S57 © 2004 Universities Federation for Animal Welfare Animal Welfare 2004, 13: S57-69 The Old School, Brewhouse Hill, Wheathampstead, ISSN 0962-7286 Hertfordshire AL4 8AN, UK Cant stop, wont stop: is stereotypy a reliable animal welfare indicator? GJ Mason* and NR Latham Department of Zoology, Oxford University, South Parks Road, Oxford OX1 3PS, UK * Contact for correspondence and requests for reprints: [email protected] Abstract We estimate that stereotypies are currently displayed by over 85 million farm, laboratory and zoo animals worldwide. This paper investigates their reliability as welfare indicators, by surveying studies relating stereotypy to other welfare measures and by analysing the mechanisms underlying this behaviour. Where data exist, most (approximately 68%) situations that cause/increase stereotypies also decrease welfare. Stereotypy-eliciting situations are thus likely to be poor for welfare, although exceptions exist. Within such an environment, however, most (approximately 60%) accounts link individual stereotypy performance with improved welfare (cf approx- imately 20% linking it with reduced welfare). Thus, in a sub-optimal environment, non-stereotyping or low-stereotyping individuals could well have the poorest welfare, although again exceptions exist. Examining the mechanisms underlying stereotypy performance, we discuss four processes that could account for these complex links between stereotypy and welfare. Beneficial consequences from performing the specific source-behaviour of the stereotypy (do-it-yourself enrichment), or arising from repetition per se (mantra effects), may ameliorate welfare in poor environments. In addition, stereotypies that have become centrally controlled (habit-like), or that arise from autistic-like changes in the control of all behaviour (perseveration), are likely to be unreliable indicators of current state because they can be elicited by, or persist in, circumstances that improve welfare. To refine the role of stereotypy in welfare assessment, we suggest the collection of specific additional data to reveal when any of these four processes is acting. Until such research increases our understanding, stereotypies should always be taken seriously as a warning sign of potential suffering, but never used as the sole index of welfare; non-stereotyping or low-stereotyping individuals should not be overlooked or assumed to be faring well; simple measures of frequency should not be used to compare stereotypies that differ in age, form, or the biological or experiential characteristics of the performing animal; enrichments that do not immediately reduce stereotypies should not be assumed failures with respect to welfare; and finally, stereotypies should not be reduced by means other than tackling their underlying motivations. Keywords: animal welfare, central control, coping, crib-biting, perseveration, stereotypies Introduction At the moment, the answers to these questions are uncer- Stereotypies are repetitive, unvarying and apparently func- tain, but despite this, several practical initiatives aim to tionless behaviour patterns (eg Ödberg 1978; Mason 1991a) reduce stereotypies. Reducing stereotypy is, for example, commonly suggested to indicate welfare problems (eg the most common aim of environmental enrichment pro- Lawrence & Rushen 1993; Appleby 1999). They have been grammes in zoos (eg Shepherdson et al 1999; Young 2003). used to assess animal welfare in a number of ways. Some Animals environments may also be altered to make stereo- authors suggest that any level of stereotypy indicates poor typies unpleasant or difficult. For example, crib-biting and welfare (eg Broom & Johnson 1993; EC 1996; Laidlow wind-sucking in horses is often tackled by smearing crib 2001), others that increasing levels of stereotypy indicate edges and other horizontal surfaces with greasy or hot- decreasing levels of welfare (eg Fox 1984; Dawkins 1990; tasting substances (Kohnke 2000; Country Supplies 2003); Broom & Johnson 1993), and others still, that welfare is by using anti-stereotypy devices, such as neck straps (eg unacceptable if stereotypies occur in more than 5% of a McBride & Cuddeford 2001; Country Supplies 2003); or population (Wiepkema et al 1983), or for more than 10% of even by surgery (eg Kohnke 2000; Brouckaert et al 2002; an animals time (Broom 1983; Broom 1991). However it is Delacalle et al 2002). Other approaches target the animals unclear which, if any, of these suggestions is correct. This phenotype. For example, anti-depressants have been used to issue is important because we estimate that stereotypies are treat a variety of behavioural problems in domesticated currently performed by over 85 million animals worldwide and zoo animals (Melman 1995), and have successfully (see Table 1), which potentially means that a vast number of reduced pacing in a zoo-housed polar bear (Poulsen et al animals experience poor welfare. But is the welfare of all of 1995). Opiate antagonists have also been used to reduce these stereotypers equally impaired? Is it definitely worse crib-biting and weaving in horses (Kohnke 2000; Nicol than that of their non-stereotyping conspecifics? And are all 2000). Stereotypy has also been genetically selected methods of reducing stereotypy equally beneficial for welfare? against, for example in hens and mink (Mills et al 1985a,b; Universities Federation for Animal Welfare Science in the Service of Animal Welfare S58 Mason and Latham Table 1 Estimated number of stereotyping animals worldwide. Here, estimated global population sizes and published stereotypy prevalence data are used to estimate the total number of stereotyping captive animals. Note, however, that some populations in which stereotypies occur (eg laying hens, veal/dairy calves, laboratory and zoo primates, beef cattle, caged pets and zoo birds) are not considered here because of a lack of data, and that some of the population sizes given are not global (eg being only for Europe and the USA). The total number of stereotypers calculated around 87 million is thus an underestimate of the true global sum. Totals here represent those occurring over a period of approximately 6 months; annual figures would be larger because of those animals generally kept for less than 12 months (eg laboratory mice). Species Estimated Estimated Estimated Sources of data Notes (System) total popu- stereotypy total number lation size prevalence of stereo- (% typers individuals) Pigs 16 822 500 91.5% 15 393 000 EC (1997) and papers on Population size given for Europe and (Confined sows) stereotypy cited within it North and Central America only Poultry 68 400 000 82.6% 56 498 000 EC (2000) and papers on Population size given for Europe (Broiler breeders) stereotypy cited within it and North America only Mice 15 000 000 50.0% 7 500 000 National Association for Population size estimated from (Research and Biomedical Research annual figures and based on an laboratory breed- statistics, from the Humane estimated mouse lifespan of 6 ing establishments) Society of the United States; months. Stereotypy prevalence is a EC 1999; Australian and conservative guessed estimate; New Zealand Council for prevalence data are published only the Care of Animals in for ICR and ICR-nu mice, and are Research and Testing 98% (eg Würbel et al 1996), but (ANZCCART) unpublished this strain is known for high data stereotypy American mink 5 850 000 80.0% 4 680 000 European Fur Breeders Population size estimated from pelt (Breeding females production figures for output, based on assumed produc- on fur farms) 19971998. Stereotypy tion rate of 5 kits per female. prevalence is a mean for Prevalence estimate ideally needs two farms (de Jonge et al data from more sites 1986; Mason 1993) Wild carnivores 325 000 82.0% 246 000 International Species Stereotypy prevalence is the (Zoos) Information System (ISIS) median of species medians, from database papers on 22 species, and probably (http://www.isis.org) and an over-estimate, since non-stereo- Spedding (2000) cited in typing individuals/species are less Clubb (2001) likely to attract behavioural study Elephants 1700 47.0% 800 Clubb & Mason (2002) African and Asian elephant data (Zoos and circuses) pooled. Stereotypy prevalence is estimated at 41% for 1100 indi- viduals in zoos, and 65% for 530 individuals in circuses Horses 14 770 000 18.4% 2 724 000 Waters (2002) and the Food Population size is that of the (Stables) and Agriculture Organisation Developed world of the United Nations (http://www.fao.org) Vinke et al 2002); indeed in the Netherlands, it is now welfare assessment might be refined, and highlight the national policy for fur farmers to breed out this behaviour unknowns still needing research. (eg EC 2001; Vinke et al 2002). Zoos may also indirectly Stereotypies and welfare: what are the links? act similarly, in that they often do not replace or breed from highly stereotypic individuals (Ironmonger 1992; Irven The evidence linking stereotypies with poor welfare is 1993; Dollinger et al 1996). But do such approaches auto- diverse, and also well known. Extensively reviewed by matically improve welfare? Our aim here is to help answer many authors (eg Ödberg 1978; Mason 1991a,b; Lawrence this question by examining the relationship between stereo- & Rushen 1993; Garner & Mason 2002), it comprises the typies and suffering, and by using the current understanding types of environment in which stereotypies often develop of the causes of stereotypy to interpret the confusing picture (eg restraint