Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-05T04:48:49.430Z Has data issue: false hasContentIssue false

Consequences of enhancing environmental complexity for laboratory rodents — a review with emphasis on the rat

Published online by Cambridge University Press:  11 January 2023

DB Sørensen*
Affiliation:
Centre for Bioethics and Risk Assessment, Division of Laboratory Animal Science and Welfare, Department of Veterinary Pathobiology, The Royal Veterinary and Agricultural University of Copenhagen, Groennegaardsvej 15, 1870 Frederiksberg C, Denmark
JL Ottesen
Affiliation:
Novo Nordisk A/S, Novo Nordisk Park, 2760 Måløv, Denmark
AK Hansen
Affiliation:
Centre for Bioethics and Risk Assessment, Division of Laboratory Animal Science and Welfare, Department of Veterinary Pathobiology, The Royal Veterinary and Agricultural University of Copenhagen, Groennegaardsvej 15, 1870 Frederiksberg C, Denmark
*
* Contact for correspondence and requests for reprints: [email protected]
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.

Enhancing the complexity of the environments of captive animals is often referred to as environmental enrichment, and aims to have positive effects on the animals’ well-being. Such enrichments may have consequences both for so-called ‘normal’ behaviour and for the pathophysiology of the animals in question. The effects of a lack of environmental complexity, including social isolation, on home cage behaviour and on pathophysiology in rats is considered in this review. Several preference tests on rats — choice tests and operant tests — indicate a preference for bedding, nesting material and social contact. Contradictory research results concerning the need for gnawing objects per se are more difficult to interpret, and it is argued that excessive gnawing may be indicative of primary frustration and hence reduced welfare. One disadvantage of providing environmental enrichment to laboratory animals is a possible increase in subject variability, resulting in the need to use a greater number of test animals. However, this increased variability seems to be inconsistent and is not very well documented. It is argued that in cases where the behavioural benefits of environmental enrichment justify the use of more animals, better welfare should be more highly valued than a reduction in the number of animals used.

Type
Research Article
Copyright
© 2004 Universities Federation for Animal Welfare

References

Amsel, A 1992 Frustration Theory: An Analysis of Dispositional Learning and Memory. Cambridge University Press: Cambridge, UKCrossRefGoogle Scholar
Andrews, J S, Jansen, J H M, Linders, S, Princen, A and Broekkamp, C L E 2001 Performance of four different rat strains in the autoshaping, two-object discrimination, and swim maze tests of learning and memory. Physiology and Behavior 57: 785790CrossRefGoogle Scholar
Archer, J and Birke, L 1983 Exploration in Animals and Humans. Van Nostrand Reinhold Company: Cambridge, UKGoogle Scholar
Baenninger, L P 1967 Comparison of behavioural development in socially isolated and grouped rats. Animal Behaviour 15: 312323CrossRefGoogle ScholarPubMed
Barnett, J L, Dickson, R G and Hocking, W E 1979 Genotype and environment in the social interactions of wild and domestic ‘Norway’ rats. Aggressive Behavior 5: 1051193.0.CO;2-U>CrossRefGoogle Scholar
Barnett, S A 1975 Reproductive behaviour. In: Barnett S A (ed) The Rat. A Study in Behavior pp 138-164 The University of Chicago Press: Chicago, USAGoogle Scholar
Batchelor, G R 1994 The rest/activity rhythm of the laboratory rat housed under different systems. Animal Technology 45: 181187Google Scholar
Baumans, V, Stafleu, F R and Bouw, J 1987 Testing housing system for mice — the value of a preference test. Zeitschrift für Versuchstierkunde 29: 914Google ScholarPubMed
Beaver, B V 1989 Environmental enrichment for laboratory animals. ILAR (Institute for Laboratory Animal Research) News 31: 511Google Scholar
Blanchard, R J, Blanchard, D C and Flannelly, K 1985 Social stress, mortality and aggression in colonies and burrowing habitats. Behavioural Processes II: 209213CrossRefGoogle Scholar
Blom, H J M, Van Tintelen, G, Baumans, V, Van Den Broek, J and Beynen, A C 1995 Development and application of a preference test system to evaluate housing conditions for laboratory rats. Applied Animal Behaviour Science 43: 279290CrossRefGoogle Scholar
Blom, H J M, Van Tintelen, G, Van Vorstenbosch, C J A H V, Baumans, V and Beynen, A C 1996 Preferences of mice and rats for types of bedding material. Laboratory Animals 30: 234244CrossRefGoogle ScholarPubMed
Brown, K J and Grunberg, N E 1995 Effects of housing on male and female rats: crowding stresses males but calms females. Physiology and Behavior 58: 10851089CrossRefGoogle Scholar
Buhot-Averseng, M-C 1981 Nest-box choice in the laboratory mouse: preferences for nest-boxes differing in design (size and/or shape) and composition. Behavioural Processes 6: 337384CrossRefGoogle ScholarPubMed
Büttner, D 1993 Upright standing in the laboratory rat — time expenditure and its relation to locomotor activity. Journal of Experimental Animal Science 36: 1926Google ScholarPubMed
Chmiel, D J and Noonan, M 1996 Preference of laboratory rats for potentially enriching stimulus objects. Laboratory Animals 30: 97101CrossRefGoogle ScholarPubMed
Claassen, V 1994 Housing conditions. In: Claassen, V (ed) Neglected Factors in Pharmacology and Neuroscience Research pp 225250. Elsevier: Amsterdam, The NetherlandsGoogle Scholar
Collier, G H, Johnson, D F, CyBulski, K A and McHale, C A 1990 Activity patterns in rats (Rattus norvegicus) as a function of the cost of access to four resources. Journal of Comparative Psychology 104: 5365CrossRefGoogle ScholarPubMed
Collier, G H, Johnson, D F, Hill, W L and Kaufman, L W 1986 The economics of the law of effect. Journal of the Experimental Analysis of Behavior 46: 113136Google Scholar
Dawkins, M S 1990 From an animal's point of view: motivation, fitness, and animal welfare. Behavioral and Brain Sciences 13: 161CrossRefGoogle Scholar
Denny, M S 1975 The rat's long-term preference for complexity in its environment. Animal Learning and Behavior 3: 245249CrossRefGoogle Scholar
Duncan, I J H 1992 Measuring preferences and the strength of preferences. Poultry Science 71: 658663CrossRefGoogle ScholarPubMed
Eskola, S and Kaliste-Korhonen, E 1998 Effects of cage type and gnawing blocks on weight gain, organ weights and open-field behaviour in Wistar rats. Scandinavian Journal of Laboratory Animal Science 25: 180193Google Scholar
Eskola, S, Lauhikari, M, Voipio, H-M, Laitinen, M and Nevalainen, T 1999a Environmental enrichment may alter the number of rats needed to achieve statistical significance. Scandinavian Journal of Laboratory Animal Science 26: 134144Google Scholar
Eskola, S, Lauhikari, M, Voipio, H-M and Nevalainen, T 1999b The use of aspen blocks and tubes to enrich the cage environment of laboratory rats. Scandinavian Journal of Laboratory Animal Science 26: 110Google Scholar
Gärtner, K 1999 Reduction or refinement: standard or enriched cages for mice in experiments? Influence of cage enrichment on deviation. In: Tur-Mari J A and Orellana-Muriana J M (eds) Proceedings of the International Council for Laboratory Animal Science (ICLAS) and Federation of European Laboratory Animal Science (FELASA) Meeting, Palma de Mallorca, Spain, May 1999 p 120 (Abstract)Google Scholar
Goldsmith, J F, Brain, P F and Benton, D 1978 Effects of the duration of individual or group housing on behavioural and adrenocortical reactivity in mice. Physiology and Behavior 21: 757760CrossRefGoogle ScholarPubMed
Grant, E C 1963 An analysis of the social behaviour of the male laboratory rat. Behaviour 21: 260281CrossRefGoogle Scholar
Haemisch, A and Gärtner, 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 (DBA/2J and CBA/J). Journal of Experimental Animal Science 36: 101116Google ScholarPubMed
Haemisch, A and Gärtner, K 1997 Effects of cage enrichment on territorial aggression and stress physiology in male laboratory mice. Acta Physiologica Scandinavica 161: 7376Google Scholar
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 and Behavior 56: 10411048CrossRefGoogle ScholarPubMed
Hansen, A K, Sandøe, P, Svendsen, O, Forsman, B and Thomsen, P 1998 The need to refine the notion of reduction. Proceedings of the International Conference on Humane Endpoints in Animal Experiments for Biomedical Research, Zeist, The Netherlands, 22-25th November 1998 pp 139-144Google Scholar
Heizmann, V, Jonas, I, Hirschenauer, K and Havelec, L 1998 Choice tests with groups of mice: nestbox, nesting material and tubes as enrichment items for laboratory mice. Journal of Experimental Animal Science 39: 4360Google Scholar
Hogan, J A 1967 Fighting and reinforcement in the Siamese fighting fish (Betta splendens). Journal of Comparative and Physiological Psychology 64: 356359CrossRefGoogle ScholarPubMed
Hurst, J L, Barnard, C J, Hare, R, Wheeldon, E B and West, C D 1996 Housing and welfare in laboratory rats: time-budgeting and pathophysiology in single-sex groups. Animal Behaviour 52: 335360CrossRefGoogle 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: 329347Google Scholar
Hurst, J L, Barnard, C J, Nevison, C M and West, C D 1998 Housing and welfare in laboratory rats: the welfare implications of social isolation and social contact among females. Animal Welfare 7: 121136Google Scholar
Hurst, J L, Barnard, C J, Tolladay, U, Nevison, C M and West, C D 1999 Housing and welfare in laboratory rats: effects of cage stocking density and behavioural predictors of welfare. Animal Behaviour 58: 563586CrossRefGoogle ScholarPubMed
Jensen, K K and Sandøe, P 1997 Animal welfare: relative or absolute? Applied Animal Behaviour Science 54: 3337CrossRefGoogle Scholar
Kaliste-Korhonen, E, Eskola, S, Rekila, T and Nevalainen, T 1995 Effects of gnawing material, group size and cage level in rack on Wistar rats. Scandinavian Journal of Laboratory Animal Science 22: 291299Google Scholar
Kaliste-Korhonen, E, Kelloniemi, J and Harri, M 1996 Cage material and rat behaviour. Scandinavian Journal of Laboratory Animal Science 23: 125128Google Scholar
Kennes, D, Ödberg, F O, Bouquet, Y and De Rycke, P H 1988 Changes in naloxone and haloperidol effects during the development of captivity-induced jumping stereotypy in bank voles. European Journal of Pharmacology 153: 1924CrossRefGoogle ScholarPubMed
Krohn, T C, Hansen, A K and Dragsted, N 2003 Telemetry as a method for measuring the impact of housing conditions on rats’ welfare. Animal Welfare 12: 5362Google Scholar
Lore, R and Flannelly, K 1977 Rat societies. Scientific American 236: 106116CrossRefGoogle ScholarPubMed
Manser, C E, Broom, D M, Overend, P and Morris, T H 1998a Investigations into the preferences of laboratory rats for nest-boxes and nesting materials. Laboratory Animals 32: 2335CrossRefGoogle ScholarPubMed
Manser, C E, Broom, D M, Overend, P and Morris, T H 1998b Operant studies to determine the strength of preference in laboratory rats for nest-boxes and nesting materials. Laboratory Animals 32: 3641CrossRefGoogle ScholarPubMed
Manser, C E, Elliott, H, Morris, T H and Broom, D M 1996 The use of a novel operant test to determine the strength of preference for flooring in laboratory rats. Laboratory Animals 30: 16CrossRefGoogle ScholarPubMed
Manser, C E, Morris, T H and Broom, D M 1995 An investigation into the effects of solid or grid cage flooring on the welfare of laboratory rats. Laboratory Animals 29: 353363CrossRefGoogle ScholarPubMed
Matthews, L R and Ladewig, J 1994 Environmental requirements of pigs measured by behavioural demand functions. Animal Behaviour 47: 713719CrossRefGoogle Scholar
McFarland, D J 1977 Decision-making in animals. Nature 269: 1521CrossRefGoogle Scholar
McGregor, P K and Ayling, S J 1990 Varied cages result in more aggression in male CFLP mice. Applied Animal Behaviour Science 26: 277281CrossRefGoogle Scholar
Mering, S 2000 Housing environment and enrichment for laboratory rats — refinement and reduction outcomes. PhD Thesis, University of Kuopio, Finland. Kuopio University Printing Office: Kuopio, FinlandGoogle Scholar
Mering, S, Kaliste-Korhonen, E and Nevalainen, T 2001 Estimates of appropriate number of rats: interaction with housing environment. Laboratory Animals 35: 8090CrossRefGoogle ScholarPubMed
Mulder, J B 1975 Bedding preferences of pregnant laboratory-reared mice. Behavior Research Methods and Instrumentation 7: 2122CrossRefGoogle Scholar
Nevalainen, T, Lauhikari, M, Eskola, S and Voipio, H-M 1999 Environmental enrichment may alter the number of animals needed. In: Tur-Mari J A and Orellana-Muriana J M (eds) Proceedings of the International Council for Laboratory Animal Science (ICLAS) and Federation of European Laboratory Animal Science (FELASA) Meeting, Palma de Mallorca, Spain, May 1999 p SI (Abstract)Google Scholar
Nevison, C M, Hurst, J L and Barnard, C J 1999a Strain-specific effects of cage enrichment in male laboratory mice (Mus musculus). Animal Welfare 8: 361379Google Scholar
Nevison, C M, Hurst, J L and Barnard, C J 1999b Why do male ICR (CD-1) mice perform bar-related (stereotypic) behaviour? Behavioural Processes 47: 95111CrossRefGoogle ScholarPubMed
Ödberg, F O 1987 The influence of cage size and environmental enrichment on the development of stereotypies in bank voles (Clethrionomys glareolus). Behavioural Processes 14: 155173CrossRefGoogle ScholarPubMed
Orok-edem, E and Key, D 1994 Response of rats (Rattus norvegicus) to enrichment objects. Animal Technology 45: 2530Google Scholar
Paré, W P 1993 Passive-avoidance behavior in Wistar-Kyoto (WKY), Wistar, and Fischer-344 rats. Physiology and Behavior 54: 845852CrossRefGoogle ScholarPubMed
Patterson-Kane, E C, Harper, D N and Hunt, M 2001 The cage preferences of laboratory rats. Laboratory Animals 35: 7479CrossRefGoogle ScholarPubMed
Poole, T and Dawkins, M S 1999 Environmental enrichment for vertebrates. In: Poole, T and English, P (eds) The UFAW Handbook on the Care and Management of Laboratory Animals pp 1320. Blackwell Science: Oxford, UKGoogle Scholar
Rock, F M, Jaslow, B W, Petersom, A, Kaeppeli, M K and Price, J L 2000 Preference of single housed rats for a solid-bottom or wire-bottom stainless steel cage floor. Proceedings of the 51st American Association for Laboratory Animal Science (AALAS) National Meeting, San Diego, USA, November 5-9th, 2000 p 79 (Abstract)Google Scholar
Rollin, B 1989 Animal pain. In: Regan, T and Singer, P (eds) Animal Rights and Human Obligations. Prentice-Hall Inc: New Jersey, USAGoogle Scholar
Roper, T J 1975 Nest material and food as reinforcers for fixed-ratio responding in mice. Learning and Motivation 6: 327343CrossRefGoogle Scholar
Saibaba, P, Sales, G D, Stodulski, G and Hau, J 1996 Behaviour of rats in their home cages: daytime variations and effects of routine husbandry procedures analysed by time sampling techniques. Laboratory Animals 30: 1321CrossRefGoogle ScholarPubMed
Sandøe, P 1996 Animal and human welfare — are they the same kind of thing? Acta Agriculturae Scandinavica, Section A, Animal Science 27: 1115 (Suppl)Google Scholar
Sandøe, P, Crisp, R and Holtug, N 1997 Ethics. In: Appleby, M C and Hughes, B O (eds) Animal Welfare pp 318. CAB International: Wallingford, UKGoogle Scholar
Sherwin, C M 1996a Laboratory mice persist in gaining access to resources: a method of assessing the importance of environmental features. Applied Animal Behaviour Science 48: 203214CrossRefGoogle Scholar
Sherwin, C M 1996b Preferences of individually housed TO strain laboratory mice for loose substrate or tubes for sleeping. Laboratory Animals 30: 245251CrossRefGoogle ScholarPubMed
Sherwin, C M 1997 Observations on the prevalence of nestbuilding in non-breeding TO strain mice and their use of two nesting materials. Laboratory Animals 31: 125132CrossRefGoogle ScholarPubMed
Simonsen, H B 1996 Assessment of animal welfare by a holistic approach: behaviour, health and measured opinion. Acta Agriculturae Scandinavica, Section A, Animal Science 27: 9196 (Suppl)Google Scholar
Sluyter, F and Van Oortmerssen, G A 2000 A mouse is not just a mouse. Animal Welfare 9: 193205Google Scholar
Sørensen, D B 2001 Evaluating animal welfare: assessing the substitutability of two environmental factors by use of operant conditioning. PhD Thesis, The Royal Veterinary and Agricultural University of Copenhagen, Denmark. DSR Grafik: Copenhagen, DenmarkGoogle Scholar
Sørensen, D B, Ladewig, J and Lawson, L G 2001 The influence of strain on demand function for water in rats (Rattus norvegicus). Scandinavian Journal of Laboratory Animal Science 28: 19Google Scholar
Sørensen, D B, Ladewig, J, Matthews, L, Ersboll, A K and Lawson, L 2001 Measuring motivation: using the cross point of two demand functions as an assessment of the substitutability of two reinforcers. Applied Animal Behaviour Science 74: 281291CrossRefGoogle Scholar
Toates, F 1996 Cognition and evolution — an organization of action perspective. Behavioural Processes 35: 239250CrossRefGoogle Scholar
Townsend, P 1997 Use of in-cage shelters by laboratory rats. Animal Welfare 6: 95103Google Scholar
Tsai, P-P and Hackbarth, H 1999 Environmental enrichment in mice: is it suitable for every experiment? In: Tur-Mari J A and Orellana-Muriana J M (eds) Proceedings of the International Council for Laboratory Animal Science (ICLAS) and Federation of European Laboratory Animal Science (FELASA) Meeting, Palma de Mallorca, Spain, May 1999 p 112 (Abstract)Google Scholar
Van de Weerd, H A, Van den Broek, F A R and Baumans, V 1996 Preference for different types of flooring in two rat strains. Applied Animal Behaviour Science 46: 251261CrossRefGoogle Scholar
Van de Weerd, H A, Van Loo, P L P, Van Zutphen, L F M, Koolhaas, J M and Baumans, V 1997 Preferences for nesting material as environmental enrichment for laboratory mice. Laboratory Animals 31: 133143CrossRefGoogle ScholarPubMed
Van de Weerd, H A, Van Loo, P L P, Van Zutphen, L F M, Koolhaas, J M and Baumans, V 1998a Preferences for nest boxes as environmental enrichment for laboratory mice. Animal Welfare 7: 1125Google Scholar
Van de Weerd, H A, Van Loo, P L P, Van Zutphen, L F M, Koolhaas, J M and Baumans, V 1998b Strength of preference for nesting material as environmental enrichment for laboratory mice. Applied Animal Behaviour Science 55: 369382CrossRefGoogle Scholar
Van Der Staay, F J and Blokland, A 1996 Behavioral differences between outbred Wistar, inbred Fischer 344, brown Norway, and hybrid Fischer 344 x brown Norway rats. Physiology and Behavior 60: 97109CrossRefGoogle ScholarPubMed
Ward, G E and DeMille, D 1991 Environmental enrichment for laboratory mice. Animal Technology 42: 149156Google Scholar
Weiss, J and Taylor, G T 1985 Einfluss der käfigstruktur auf das wahlverhalten und die spontanmotilität von laborratten. Zeitschrift für Versuchstierkunde 27: 175184 [Title translation: The influence of cage environment on choice-behaviour and activity in laboratory rats]Google Scholar
Wiedenmayer, C 1997 Causation of the ontogenetic development of stereotypic digging in gerbils. Animal Behaviour 53: 461470CrossRefGoogle Scholar
Würbel, H, Chapman, R and Rutland, C 1998a Effect of feed and environmental enrichment on development of stereotypic wire-gnawing in laboratory mice. Applied Animal Behaviour Science 60: 6981CrossRefGoogle Scholar
Würbel, H, Freire, R and Nicol, C J 1998b Prevention of stereotypic wire-gnawing in laboratory mice: effects on behaviour and implications for stereotypy as a coping response. Behavioural Processes 42: 6172CrossRefGoogle ScholarPubMed
Würbel, H, Stauffacher, M and Von Holst, 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: 371385CrossRefGoogle Scholar