Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-26T18:10:09.209Z Has data issue: false hasContentIssue false
  • English
  • Français

Strain-Specific Effects of Cage Enrichment in Male Laboratory Mice (Mus Musculus)

Published online by Cambridge University Press:  11 January 2023

C M Nevison ,
J L Hurst  and
C J Barnard
C M Nevison*
Affiliation:
Animal Behaviour Research Group, School of Biological Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK Department of Veterinary Clinical Science and Animal Husbandry, University of Liverpool, Leahurst, Neston, South Wirral L64 7TE, UK
J L Hurst
Affiliation:
Department of Veterinary Clinical Science and Animal Husbandry, University of Liverpool, Leahurst, Neston, South Wirral L64 7TE, UK
C J Barnard
Affiliation:
Animal Behaviour Research Group, School of Biological Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK
*
† Contact for correspondence and reprint requests
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

‘Environmental enrichment’ is often considered to improve captive animal welfare. However, some studies using male mice, Mus musculus, indicate that increasing cage complexity increases aggression. Limited evidence suggests that enrichment differs in its effects on behaviour and physiology between strains; but behaviour also differs between strains in non-enriched environments. Differences in enrichment type, evaluation methods, and strains used, have caused difficulty in interpreting the efficacy of environmental enrichment in improving welfare. Using enrichment suitable for commercial laboratories (nesting material and a Perspex tunnel), we compared within-cage behavioural and physiological responses among males of six strains housed in non-enriched standard polypropylene cages with those housed in ‘enriched’ cages. Outbred ICR(CD-l) and TO mice, and inbred BALB/c mice were more aggressive than C57BL/6, CBA/Ca and DBA/2 mice, which exhibited low levels of aggression typical of most inbred strains. Enrichment did not significantly affect aggression levels. Animals in enriched cages spent more time investigating the internal cage environment, eating and drinking, and in stereotypic behaviour patterns, although levels differed between strains. The greatest increase in stereotypy levels (bar-related stereotypies) with enrichment was found in DBA/2 mice. Higher testosterone levels were maintained over the study period in mice housed in enriched cages, and in more aggressive strains. IgG levels were also higher in mice housed in enriched cages, and in the outbred strains ICR(CD-l) and TO compared with inbred strains. The relationship between aggression, testosterone and ‘enrichment ‘ suggests that increasing complexity in laboratory cages may increase a naturally selected territorial response in some strains. The implications for strain-specific welfare are discussed.

Keywords

animal welfarebehaviourenrichmentmicephysiologystrain differences
Type
Research Article
Information
Animal Welfare , Volume 8 , Issue 4: Special Issue: Genetics and Animal Welfare , November 1999 , pp. 361 - 379
Copyright
© 1999 Universities Federation for Animal Welfare

Footnotes

*

Current address

References

Barnard, C J, Bebnke, J M, Gage, A R, Brown, H and Smithurst, PR 1997 Immunity costs and behavioural modulation in male laboratory mice (Mus musculus) exposed to the odours of females. Physiology & Behavior 62: 857–866.CrossRefGoogle Scholar
Barnard C J, Behnke J M and Sewell 1993 Social behaviour, stress and susceptibility to infection in house mice (Mus musculus) - effects of duration of groups and aggressive behaviour prior to infection on susceptibility to Babesia microti. Parasitology 103: 183–192Google Scholar
Barnard, C J, Behnke, J M and Sewell, J 1994a Social behaviour and susceptibility to infection in house mice (Mus musculus) - effects of group size, aggressive behaviour and status related hormonal responses prior to infection on resistance to Babesia microti. Parasitology 108: 487–496CrossRefGoogle Scholar
Barnard, C J, Behnke, J M and Sewell, J 1994b Social behaviour, stress and susceptibility to infection in house mice (Mus musculus)·, effects of duration of grouping and aggressive behaviour prior to infection on susceptibility to Babesia microti. Parasitology 107: 183–192CrossRefGoogle Scholar
Barnard, C J, Behnke, J M and Sewell, J 1996a Social status and resistance to disease in house mice (Mus musculus) - status related modulation of hormonal responses in relation to immunity costs in different social and physical environments. Ethology 102: 63–84CrossRefGoogle Scholar
Barnard, C J, Behnke, J M and Sewell, J 1996b Environmental enrichment, immunocompetence and resistance to Babesia microti in male laboratory mice. Physiology & Behavior 60: 1223–1231CrossRefGoogle Scholar
Barnard, C J and Hurst, J L 1996 Welfare by design: the natural selection of welfare criteria. Animal Welfare 5: 405–434CrossRefGoogle Scholar
Barnard, C J, Hurst, J L and Aldhous, P 1991 Of mice and kin: the functional significance of kin bias in social behaviour. Biological Reviews 66: 379–430CrossRefGoogle ScholarPubMed
Berry, R J 1987 House mouse. Biologist 34: 177–186Google Scholar
Bisazza, A 1981 Social organisation and territorial behaviour in three strains of mice. Bollettino do Zoologia 48: 157–16Google Scholar
Brain, P F 1988 Hormones and aggression in infra-human vertebrates. In: Brain, P F and Benton, D (eds) The Biology of Aggression pp 181–213. Sijthoff and Noordhoff International: Alphen aan den Rijn, The NetherlandsGoogle Scholar
Brain, P F 1989 Social stress in laboratory mouse colonies. In: Laboratory Animal Welfare Research: Rodents. Proceedings of a Symposium Organised by Universities Federation for Animal Welfare and Held at the Royal Holloway and Bedford New College, University of London, Egham, Surrey, 22nd April 1988 pp 49–61. Universities Federation for Animal Welfare: Potters Bar, UKGoogle Scholar
Brown, R E 1985 The rodents ii: suborder Myomorpha. In: Brown, R E and Macdonald, D W (eds) Social Odours in Mammals. Volume 1 pp 345–457. Clarendon Press: Oxford, UKGoogle Scholar
Chamove, A S 1989 Cage design reduces emotionality in mice. Laboratory Animals 23: 215–219CrossRefGoogle ScholarPubMed
Crowcroft, P 1955 Territoriality in wild house mice, Mus musculus. Journal of Mammalogy 36: 299–301CrossRefGoogle Scholar
Crowcroft, P 1966 Mice all Over. Foulis: London, UKGoogle Scholar
Crowcroft, P and Rowe, F P 1963 Social organization and territorial behaviour in the wild house mouse (Mus musculus L.). Proceedings of the Zoological Society of London. 140: 517–531CrossRefGoogle Scholar
Dawkins, M S 1988 Behavioural deprivation: a central problem in animal welfare. Applied Animal Behaviour Science 20: 209–225CrossRefGoogle Scholar
Eklund, A 1996 The effects of inbreeding on aggression in wild male house mice (Mus domesticus). Behaviour 133: 883–901CrossRefGoogle Scholar
Estep, D Q, Lanier, D L and Dewsbury, D A 1975 Copulatory behaviour and nest-building behaviour of wild house mice (Mus musculus). Animal Learning and Behaviour 3: 329–336CrossRefGoogle ScholarPubMed
Festing, M F W 1979 Inbred Strains in Biomedical Research. Macmillan Press: London, UKCrossRefGoogle Scholar
Haemisch, A and Gartner, K 1994 The cage design affects intermale aggression in small groups of male laboratory mice: strain specific consequences on social organization, and endocrine activations in two inbred strains. Journal of Experimental Animal Science 36: 101–116Google ScholarPubMed
Haemisch, A, Voss, T, and Gärtner, K 1994 Effects of environmental enrichment on aggressive behaviour, dominance hierarchies and endocrine states in male DBA/2J mice. Physiology & Behavior 56: 1041–1048CrossRefGoogle ScholarPubMed
Hennesey, M B and Foy, T 1987 Nonedible material elicits chewing and reduces the plasma corticosterone response during novelty in mice. Behavioural Neuroscience 101: 237–245.CrossRefGoogle Scholar
Home Office 1989 Code of Practice for The Housing and Care of Animals Used in Scientific Procedures. HMSO: London, UKGoogle Scholar
Hurst, J L 1993 The priming effects of urine substrate markers on interactions between male house mice, Mus musculus domesticus, Schwartz and Schwartz. Animal Behaviour 45: 55–81CrossRefGoogle Scholar
Hurst, J L, Barnard, C J, Hare, R, Wheeldon, E B and West, C D 1996 Housing and welfare in laboratory rats: status dependent time-budgeting and pathophysiology in single-sex groups maintained in open rooms. Animal Behaviour 52: 335–360CrossRefGoogle Scholar
Hurst, J L, Barnard, C J, Nevison, C M and West, C D 1997 Housing and welfare in laboratory rats: Welfare implications of isolation and social contact among caged males. Animal Welfare 6: 329–347CrossRefGoogle Scholar
Jones, S E and Brain, P F 1987 Performances of inbred and outbred laboratory mice in putative tests on aggression. Behaviour Genetics 17: 87–96CrossRefGoogle ScholarPubMed
Lynch C B and Possidente B P Jr 1978 Relationships of maternal nesting to thermoregulatory nesting in house mice (Mus musculus) at warm and cold temperatures. Animal Behaviour 26: 1136–1143CrossRefGoogle Scholar
Mackintosh, J H 1989 Aggression in confined populations. In: Brain, P F, Mainardi, D and Parmigiani, S (eds) House Mouse Aggression pp 119–134. Harwood Academic Publishers: London, UKGoogle Scholar
Mancini, G, Carbonara, A O and Heremans, J F 1965 Immunochemical quantitation of antigens by single radial immunodiffusion. Immunochemistry 2: 235–254CrossRefGoogle ScholarPubMed
Manosevitz, M and Montemayer, R J 1972 Interaction of environmental enrichment and genotype. Journal of Comparative and Physiological Psychology 38: 191–201Google Scholar
Manosevitz, M and Pryor, J B 1975 Cage size as a factor in environmental enrichment. Journal of Comparative and Physiological Psychology 89: 648–654CrossRefGoogle Scholar
Manser, C E 1992 The Assessment of Stress in Laboratory Animals. RSPCA: Horsham, UKGoogle Scholar
Martin, P and Bateson, P 1986 Measuring Behaviour: An Introductory Guide. Cambridge University Press: Cambridge, UKGoogle Scholar
McFarland, D J 1989 Problems of Animal Behaviour. Longman: Harlow, UKGoogle Scholar
McGregor, P K and Ayling, S J 1990 Varied cages result in more aggression in male CFLP mice. Applied Animal Behaviour Science 26: 227–281CrossRefGoogle Scholar
Newberry, R C 1995 Environmental enrichment: increasing the biological relevance of captive environments. Applied Animal Behaviour Science 44: 229–243CrossRefGoogle Scholar
Rodgers, R J 1989 Physiological consequences of defeat. In: Brain, P F, Mainardi, D and Parmigiani, S (eds) House Mouse Aggression pp 233–252. Harwood Academic Publishers: London, UKGoogle Scholar
Rushen, J and de Passillé, A M B 1992 The scientific assessment of animal welfare: a critical review. Canadian Journal of Animal Science 72: 721–743CrossRefGoogle Scholar
Sandnabba, N K 1997 Territorial behaviour and social organization as a function of the level of aggresiveness of male mice. Ethology 103: 566–577CrossRefGoogle Scholar
Scharmann, W 1991 Improved housing of mice, rats and guinea pigs - a contribution to the refinement of animal experiments. ATLA 19: 108–114Google Scholar
Sherwin, C M 1997 Observations on the prevalence of nest building in non-breeding TO strain mice and their use of two nesting materials. Laboratory Animals 31: 125–132CrossRefGoogle ScholarPubMed
Sherwin, C M and Nicol, C J 1997 Behavioural demand functions of caged laboratory mice for additional space. Animal Behaviour 53: 67–74CrossRefGoogle Scholar
Southwick, C H and Clark, L H 1968 Interstrain differences in aggressive behaviour and exploratory activity of inbred mice. Communications in Behavioural Biology –A 1: 49–59Google Scholar
Van Oortmerssen, G A 1971 Biological significance, genetics and evolutionary origin of variability in behaviour within and between inbred strains of mice (Mus musculus). Behaviour 36: 1–92CrossRefGoogle Scholar
Van de Weerd, H A, Baumans, V, Koolhaas, J M and Van Zutphen, LFM 1994 Strain specific behavioural response to environmental enrichment in the mouse. Journal of Experimental Animal Science 36: 117–127.Google ScholarPubMed
Van de Weerd, H A, Van Loo, P L P, Van Zutphen, LFM, Koolhaas, J M and Baumans, V 1997 Nesting material as environmental enrichment has no adverse effects on behaviour and physiology of laboratory mice. Physiology & Behavior 62: 1019–1028CrossRefGoogle ScholarPubMed
Vom Saal, F S 1989 Perinatal testosterone exposure has opposite effects on adult intermale aggression and infanticide in mice. In: Brain, P F, Mainardi, D, Parmigiani, S (eds) House Mouse Aggression pp 174–204. Harwood Academic Publishers: London, UKGoogle Scholar
Wainwright, P E, Huang, Y S, Bulman-Fleming, B, Levesque, S and McCutcheon, D 1994 The effects of dietary fatty acid composition combined with environmental enrichment on brain and behaviour in mice. Behavioural Brain Research 60: 125–136CrossRefGoogle ScholarPubMed
Wolfensohn, S and Lloyd, M 1994 Handbook of Laboratory Animal Management and Welfare. Oxford University Press; Oxford, UKGoogle Scholar
Würbel, H, Stauffacher, M and Van Hoist, D 1996 Stereotypies in laboratory mice: Quantitative and qualitative description of the ontogeny of ‘wire-gnawing’ and ‘jumping’ in Zur:ICR and Zur: ICR NU. Ethology 102: 371–385CrossRefGoogle Scholar
Zieliński, W J and Vandenburgh, J G 1993 Testosterone and competitive ability in male house mice, Mus musculus: laboratory and field studies. Animal Behaviour 45: 873–891CrossRefGoogle Scholar