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Environmental enrichment

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Click here to view examples of effective enrichment for laboratory-housed dogs.

 

Definition

 

Environmental enrichment (EE) is commonly used as a Refinement for laboratory-housed dogs, and it is recommended in both legislation and good practice guidelines. Environmental enrichment is the provision of items or opportunities which enhance the well-being of captive animals and promote desirable behaviours [1]. However, in order to act as Refinements, the enrichment items must improve the welfare of the dogs.

Appropriate enrichment provides opportunities for animals to make choices, increasing their ability to maintain homoeostasis or to control social interactions [2]. Given the time spent in the home pen, providing suitable EE should be considered an critical Refinement for the laboratory-housed dog.

 

Benefits of environmental enrichment for laboratory-housed dogs

 

There is considerable literature on the benefits of EE for kennelled dogs (see [3] for review). When housed according to the minimum prescribed standards, dogs often lack sufficient stimuli and the space needed to display species specific behaviours [4]. The provision of increased social contact (e.g. [5]) and the provision of toys are most frequently recommended in the literature (e.g. [6]). Laboratory-housed dogs have been found to show much interest in toys, particularly those which are novel in nature, can be chewed (e.g. rawhide, nylabone) or generate noise [7,16].

We found positive changes in laboratory-housed dogs’ behaviour following the introduction of feeding toy enrichment [8]. An area separate from the dog’s home pen suitable for exercise is also recommended; such an area may include a variety of chews, toys and climbing equipment to encourage a range of foraging and active behaviours in the dog, allowing the expression of natural behaviour. Examples of enrichment items and exercise areas can be seen here.

A concern when altering the environment of a laboratory animal is that the alteration will interact with the effects of the test substance and will invalidate comparisons with historical data [9]. However, it is important to consider enrichment of the environment when considering methods of improving the welfare of dogs housed in laboratories. When housed according to the minimum prescribed standards, dogs often lack sufficient stimuli and the space needed to display species specific behaviours [4]. Dogs kept in low-stimulus housing conditions may, for example, develop excessive fear or aggression, increased auto-grooming and vocalisations, increased passiveness, and show manipulation of enclosure barriers, repetitive locomotive behaviour (stereotypies) and corprophagy (e.g. [10,11,12]). Most of these behavioural patterns are commonly used as indicators of chronic stress (e.g. [12]). Schipper et al. [4] studied 17 laboratory beagle dogs and found that the provision of a feeding enrichment toy resulted in a decrease in inactive time and when compared to the control group, appeared to prevent an increase in the rate of stereotypies displayed over time.

There may be a reluctance to use feeding enrichment toys for laboratory-housed dogs because of a belief that it may make the dogs less willing to interact with human handlers, may encourage aggression or possessiveness within the kennel and may negatively affect health [13]. Gaines et al. [13] studied this in a population of 22 military working dogs, eight of which were provided with a Kong feeding enrichment toy for four months at one hour per weekday evening. No differences were reported in working ability, nor any adverse effects on health or increase in aggression. Rather than an adverse effect on working performance, enriched dogs were found to learn faster from positive reinforcement training compared to control dogs not enriched with the feeding toy. In a review, Wells [6] found that providing kennelled dogs with increased opportunities to make social contact, with conspecifics and humans, may allow the dog to gain more control over its environment, thereby decreasing the chances of the individual failing to cope with the pressures of confinement [11].

It is now widely recommended, based on available evidence, that kennelled dogs should be housed in pairs or groups (e.g. [5,11,10,15]). Laboratory-housed dogs have been found to show much interest in toys, particularly those which are novel in nature, can be chewed (e.g. rawhide, nylabone) or generate noise (e.g. [7,15]). Suspending toys slightly off the ground may also keep toys clean, increase the ease of husbandry, reduce competition between dogs and encourage interaction with the toys animals (e.g. [7,16]). Wells [6] also found that enrichment with various toys resulted in increased activity in the dogs, a desirable change in behaviour for kennelled dogs.

Impact of increased handling enrichment on health

 

Given the already established need for normal healthy subjects, the effects of enrichment on the brain must be taken into account. In order for laboratory animals to model normal humans, it is important that their environment supports normal development as far as possible to ensure high fidelity models. Investigations into the effects of environmental enrichment and refinements in procedures have also found important effects on other aspects of health and behaviour.

These studies show that as well as being able to influence neural development through changes in the environment, it is possible to positively influence health in captive animals. Again, these positive changes ensure as healthy subjects as far as possible and therefore high fidelity models, as well as promoting good welfare. Although there is some resistance to implementing enrichment because of the perceived loss of standardisation, there is increasing evidence that enrichment need not result in greater variability, and indeed that high levels of standardisation may not be beneficial to science. Würbel [17] and Würbel and Garner [18] argue that institutional standardisation leads to poor external validity and reduces replicability between laboratories because of systematic differences. In line with this, they suggest that it would be better to design factorial experiments. While Benefiel et al. [19] found that enrichments sometimes lead to increased variability,

Hubrecht [20] reviewed the literature and found that for many of the studies which have found conflicting or negative effects of enrichment, the purpose of the enrichment was not always with the aim of improving welfare. Often, more elaborate enrichment was used than was appropriate for the animals under study, or the enrichment was not necessarily appropriate for the animals. This may account for the variability in success of various enrichment strategies, as such enrichment should always aim to improve welfare, however the term may be misused. Wolfer et al. [21] specifically investigated the effects of cage enrichment on mice. Three strains of mice were acquired by three laboratories and kept one of three housing conditions: small, standard or enriched cages. Those housed in small and standard cages showed impaired brain development, abnormal repetitive behaviours and anxious behaviours. The authors state that there was little variation in results between the laboratories or between the groups of mice when they were tested using four standard behavioural tests (an elevated O-maze, open-field test, novel-object test and place navigation in a water maze). Conversely, Crabbe, Wahlsten and Dudek [22] investigated the effects of rigorous standardisation in mouse husbandry across three laboratories and found marked and systematic differences between laboratories despite the measures taken to ensure practices were identical.

Würbel [23] offers an explanation for this. He suggests that since phenotypes differ depending on housing conditions, standardisation may not be optimal for good science. Standardisation produces results idiosyncratic to that particular environment and encourages systematic variation. Promoting natural behaviour and the corresponding physiological responses may be more valid. Enriched animals may actually be less sensitive to environmental idiosyncrasies. Since standard laboratory cages impose constraints on behaviour and brain development, resulting in behavioural abnormalities and aberrant brain functions these animals may make poor models for humans. An environment which meets an animal’s needs may guarantee normal behavioural and brain development [24]. Therefore animals which have more normal development and behaviour may be more robust to variations caused by changes in the environment as long as the environment does not cause excessive stress or inhibit the ability to perform natural behaviours. Wurbel [24] suggests that rather than attempting to eliminate the effects of environmental factors through standardisation, or to ‘explain them away’ by simply listing them, to promote good science it is desirable to systematically vary environmental factors and use factorial designs to investigate the effects of factors. This may reveal biologically relevant interactions between the genetic and environmental background of the animal while reducing the limited external validity of results which is caused by high levels of standardisation.

Although there are clearly many important factors in ensuring quality in scientific research, from the design to the analysis and publication of results, welfare has a central role to play. It has been shown that changes in welfare exert influence over not just behaviour, but physiology and immunology which are of course of great interest to those using animals in scientific research. Some authors have advised against using environmental enrichment to prevent confounds through loss of standardisation. However, others have shown that improving welfare through environmental enrichment promotes more normal physiology and behaviour in animals, which is of course important when these animals are models for humans, and also may results in animals which are less sensitive to the idiosyncrasies between laboratories. As Crabbe et al. [22] showed, even when the level of standardisation is high there is variation between laboratories resulting in unpredictable differences in the animals. To ensure good quality in science, harmonisation in welfare needs to be achieved, to allow animals a variety of coping mechanisms and to prevent decreases in welfare which have a negative impact on data. The principles in measuring animal welfare and in improving quality of science are the central theme of this project. The purpose of the project is to identify valid measures of welfare in the laboratory dog and use these measures to empirically examine the link between welfare and quality of data output. The factors ensuring quality in science have been laid out by Poole [25] and Festing [26].


1. Buchanan-Smith, H.M. (2010). Environmental enrichment for primates in laboratories. Advances in Science and Research, 5, 41-56.

2.Hubrecht, R.C. (2014). The welfare of animals used in research. Chichester: Wiley-Blackwell.

3. Wells, D. (2004). A review of environmental enrichment for kennelled dogs, canis familiaris. Applied Animal Behaviour Science, 85 (3-4), 307-317.

4. Schipper, L. L., Vinke, C. M., Schilder, M. B. & Spruijt, B. M. (2008). The effect of feeding enrichment toys on the behaviour of kennelled dogs (Canis familiaris). Applied Animal Behaviour Science, 114 (1), 182-195.

5. Mertens, P. A. & Unshelm, J. (1996). Effects of group and individual housing on the behavior of kennelled dogs in animal shelters. Anthrozoos, 9 (1), 40-51.

6. Wells, D. (2004). The influence of toys on the behaviour and welfare of kennelled dogs. Animal Welfare, 13 (3), 367-373.

7. Hubrecht, R. & Serpell, J. (1993). Influence of housing conditions on the behaviour and welfare of dogs. Applied Animal Behavior Science, 35 (3), 293.

8. Hall, L.E. (2014). A practical framework for harmonising welfare and quality of data output in the laboratory-housed dog. (Unpublished PhD thesis). University of Stirling, Stirling, UK.
9. Dean, S. (1999). Environmental enrichment of laboratory animals used in regulatory toxicology studies. Laboratory Animals, 33 (4), 309-327

10. Hetts, S., Derrell Clark, J., Calpin, J. P., Arnold, C. E. & Mateo, J. M. (1992). Influence of housing conditions on beagle behaviour. Applied Animal Behaviour Science, 34 (1), 137-155.

11. Hubrecht, R., Serpell, J. & Poole, T. (1992). Correlates of pen size and housing conditions on the behaviour of kennelled dogs. Applied Animal Behaviour Science, 34 (4), 365-383.

12. Beerda, B., Schilder, M., Bernadina, W., Van Hooff, J., De Vries, H. & Mol, J. (1999). Chronic stress in dogs subjected to social and spatial restriction. II. Hormonal and immunological responses. Physiology and Behavior, 66 (2), 243-254.

13. Gaines, S. A., Rooney, N. J. & Bradshaw, J. W. (2008). The effect of feeding enrichment upon reported working ability and behavior of kenneled working dogs. Journal of Forensic Sciences, 53 (6), 1400-1404.

14. Hetts, S., Derrell Clark, J., Calpin, J., Arnold, C. & Mateo, J. (1992). Influence of housing conditions on beagle behaviour. Applied Animal Behaviour Science, 34 (1-2), 137-155.

15. Hubrecht, R. (1995a). Enrichment in puppyhood and its effects on later behaviour of dogs. Laboratory Animal Science, 45, 70-75.

16. Hubrecht, R. (1995b). The welfare of dogs in human care. In J. Serpell. (Ed.), The domestic dog: Its evolution, behaviour and interactions with people. Cambridge: Cambridge University Press.
17. Wurbel, H. (2000). Behaviour and the standardization fallacy. Nature Genetics, 26 (3), 263-263.

18. Wurbel, H. & Garner, J. P. (2007). Refinement of rodent research through environmental enrichment and systematic randomization. NC3Rs, 9, 1-9.

19. Benefiel, A. C., Dong, W. K. & Greenough, W. T. (2005). Mandatory enriched housing of laboratory animals: the need for evidence-based evaluation. ILAR Journal, 46 (2), 95-105.

20. Hubrecht, R. (2010). Enrichment: Animal welfare and experimental outcomes. In R. Hubrecht & J. Kirkwell (Eds.), The UFAW handbook on the care and management of laboratory and other research animals: eighth edition. Chichester: Wiley-Blackwell.

21. Wolfer, D. P., Litvin, O., Morf, S., Nitsch, R. M., Lipp, H.-P. & Wurbel, H. (2004). Laboratory animal welfare: Cage enrichment and mouse behaviour. Nature, 432 (7019), 821-822.

22. Crabbe, J. C., Wahlsten, D. & Dudek, B. C. (1999). Genetics of mouse behavior: Interactions with laboratory environment. Science, 284 (5420), 1670-1672.

23. Wurbel, H. (2001). Ideal homes? Housing effects on rodent brain and behaviour. Trends in Neurosciences, 24 (4), 207-211.

24. Wurbel, H. (2002). Behavioral phenotyping enhanced - beyond (environmental) standardization. Genes, Brain and Behavior, 1 (1), 3-8.

25. Poole, T. (1997). Happy animals make good science. Laboratory Animals, 31 (2), 116-124.

26. Festing, M. (2010). The design of animal experiments. In R. Hubrecht & J. Kirkwell(Eds.), The UFAW Handbook on the Care and Management of Laboratory and Other Research Animals: Eighth Edition. Chichester: Wiley-Blackwell (p. 23-36).

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