animal Welfare Science 4: 143149CrossRefGoogle Scholar
Ross, C 1988 The intrinsic rate of natural increase and reproductive effort in primates. Journal of Zoology 214: 199219CrossRefGoogle Scholar
Royal Society/Universities Federation for Animal Welfare 1987 Guidelines on the Care of Laboratory Animals and their Use for Scientific Purposes: 1. Housing and Care. The Royal Society and the Universities Federation for Animal Welfare: London, UKGoogle Scholar
Savage, A 1990 The reproductive biology of the cotton-top tamarin (Saguinus oedipus oedipus) in Colombia. Dissertation Abstracts International B51(4)Google Scholar
Savage, A 1995 The Cotton-Top Tamarin SSP Husbandry Manual. Available at: http://www.csew.com/cottontop/Google Scholar
Savage, A, Giraldo, L H, Blumer, E S, Soto, L H, Burger, W and Snowdon, C T 1993 Field techniques for monitoring cotton-top tamarins (Saguinus oedipus oedipus) in Colombia. American Journal of Primatology 31: 189196CrossRefGoogle ScholarPubMed
Scanlon, C E, Chalmers, N R and Monteiro da Cruz, M A O 1989 Home range use and the exploitation of gum in the marmoset Callithrix jacchus jacchus. International Journal of Primatology 10: 123136Google Scholar
Schoenfeld, D 1989 Effects of environmental impoverishment on the social behavior of marmosets (Callithrix jacchus). American Journal of Primatology (Supplement 1): 4551Google Scholar
Scullion, F T 1987 Husbandry, breeding and maintenance of a viable population of cotton-top tamarins (S. o. oedipus) Animal Technology 38: 167174Google Scholar
Smith, J A and Boyd, K M 2002 The Boyd Group Papers on the Use of Non-Human Primates in Research and Testing. The British Psychological Society: Leicester, UKGoogle Scholar
Snowdon, C T 1989 The successful captive breeding of endangered primates. In: Seth, P K and Seth, S (eds) Perspectives in Primate Biology, Volume 3 pp 245255. Today and Tomorrow's Printers and Publishers: New Delhi, IndiaGoogle Scholar
Snowdon, C T 1996 Infant care in cooperatively breeding species. Advances in the Study of Behavior 25: 643689CrossRefGoogle Scholar
Snowdon, C T and Savage, A 1989 Psychological well-being of captive primates: general considerations and examples from callitrichids. In: Segal, E F (ed) Housing, Care and Psychological Well-being of Captive and Laboratory Primates pp 7588. Noyes Publications: Park Ridge, New Jersey, USAGoogle Scholar
Snowdon, C T, Savage, A and McConnell, P B 1985 A breeding colony of cotton-top tamarins (Saguinus oedipus). Laboratory Animal Science 35: 477480Google ScholarPubMed
Snowdon, C T and Soini, P 1988 The tamarins, genus Saguinus. In: Mittermeier, R A, Rylands, A B, Coimbra-Filho, A F and da Fonseca, G A B (eds) Ecology and Behavior of Neotropical Primates, Volume 2 pp 223298. World Wildlife Fund: Washington, DC, USAGoogle Scholar
Stevenson, M F 1984 The captive breeding of marmosets and tamarins. Proceedings of the Symposium of the Association of British Wild Animal Keepers 8: 4960Google Scholar
Stevenson, M F 1986 Captive breeding of callitrichids: a comparison of reproduction and propagation in different species. In: Else, J G and Lee, P C (eds) Primate Ecology and Conservation pp 301313. Cambridge University Press: Cambridge, UKGoogle Scholar
Stevenson, M F and Rylands, A B 1988 The marmosets, genus Callithrix. In: Mittermeier, R A, Rylands, A B, Coimbra-Filho, A F and da Fonseca, G A B (eds) Ecology and Behavior of Neotropical Primates, Volume 2 pp 131222. World Wildlife Fund: Washington, DC, USAGoogle Scholar
Tardif, S D, Carson, R L and Clapp, N K 1986 Breeding performance of captive-born cottontop tamarin (Saguinus oedipus) females: proposed explanations for colony differences. American Journal of Primatology 11: 271275CrossRefGoogle ScholarPubMed
Tardif, S D, Richter, C B and Carson, R L 1984a Reproductive performance of three species of Callitrichidae. Laboratory Animal Science 34: 272275Google ScholarPubMed
Tardif, S D, Richter, C B and Carson, R L 1984b Effects of sibling-rearing experience on future reproductive success in two species of Callitrichidae. American Journal of Primatology 6: 377380CrossRefGoogle ScholarPubMed
Terborgh, J 1983 Five New World Primates: A Study in Comparative Ecology. Princeton University Press: Princeton, New Jersey, USAGoogle Scholar
Ventura, R, Buchanan-Smith, H M and Morris, K 2001 An enriched environment accelerates infant development in common marmosets. Primate Eye 73: 19Google Scholar
Woodbeck, T and Reinhardt, V 1991 Perch use by Macaca mulatta in relation to cage location. Laboratory Primate Newsletter 30: 1112Google Scholar
Yoneda, M 1981 Ecological studies of Saguinus fuscicollis and Saguinus labiatus with reference to habitat segregation and height preference. Kyoto University Overseas Research Reports of New World Monkeys 2: 4350Google Scholar