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Positive animal welfare states and reference standards for welfare assessment DJ Mellor
a
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Animal Welfare Science and Bioethics Centre, PN453, Massey University, Palmerston North 4442, New Zealand Accepted author version posted online: 30 May 2014.Published online: 18 Aug 2014.
Click for updates To cite this article: DJ Mellor (2015) Positive animal welfare states and reference standards for welfare assessment, New Zealand Veterinary Journal, 63:1, 17-23, DOI: 10.1080/00480169.2014.926802 To link to this article: http://dx.doi.org/10.1080/00480169.2014.926802
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New Zealand Veterinary Journal 63(1), 17–23, 2015
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Review Article
Positive animal welfare states and reference standards for welfare assessment
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DJ Mellor*§
Abstract
Introduction
Developments in affective neuroscience and behavioural science during the last 10–15 years have together made it increasingly apparent that sentient animals are potentially much more sensitive to their environmental and social circumstances than was previously thought to be the case. It therefore seems likely that both the range and magnitude of welfare trade-offs that occur when animals are managed for human purposes have been underestimated even when minimalistic but arguably well-intentioned attempts have been made to maintain high levels of welfare. In light of these neuroscience-supported behaviour-based insights, the present review considers the extent to which the use of currently available reference standards might draw attention to these previously neglected areas of concern. It is concluded that the natural living orientation cannot provide an all-embracing or definitive welfare benchmark because of its primary focus on behavioural freedom. However assessments of this type, supported by neuroscience insights into behavioural motivation, may now carry greater weight when used to identify management practices that should be avoided, discontinued or substantially modified. Using currently accepted baseline standards as welfare reference points may result in small changes being accorded greater significance than would be the case if they were compared with higher standards, and this could slow the progress towards better levels of welfare. On the other hand, using “what animals want” as a reference standard has the appeal of focusing on the specific resources or conditions the animals would choose themselves and can potentially improve their welfare more quickly than the approach of making small increments above baseline standards. It is concluded that the cautious use of these approaches in different combinations could lead to recommendations that would more effectively promote positive welfare states in hitherto neglected areas of concern.
The present review is the last in a series of three that is intended to assist veterinarians, animal-based scientists and others to update and extend their animal welfare science knowledge, especially with regard to the promotion of positive welfare states in animals. The first review provides a brief non-technical outline of contributions of affective neuroscience and behavioural science to understanding positive welfare states and introduces the new concept of positive affective engagement which encapsulates the experiences animals may have when they are successfully undertaking rewarding goal-directed behaviours (Mellor 2015a). Furthermore, it expands on previous accounts of neuroscience support for interpreting the behaviour of animals in terms of what they may intend to achieve, i.e. their goals, and the positive or negative affects that may accompany such behaviours when they succeed or fail to achieve those goals (Panksepp 2005; Boissy et al. 2007).
KEY WORDS: Affective neuroscience, natural living, baseline standards, what animals want, cognitive bias, reference standards, positive welfare
* Animal Welfare Science and Bioethics Centre, PN453, Massey University, Palmerston North 4442, New Zealand § Author for correspondence. Email: [email protected] http://dx.doi.org/10.1080/00480169.2014.926802 © 2014 New Zealand Veterinary Association
In highlighting these points, the first review notes that scientific acceptance of the existence of particular affective states largely depends on a good understanding of the underlying neurological mechanisms (Mellor 2015a). It is argued, further, that an increasing knowledge of some other neurophysiological mechanisms may strengthen confidence in behaviour-based inferences about the character of various situation-related motivational affects, i.e. those associated with some environmental and social interactions, provided that such inferences are arrived at cautiously (Wemelsfelder 1997, 2007). The first review therefore sets the scene for the second one (Mellor 2015b), which describes environment-focused and animal-toanimal interactive behaviours, some of which are anticipated to involve positive affective engagement. It highlights the potentially widespread occurrence of such situation-related positive affects and contrasts them with the negative affects that may arise when animals do not have opportunities to engage in rewarding behaviours. The present review extends the previous two by analysing how greater confidence in inferences regarding the presence and nature of situation-related affects might guide the choice of reference standards used to differentiate between acceptable and unacceptable ways of managing animals. The reference standards considered are natural living, baseline standards and what animals want.
QBA
Qualitative behavioural assessment
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Natural living as a reference standard for animal welfare assessment It may be concluded from the previous reviews (Mellor 2015a, b) that an animal which is fully engaged by exploring and food gathering in stimulus-rich environments and by interacting pleasantly with other animals in its social group may experience intrinsic, deeply embedded feelings of reward. It may also be concluded that without such diverse engagement the animal could not experience the full range of positive welfare states that are potentially available to it. This highlights the importance of providing opportunities for animals to undertake such activities, a view that is in harmony with the natural living orientation towards animal welfare (Fraser 2003). This orientation incorporates the notion that the closer an animal’s surroundings and social circumstances are to those pertaining in its natural, wild or ancestral environment, the more it will be able to express its species-specific behaviours and the better its welfare may be (Dawkins 1998; Spinka 2006; Fraser 2008a). The account given in the second review (Mellor 2015b) reinforces this idea by providing examples of the important neurosciencesupported behaviour-based proposition that deeply felt feelings of reward, understood in terms of positive affective engagement, may be integral to good states of welfare generated in this way. Understood thus, natural living is a helpful concept because it points towards the best that such behavioural freedom might achieve affectively on behalf of animals. But there is a caveat. It is that such an outcome may only be achieved in circumstances where the affective impacts of other factors that negatively affect welfare do not overshadow these benefits (Spinka 2006; Fraser 2008b; Mellor et al. 2009). In reality, however, they often do. It is well understood that in natural, rangeland or wild environments animals may be exposed to a wide range of challenges to their welfare (Fraser 2008b). At their extreme, these challenges include the frightening, debilitating, distressing, painful and/or fatal consequences of prolonged drought, fire, major weather events, severe nutritional inadequacies and overwhelming microbial, parasitic and other diseases, as well as traumatic injuries and, depending on the species, being a target for predation (Mellor et al. 2009). Animals may also experience neophobiainduced fear responses to unexpected changes in the environment (Berdoy 1994; Wemelsfelder and Birke 1997), distress and pain associated with injurious and/or fatal agonistic interactions with conspecifics (Masterton-Gibbons and Dugatkin 1995; Spinka 2006), and loneliness, depression or grief due to the death of, or lasting separation from, bonded others, including newborns, juveniles and adults (Panksepp 2003, 2010; Newberry and Swanson 2008). At times, therefore, animals living naturally without human intervention may experience significant suffering or misery, characterised by the experience of strongly negative affects. Of course, when animals are under human care or control, comprehensive management strategies are available to prevent or minimise both extreme and far less extreme welfare compromises, and they are often very successful in doing so (Mellor et al. 2009; Webster, 2011). Thus, it is widely considered that providing living circumstances that minimise compromise in nutritional, environmental, health, behavioural and mental domains of
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welfare (Deag 1996; Broom and Fraser 2007; Mellor et al. 2009), is far more important than keeping animals in replicated natural or wild environments (Claxton 2011). Indeed, at its best, human participation in the lives of domesticated animals may be seen to make major contributions to their capacity to have generally positive lives (Anonymous 2009; Green and Mellor 2011). Thus, the limited focus of the natural living orientation on the benefits of behavioural freedom restricts its usefulness as an allembracing and definitive benchmark for the best ways to keep and manage animals (Spinka 2006). It may be anticipated, however, that this orientation will continue to aid the identification of practices that should be avoided, discontinued or substantially modified (Mellor 2015b). This is because the neuroscience explanations of how such practices may generate strong negative affects (Panksepp 2005; Boissy et al. 2007; Rolls 2007), in supporting previous predominantly behaviourbased conclusions (Dawkins 2006; Kirkden and Pajor 2006; Mason and Rushen 2006), should help to ensure that, henceforth, natural living evaluations of this type will carry greater weight.
Animal welfare assessment using baseline reference standards Past regulatory improvements in animal welfare have been achieved mainly by defining and then progressively increasing minimum, or baseline, welfare standards in a process described as incremental improvement (Mellor and Stafford 2001; Anonymous 2009). Pragmatically, suggested or required increments have often been kept small in order to engage and then retain the willing participation of those whose management of animals was being regulated, including, in commercial contexts, livestock producers (Mellor and Bayvel 2004, 2008). Nevertheless, each such increment achieved did indicate a sector’s commitment to this process and, despite being small, was openly acknowledged as worthwhile (Mellor and Stafford 2001). Nevertheless, this approach raises an area of potential concern. Using the lowest acceptable standard of the time as the reference point might have enticed those involved to regard small improvements as being of greater significance than would have been the case had the comparison been with a higher standard. For example, keeping sows confined at high densities in group pens on bare concrete surrounded by solid partitions may be judged to be an improvement on very close individual confinement in gestation stalls, but would be considered to be less acceptable than group housing in larger pens on fresh deep litter to encourage rooting and at low enough densities to allow each sow to move freely. The inadequacy of both gestation stalls and cramped featureless group pens is re-emphasised by the increasing neuroscience support for prior behaviour-based conclusions regarding the significance of the welfare deprivations imposed by confining animals in impoverished environments (Mellor 2012a). Judged thus, a change from individual stalls to such group pens clearly would not advance sow welfare sufficiently to obviate the need to continue efforts to make much greater improvements. These observations raise the question of how much space and what environmental and social conditions would provide an acceptable level of stimulation. One approach has been to evaluate
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enrichment initiatives by how much they eliminate or markedly reduce stereotypical behaviours compared to their incidence in non-enriched conditions (Mason and Latham 2004; Mason and Rushen 2006). This approach has certainly led to some welfare improvements. However, stereotypies may not be fully informative as indices because, individually or collectively, their aetiology is complex (Mason and Latham 2004; Mason and Rushen 2006) and they may access some aspects of impoverishment-induced welfare compromise, and not others. Moreover, if it were established that the welfare deprivations indicated by stereotypies were located mainly towards the strongly negative end of the welfare-suffering continuum, their use would leave undetected somewhat less severe welfare compromises which would also be of significant concern. Additional complementary approaches help to fill such gaps. One in common use is to determine whether enrichment also increases desirable behaviours such as exploration and play (Mason and Latham 2004; Mason et al. 2007). The matters considered in the second review (Mellor 2015b) suggest that an increased incidence of affiliative behaviours in addition to play might also be informative in this regard. A second approach involves skilled observers undertaking evaluations of the demeanour, appearance and activity of animals using what Wemelsfelder called Qualitative Behavioural Assessment (QBA) (Wemelsfelder 1997, 2007; Wemelsfelder et al. 2001). QBA formally describes, and potentially enhances, what for decades have been conducted as routine experience-based assessments by veterinarians, animal-based scientists, stock handlers, informed pet owners and others who have daily engagement with animals in clinical, production, scientific, domestic and other contexts (Anonymous 2009; Wathes 2010). To date, indices of negative welfare impacts such as depressive non-responsiveness and increased aggression have usually been detected in this way (Stevenson 1983; Wood-Gush and Vestergaard 1989). The conceptual foundation of such qualitative judgments is that they constitute an integrated whole animal perspective that recognises behaviour as being a dynamically expressive body language that provides a consistent basis for assessing the quality of an animal’s experience (Wemelsfelder 2007). It is suggested here that as understanding of the neuroscience/behaviour nexus improves it may help to support QBA both conceptually and as a formal methodology by providing a clearer indication of the limits of its application. Finally, a third approach, described in detail elsewhere (Mellor et al. 2009; Green and Mellor 2011; Beausoleil and Mellor 2012), is to make assessments of welfare status using the Five Domains model (Mellor and Reid 1994; Mellor 2004). Such assessments focus on well-established linkages between physical/ functional states and affective states such as hypercapnia leading to breathlessness, dehydration to thirst, negative energy balance to hunger, injury to pain, and a markedly restricted capacity to explore and forage to frustration or depressive withdrawal (Mellor 2012b). Using this model, differentiation of four physical/functional domains enables the potential impacts of nutritional, environmental, health and behavioural states on the associated affective experiences animals may have to be evaluated systematically within a fifth mental domain (Mellor et al. 2009). The effects of these mental impacts are taken to represent key facets of the animals’ welfare state. The Five Domains assessment model has been used in New Zealand since 1997 to rank the anticipated and observed negative
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impacts of every scientific procedure conducted on living mammals, birds and other vertebrates (Williams et al. 2006). It may also be applied to welfare assessments of the wide range of animals used or managed by people for other purposes, including farming, companionship, recreation, sports, service and motive power (Mellor et al. 2009). And finally, adaptations of the model have been developed to assess the acceptability or otherwise of vertebrate pest control methods in Australia (Sharp and Saunders 2008) and New Zealand (Beausoleil et al. 2012a), and have also been incorporated into a position statement focused on promoting positive welfare states in zoo and aquarium animals (Portas 2013). As the Five Domains approach and QBA have complementary strengths, it has been suggested that combining them would enhance welfare assessments (Beausoleil and Mellor 2012). In conclusion, the regulatory setting of baseline or minimum standards is intended to ensure that the welfare of animals managed to those standards will be acceptable (Mellor and Bayvel 2004, 2008). However, as most such standards in current codes of practice or welfare focus mainly on minimising or at best neutralising largely homeostasis-related negative affects by providing only the basic necessities of life, they alone can do little to promote positive welfare states (Mellor 2012a). This observation, and the capacity of animals to experience a range of positive affects (e.g. Fraser 2008b; Yeates and Main 2008; Mellor 2015a), suggest that minimum code standards should be expanded to at least include what are currently optional best practice recommendations that would provide greater opportunities for animals to experience positive affects. Some initiatives of this type are apparent, for example in Europe (Anonymous 2010a), New Zealand (Anonymous 2005, 2012) and the United States of America (Anonymous 2011). There is a clear need for such code enhancement to be accelerated, because, when judged in terms of opportunities to experience positive affects, the best welfare states achievable by full compliance with most present code minima may be rated as unacceptable.
What animals want as a welfare reference standard The discussion so far has emphasised behavioural indices of affective responses to stimulus-rich, somewhat enriched or impoverished environments. An alternative approach is to ascertain what animals want to achieve or avoid by applying behavioural tests aimed at revealing particular conditions they find rewarding or unpleasant (Dawkins 2006; Kirkden and Pajor 2006; Fraser 2008b). The appeal of this approach is that it offers the prospect of identifying specific resources or conditions that animals would choose themselves. These could then become candidates for use in improving their welfare to a greater extent than the approach of making small increments above minimum or baseline standards. The methodology involves tests to assess animals’ preferences and motivation, defined operationally as the tendency for them to perform a particular behaviour, but understood as reflecting their desire to behave in that way (Kirkden and Pajor 2006). Many of the design-specific subtleties and pitfalls of interpreting the outcomes of such tests have been clarified progressively over the 40 years since their introduction, and this has provided an increasingly secure conceptual foundation for their current use
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(Fraser, 2008b). In depth assessment of animals’ wants is now understood to require that four distinct research questions be addressed (Kirkden and Pajor 2006): first, whether an animal is motivated to obtain or avoid a particular resource, i.e. what the animal wants or does not want; second, whether it has a preference amongst alternative resources presented together, i.e. choosing what it wants among two or more options; third, how strong its motivation or preference is, i.e. how much it wants a resource; and fourth, whether its preference per se, or the strength of its preference, is altered by changes in its internal or external environment, i.e. the impacts of internal or external factors on its “wanting”. Some examples of resources that have been investigated and, in some cases, are well demonstrated as preferred by different species, are presented in Table 1. Of course, a key factor in deciding which resources should be provided in addition to basics such as water and food is the relative strength of animals’ preferences for each one, which represents a combination of the second and third questions above, but significant conceptual and experimental design complexities remain and may hinder interpretation of the results (Dawkins 1990; Kirkden et al. 2003; Kirkden and Pajor 2006; Richter et al. 2010). Nevertheless, it appears that methods for rigorously demonstrating animals’ preferences, aversions and priorities have already led to significant changes in resource provision and management strategies directed at welfare improvement (e.g. Anonymous 2010a, 2011, 2013) and that they may become even more influential after further development (Kirkden and Pajor 2006). A criticism of the notion of wants is that animals may not distinguish between welfare-enhancing preferences and those that are not in their long-term best interests (Webster 1994; Yeates and Main 2008) resulting, for example, in obesity-induced ill health in pet dogs that are allowed to over eat. A related concern, specifically regarding commercial livestock enterprises, is that poorly defined minimum standards based on wants may lead to unnecessary production costs. In the present context,
Table 1. Some preferences of different species for particular resources that have been investigated which have influenced thinking about their welfare management. Species Layer hens
Food, perches, scratch pads, nest boxes, dust runs Cool floors in hot weather, straw-insulated floors in cold weather, access to substrate for rooting or nest building, group housing
Dairy cows
Bedding material, opportunity to rest, shade in hot
Beef cattle
Soft as opposed to hard slatted flooring
Blue foxes
Sand floor, nest box, gnawing bones, extra space
weather
(Vulpes lagopus) Mink (Mustela vison) Mice and rats
however, the term wants is taken to mean an animal’s expectations of being rewarded allied to its potential to experience particular types of positive affects (Mellor 2015a). Thus, provided that significant medium- and long-term harm can be ruled out, giving animals opportunities to behave in ways that achieve such wanted positive affects would be welfare enhancing. Understood in this way, determining what animals want is relevant to both commercial and non-commercial contexts.
Cognitive bias assessment and animal welfare status Interest has been growing recently in the assessment of cognitive bias in animals. The term originates from human psychological research (Paul et al. 2005). It refers to effects of affective state on cognitive processes, showing, for example, that negative emotional states may be accompanied by greater attention to threatening stimuli and more pessimistic interpretations of ambiguous information, whereas positive states may be accompanied by more optimistic judgements (Paul et al. 2005; Mendl et al. 2009). Conceptual and methodological approaches to experimental design have been developed for animal studies (Paul et al. 2005; Mendl et al. 2009, 2010b). However, it seems likely that these approaches will be modified as their limitations are explored further (Doyle et al. 2010a, 2010b, 2011), as potentially confounding impacts of genetically determined differences in temperament are investigated (Beausoleil et al. 2008, 2012b), and as they are used in additional contexts or species (Mendl et al. 2010a; Bethell et al. 2012; Douglas et al. 2012). Further validation therefore appears to be merited, notwithstanding some behavioural evidence that is consistent with the potential for such cognitive biases to exist in a range of species, including rhesus monkeys, dogs, pigs, sheep and domestic chickens (for references see: Mendl et al. 2009, 2010a; Bethell et al. 2012; Douglas et al. 2012). If such validation were to be forthcoming, demonstrating the presence of positive or negative cognitive biases in particular circumstances could provide an additional means of determining the acceptability or otherwise of different animal management systems.
Preferred resources
bathing substrate, litter-covered floors, outdoor Pigs
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Use of a tunnel, raised observation platform, alternative nest box or a small swimming pool Food, options for exercise, nest building substrate, social contact
Sources: Matthews and Ladewig 1987; Fraser and Matthews 1997; Widowski and Duncan 2000; Mason et al. 2001; Balcombe 2006; Kendall et al. 2006; Fraser 2008b; Koistinen et al. 2009a, 2009b; Arnold and Matthews 2010; Wechsler 2007, 2011.
Discussion The growing neuroscience support for behavioural science inferences regarding the wide range of affective experiences animals may have (Panksepp 2005; Boissy et al. 2007) has made it increasingly apparent that sentient animals are potentially much more sensitive to their environmental and social circumstances than was previously thought to be the case. Thus, while acknowledging that welfare trade-offs are virtually inevitable when managing animals for human purposes (Fraser 2008b; Mellor et al. 2009; Webster 2011), it seems likely that both the range and magnitude of some trade-offs have been underestimated even when minimalistic but arguably well-intentioned attempts have been made to maintain high levels of welfare. The present analysis, supported by the two previous reviews (Mellor 2015a, b), suggests that this may be the case in particular with regard to animals having limited opportunities to engage in welfare-enhancing exploratory, foraging and affiliative behaviours, and therefore that, often, the benefits of them experiencing related positive affective
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engagement have unwittingly been neglected. It follows that welfare reference standards should now be chosen to more strongly reflect a need for such opportunities to be provided.
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Revisions to regulatory welfare codes, when they occur, usually include some worthwhile increments in minimum standards, the magnitudes of which vary with the animal-use sector involved. For example, parts of the intensive farming sector have often resisted all but quite limited environmental enrichment initiatives, viewing many of them as scientifically unsupported, impractical, and potentially costly impositions. This raises a question for policy makers: Is merely meeting the survival needs of farm animals by only addressing their homeostasis-related negative affects a supportable benchmark for determining minimum welfare standards? A clear implication of the present analysis, and those of others (Yeates and Main 2008), is that it is not, and that providing opportunities for animals to experience more of the positive affects of which they are capable must be given greater attention. There have been some recent promising developments of this type in New Zealand, in line with similar ones elsewhere (e.g. Anonymous 2010a, 2011). For example, group housing of sows, which allows better behavioural expression, is set to replace gestation stalls (Anonymous 2010b). Also in progress is a phased replacement of conventional cages with much larger colony cages having height, floor area and “furnishing” standards that will enable layer hens to engage in a wider range of their natural behaviours (Anonymous 2012, 2013). In contrast to the intensive farming sector, the zoo and aquarium sector in Australasia is already strongly committed to environmental enrichment to mitigate negative impacts of the confinement management of many of their species (e.g. Anonymous 2005). Moreover, this sector has recently made policy decisions based on some of the present insights to re-evaluate and, wherever practicable, to further improve their enrichment procedures (Portas 2013). Extensive grazing of pastorally farmed deer, goats, sheep and beef cattle potentially offers them more opportunities to engage in behaviours that may be accompanied by positive exploratory, foraging and affiliative affects. This is beneficial from a welfare perspective. However, the negative affective impacts of conditions such as extreme weather events and protracted drought (see above), when they occur, would act to overshadow such positive affects. Accordingly, the welfare codes for these species rightly give significant attention to the avoidance or mitigation of such imposts. Of course, some outdoor grazing systems are in fact forms of intensive management and cannot easily secure such welfare benefits. A good example is strip grazing of animals at high densities behind electric fences in order to make efficient use of pasture or root crops. The laudable intention here is to maintain higher nutritional levels over longer periods. However, the welfare benefits of this might be negated by space restrictions limiting freely ranging exploration and foraging, and by the potential for hunger levels to rise markedly if the pasture or other forages are allowed to be consumed almost completely before the animals are given access to the next strip. Consideration should be given to expanding Code standards to address such concerns. The framing of codes of welfare in terms that accommodate the production complexities of each farming or management system and incorporate sufficient validated current understanding of the determinants of acceptable welfare states is well known to be an
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extremely complex enterprise (Mellor and Bayvel 2004, 2008; Fraser 2008b). The foregoing analysis suggests that the following questions might assist when considering initiatives to promote positive welfare states. To what extent have carefully considered natural living perspectives ruled out unacceptable approaches and ruled in validated greater opportunities for animals to experience positive affective engagement? Have the benchmark comparators for baseline or minimum standards been set high enough to achieve meaningful and not merely cosmetic improvements in environmental conditions? How has understanding of what animals want, based on neuroscience/behaviour science support for their preferences, aversions and priorities, been incorporated into standards that relate in particular to environment-focused and animal-to-animal interactive behaviours? An additional set of such questions may be derived from a combination of the Farm Animal Welfare Council characterisation of what would constitute a good life for animals (Anonymous 2009) and related implications of the present analysis. Overall, what opportunities have been provided for the animals’ comfort, pleasure, interest and confidence? More specifically, what provisions have been made to ensure that consuming the food provided will be an enjoyable experience? How will expressions of normal behaviour be encouraged and harmless wants met? What environmental choices will be available that will encourage exploratory and food acquisition activities which are rewarding? And what provisions have been made to enable social species to engage in bonding and bond affirming activities and, as appropriate, other affiliative interactions such as maternal and group care of young, play behaviour and sexual activity? Recently, the quality of life of animals has been characterised in terms of a four-tier scale, i.e. a life not worth living, a life worth avoiding, a life worth living and a good life (Green and Mellor 2011; Yeates 2011). It is suggested here that using the questions outlined above to modulate the application of different reference standards to the formulation of welfare codes would help to ensure that animals have more opportunities to experience satisfying, rewarding or pleasurable affects, and this could offer a means to transform lives otherwise dominated by negative experiences into lives worth living and, preferably, good lives.
Acknowledgements I am indebted to the following colleagues who assisted during the preparation of this paper: in New Zealand, Ngaio Beausoleil, Corrin Hulls, Craig Johnson, Nikki Kells and Kevin Stafford (Massey University), Mark Fisher and Cheryl O’Connor (Ministry for Primary Industries), and Jim Webster (AgResearch); in Australia, Andrew Fisher, Paul Hemsworth, Ellen Jongman and Jean-Loup Rault (Animal Welfare Science Centre, Melbourne) and Susan Hazel (University of Adelaide); and in Canada, David Fraser (Animal Welfare Program, University of British Columbia).
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*Fraser D, Matthews LR. Preference and motivation testing. In: Appleby MC, Hughes BO (eds). Animal Welfare. Pp 159–73. CAB International, Wallingford, UK, 1997 Green TC, Mellor DJ. Extending ideas about animal welfare assessment to include “quality of life” and related concepts. New Zealand Veterinary Journal 59, 316– 24, 2011 Kendall PE, Nielsen PP, Webster JR, Verkerk GA, Littlejohn RP, Matthews LR. The effects of providing shade to lactating dairy cows in a temperate climate. Livestock Science 103, 148–57, 2006 Kirkden RD, Edwards JSS, Broom DM. A theoretical comparison of the consumer surplus and the elasticities of demand as measures of motivational strength. Animal Behaviour 65, 157–78, 2003 Kirkden RD, Pajor EA. Using preference, motivation and aversion tests to ask scientific questions about animals’ feelings. Applied Animal Behaviour Science 100, 29–47, 2006 Koistinen T, Orjala H, Mononen J, Korhonen HT. Position of operant cost affects blue foxes’ time budget between sand floor and mesh floor. Applied Animal Behaviour Science 116, 266–72, 2009a Koistinen T, Jauhiainen L, Korhonen HT. Relative value of a nest box, sand floor and extra space during the breeding season in adult blue fox males. Applied Animal Behaviour Science 120, 192–200, 2009b Mason GJ, Latham N. Can’t stop, won’t stop: Is stereotypy a reliable animal welfare indicator? Animal Welfare 13, 57–69, 2004 *Mason G, Rushen J. Stereotypic Animal Behaviour: Fundamentals and Implications for Animal Welfare. 2nd Edtn. CAB International, Wallingford, UK, 2006 Mason GJ, Cooper JJ, Clarebrough C. Frustrations of fur-farmed mink. Nature 410, 35–36, 2001 Mason G, Clubb R, Latham N, Vickery S. Why and how should we use environmental enrichment to tackle stereotypic behaviour? Applied Animal Behaviour Science 102, 163–88, 2007 Masterton-Gibbons M, Dugatkin LA. Towards a theory of dominance hierarchies: Effects of assessment, group size and variation in fighting ability. Behavioral Ecology 6, 416–23, 1995 Matthews LR, Ladewig J. Stimulus requirements of housed pigs assessed by behavioural demand functions. Applied Animal Behaviour Science 17, 365– 83, 1987 *Mellor DJ. Comprehensive assessment of harms caused by experimental, teaching and testing procedures on live animals. Alternatives to Laboratory Animals 32 (Supplement 1), 453–7, 2004 Mellor DJ. Animal emotions, behaviour and the promotion of positive welfare states. New Zealand Veterinary Journal 60, 1–8, 2012a *Mellor DJ. Affective states and the assessment of laboratory-induced animal welfare impacts. Alternatives to Animal Experimentation (ALTEX) 29 (Special Issue), 445–9, 2012b Mellor DJ. Enhancing animal welfare by creating opportunities for positive affective engagement. New Zealand Veterinary Journal, 63, 3–8, 2015a Mellor DJ. Positive animal welfare states and encouraging environment-focused and animal-to-animal interactive behaviours. New Zealand Veterinary Journal, 63, 9–16, 2015b *Mellor DJ, Bayvel ACD. Application of legislation, scientific guidelines and codified standards to advancing animal welfare. In: Global Conference on Animal Welfare: An OIE initiative. Pp 249–59, Proceedings of an OIE Conference, Paris, France, 2004 Mellor DJ, Bayvel ACD. New Zealand’s inclusive science-based system for setting animal welfare standards. Applied Animal Behaviour Science 113, 313–29, 2008 *Mellor DJ, Reid CSW. Concepts of animal well-being and predicting the impact of procedures on experimental animals. In: Baker R, Jenkin G, Mellor DJ (eds). Improving the Well-being of Animals in the Research Environment. Pp 3–18. Australian and New Zealand Council for the Care of Animals in Research and Teaching, Glen Osmond, South Australia, 1994 Mellor DJ, Stafford KJ. Integrating practical, regulatory and ethical strategies for enhancing farm animal welfare. Australian Veterinary Journal 79, 762–8, 2001 *Mellor DJ, Patterson-Kane E, Stafford KJ. The Sciences of Animal Welfare. Pp 3– 94. Wiley-Blackwell, Oxford, UK, 2009 Mendl M, Burman OHP, Parker RMA, Paul ES. Cognitive bias as an indicator of animal emotion and welfare: Emerging evidence and underlying mechanisms. Applied Animal Behaviour Science 118, 161–81, 2009 Mendl M, Brooks J, Basse C, Burman O, Paul E, Blackwell E, Casey R. Dogs showing separation-related behaviour exhibit a “pessimistic” cognitive bias. Current Biology 20, R839–40, 2010a
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Mendl M, Burman OHP, Paul ES. An integrative and functional framework to the study of animal emotion and mood. Proceedings of the Royal Society B: Biological Sciences 277, 2895–904, 2010b Newberry RC, Swanson JC. Implications of breaking mother-young social bonds. Applied Animal Behaviour Science 110, 2–23, 2008 Panksepp J. Feeling the pain of social loss. Science 302, 237–9, 2003 Panksepp J. Affective consciousness: Core emotional feelings in animals and humans. Consciousness and Cognition 14, 30–80, 2005 Panksepp J. Affective neuroscience of the emotional brainmind: Evolutionary perspectives and implications for understanding depression. Dialogues in Clinical Neuroscience 112, 383–99, 2010 Paul ES, Harding EJ, Mendl M. Measuring emotional processes in animals: The utility of a cognitive approach. Neuroscience and Biobehavioral Reviews 29, 469– 91, 2005 *Portas T. Achieving positive animal welfare outcomes in zoos and aquariums. In: When coping is not enough: Promoting positive welfare states in animals. Pp 46– 50. RSPCA Scientific Seminar 2013 Proceedings, RSPCA Australia, Canberra, 2013 Richter SH, Garner JP, Auer C, Kunert J, Würbel H. Systematic variation improves reproducibility of animal experiments. Nature Methods 7, 167–8, 2010 *Rolls ET. Emotion Explained. Oxford University Press, Oxford, UK, 2007 *Sharp T, Saunders G. A model for assessing the relative humaneness of pest animal control methods. Australian Government Department of Agriculture, Fisheries and Forestry, Canberra, Australia, 2008 Spinka M. How important is natural behaviour in animal farming systems? Applied Animal Behaviour Science 100, 117–28, 2006 *Stevenson M. The captive environment: Its effect on exploratory and related behavioural responses in wild animals. In: Archer J, Birke L (eds). Exploration in Animals and Humans. Pp 176–97. Nan Nostrand Reinhold, Wokingham, UK, 1983 *Wathes C. Lives worth living? Veterinary Record 166, 468–9, 2010 *Webster J. Animal Welfare: A Cool Eye Towards Eden. Blackwell, Oxford, UK, 1994
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*Webster J. Management and Welfare of Farm Animals: UFAW Farm Handbook. 5th Edtn. Wiley-Blackwell, Oxford, UK, 2011 Wechsler B. Normal behaviour as a basis for animal welfare assessment. Animal Welfare 16, 107–10, 2007 Wechsler B. Floor quality and space allowance in intensive beef production: a review. Animal Welfare 20, 487–503, 2011 Wemelsfelder F. The scientific validity of subjective concepts in models of animal welfare. Applied Animal Behaviour Science 53, 75–88, 1997 Wemelsfelder F. How animals communicate quality of life: The qualitative assessment of behaviour. Animal Welfare 16 (Supplement 1), 25–31, 2007 *Wemelsfelder F, Birke L. Environmental challenge. In: Appleby MC, Hughes BO (eds). Animal Welfare. Pp 35–47. CAB International, Wallingford, UK, 1997 Wemelsfelder F, Hunter TEA, Mendl MT, Lawrence AB. Assessing the “whole animal”: A free choice profiling approach. Animal Behaviour 62, 209–20, 2001 Widowski TM, Duncan IJH. Working for a dustbath: Are hens increasing pleasure rather than reducing suffering? Applied Animal Behaviour Science 68, 39–53, 2000 *Williams VM, Mellor DJ, Marbrook J. Revision of a scale for assessing the severity of live animal manipulations. Alternatives to Animal Experimentation (ALTEX) 23 (Special Issue), 163–19, 2006 Wood-Gush DGM, Vestergaard K. Exploratory behavior and the welfare of intensively kept animals. Journal of Agricultural Ethics 2, 161–9, 1989 Yeates JW. Is “a life worth living” a concept worth having? Animal Welfare 20, 397–406, 2011 Yeates JW, Main DCJ. Assessment of positive welfare: A review. The Veterinary Journal 175, 293–300, 2008
Submitted 6 June 2013 Accepted for publication 14 May 2014 First published online 30 May 2014
*Non-peer-reviewed
New Zealand Veterinary Journal Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/tnzv20
Positive animal welfare states and reference standards for welfare assessment DJ Mellor
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Animal Welfare Science and Bioethics Centre, PN453, Massey University, Palmerston North 4442, New Zealand Accepted author version posted online: 30 May 2014.Published online: 18 Aug 2014.
Click for updates To cite this article: DJ Mellor (2015) Positive animal welfare states and reference standards for welfare assessment, New Zealand Veterinary Journal, 63:1, 17-23, DOI: 10.1080/00480169.2014.926802 To link to this article: http://dx.doi.org/10.1080/00480169.2014.926802
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New Zealand Veterinary Journal 63(1), 17–23, 2015
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Review Article
Positive animal welfare states and reference standards for welfare assessment
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DJ Mellor*§
Abstract
Introduction
Developments in affective neuroscience and behavioural science during the last 10–15 years have together made it increasingly apparent that sentient animals are potentially much more sensitive to their environmental and social circumstances than was previously thought to be the case. It therefore seems likely that both the range and magnitude of welfare trade-offs that occur when animals are managed for human purposes have been underestimated even when minimalistic but arguably well-intentioned attempts have been made to maintain high levels of welfare. In light of these neuroscience-supported behaviour-based insights, the present review considers the extent to which the use of currently available reference standards might draw attention to these previously neglected areas of concern. It is concluded that the natural living orientation cannot provide an all-embracing or definitive welfare benchmark because of its primary focus on behavioural freedom. However assessments of this type, supported by neuroscience insights into behavioural motivation, may now carry greater weight when used to identify management practices that should be avoided, discontinued or substantially modified. Using currently accepted baseline standards as welfare reference points may result in small changes being accorded greater significance than would be the case if they were compared with higher standards, and this could slow the progress towards better levels of welfare. On the other hand, using “what animals want” as a reference standard has the appeal of focusing on the specific resources or conditions the animals would choose themselves and can potentially improve their welfare more quickly than the approach of making small increments above baseline standards. It is concluded that the cautious use of these approaches in different combinations could lead to recommendations that would more effectively promote positive welfare states in hitherto neglected areas of concern.
The present review is the last in a series of three that is intended to assist veterinarians, animal-based scientists and others to update and extend their animal welfare science knowledge, especially with regard to the promotion of positive welfare states in animals. The first review provides a brief non-technical outline of contributions of affective neuroscience and behavioural science to understanding positive welfare states and introduces the new concept of positive affective engagement which encapsulates the experiences animals may have when they are successfully undertaking rewarding goal-directed behaviours (Mellor 2015a). Furthermore, it expands on previous accounts of neuroscience support for interpreting the behaviour of animals in terms of what they may intend to achieve, i.e. their goals, and the positive or negative affects that may accompany such behaviours when they succeed or fail to achieve those goals (Panksepp 2005; Boissy et al. 2007).
KEY WORDS: Affective neuroscience, natural living, baseline standards, what animals want, cognitive bias, reference standards, positive welfare
* Animal Welfare Science and Bioethics Centre, PN453, Massey University, Palmerston North 4442, New Zealand § Author for correspondence. Email: [email protected] http://dx.doi.org/10.1080/00480169.2014.926802 © 2014 New Zealand Veterinary Association
In highlighting these points, the first review notes that scientific acceptance of the existence of particular affective states largely depends on a good understanding of the underlying neurological mechanisms (Mellor 2015a). It is argued, further, that an increasing knowledge of some other neurophysiological mechanisms may strengthen confidence in behaviour-based inferences about the character of various situation-related motivational affects, i.e. those associated with some environmental and social interactions, provided that such inferences are arrived at cautiously (Wemelsfelder 1997, 2007). The first review therefore sets the scene for the second one (Mellor 2015b), which describes environment-focused and animal-toanimal interactive behaviours, some of which are anticipated to involve positive affective engagement. It highlights the potentially widespread occurrence of such situation-related positive affects and contrasts them with the negative affects that may arise when animals do not have opportunities to engage in rewarding behaviours. The present review extends the previous two by analysing how greater confidence in inferences regarding the presence and nature of situation-related affects might guide the choice of reference standards used to differentiate between acceptable and unacceptable ways of managing animals. The reference standards considered are natural living, baseline standards and what animals want.
QBA
Qualitative behavioural assessment
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Natural living as a reference standard for animal welfare assessment It may be concluded from the previous reviews (Mellor 2015a, b) that an animal which is fully engaged by exploring and food gathering in stimulus-rich environments and by interacting pleasantly with other animals in its social group may experience intrinsic, deeply embedded feelings of reward. It may also be concluded that without such diverse engagement the animal could not experience the full range of positive welfare states that are potentially available to it. This highlights the importance of providing opportunities for animals to undertake such activities, a view that is in harmony with the natural living orientation towards animal welfare (Fraser 2003). This orientation incorporates the notion that the closer an animal’s surroundings and social circumstances are to those pertaining in its natural, wild or ancestral environment, the more it will be able to express its species-specific behaviours and the better its welfare may be (Dawkins 1998; Spinka 2006; Fraser 2008a). The account given in the second review (Mellor 2015b) reinforces this idea by providing examples of the important neurosciencesupported behaviour-based proposition that deeply felt feelings of reward, understood in terms of positive affective engagement, may be integral to good states of welfare generated in this way. Understood thus, natural living is a helpful concept because it points towards the best that such behavioural freedom might achieve affectively on behalf of animals. But there is a caveat. It is that such an outcome may only be achieved in circumstances where the affective impacts of other factors that negatively affect welfare do not overshadow these benefits (Spinka 2006; Fraser 2008b; Mellor et al. 2009). In reality, however, they often do. It is well understood that in natural, rangeland or wild environments animals may be exposed to a wide range of challenges to their welfare (Fraser 2008b). At their extreme, these challenges include the frightening, debilitating, distressing, painful and/or fatal consequences of prolonged drought, fire, major weather events, severe nutritional inadequacies and overwhelming microbial, parasitic and other diseases, as well as traumatic injuries and, depending on the species, being a target for predation (Mellor et al. 2009). Animals may also experience neophobiainduced fear responses to unexpected changes in the environment (Berdoy 1994; Wemelsfelder and Birke 1997), distress and pain associated with injurious and/or fatal agonistic interactions with conspecifics (Masterton-Gibbons and Dugatkin 1995; Spinka 2006), and loneliness, depression or grief due to the death of, or lasting separation from, bonded others, including newborns, juveniles and adults (Panksepp 2003, 2010; Newberry and Swanson 2008). At times, therefore, animals living naturally without human intervention may experience significant suffering or misery, characterised by the experience of strongly negative affects. Of course, when animals are under human care or control, comprehensive management strategies are available to prevent or minimise both extreme and far less extreme welfare compromises, and they are often very successful in doing so (Mellor et al. 2009; Webster, 2011). Thus, it is widely considered that providing living circumstances that minimise compromise in nutritional, environmental, health, behavioural and mental domains of
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welfare (Deag 1996; Broom and Fraser 2007; Mellor et al. 2009), is far more important than keeping animals in replicated natural or wild environments (Claxton 2011). Indeed, at its best, human participation in the lives of domesticated animals may be seen to make major contributions to their capacity to have generally positive lives (Anonymous 2009; Green and Mellor 2011). Thus, the limited focus of the natural living orientation on the benefits of behavioural freedom restricts its usefulness as an allembracing and definitive benchmark for the best ways to keep and manage animals (Spinka 2006). It may be anticipated, however, that this orientation will continue to aid the identification of practices that should be avoided, discontinued or substantially modified (Mellor 2015b). This is because the neuroscience explanations of how such practices may generate strong negative affects (Panksepp 2005; Boissy et al. 2007; Rolls 2007), in supporting previous predominantly behaviourbased conclusions (Dawkins 2006; Kirkden and Pajor 2006; Mason and Rushen 2006), should help to ensure that, henceforth, natural living evaluations of this type will carry greater weight.
Animal welfare assessment using baseline reference standards Past regulatory improvements in animal welfare have been achieved mainly by defining and then progressively increasing minimum, or baseline, welfare standards in a process described as incremental improvement (Mellor and Stafford 2001; Anonymous 2009). Pragmatically, suggested or required increments have often been kept small in order to engage and then retain the willing participation of those whose management of animals was being regulated, including, in commercial contexts, livestock producers (Mellor and Bayvel 2004, 2008). Nevertheless, each such increment achieved did indicate a sector’s commitment to this process and, despite being small, was openly acknowledged as worthwhile (Mellor and Stafford 2001). Nevertheless, this approach raises an area of potential concern. Using the lowest acceptable standard of the time as the reference point might have enticed those involved to regard small improvements as being of greater significance than would have been the case had the comparison been with a higher standard. For example, keeping sows confined at high densities in group pens on bare concrete surrounded by solid partitions may be judged to be an improvement on very close individual confinement in gestation stalls, but would be considered to be less acceptable than group housing in larger pens on fresh deep litter to encourage rooting and at low enough densities to allow each sow to move freely. The inadequacy of both gestation stalls and cramped featureless group pens is re-emphasised by the increasing neuroscience support for prior behaviour-based conclusions regarding the significance of the welfare deprivations imposed by confining animals in impoverished environments (Mellor 2012a). Judged thus, a change from individual stalls to such group pens clearly would not advance sow welfare sufficiently to obviate the need to continue efforts to make much greater improvements. These observations raise the question of how much space and what environmental and social conditions would provide an acceptable level of stimulation. One approach has been to evaluate
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enrichment initiatives by how much they eliminate or markedly reduce stereotypical behaviours compared to their incidence in non-enriched conditions (Mason and Latham 2004; Mason and Rushen 2006). This approach has certainly led to some welfare improvements. However, stereotypies may not be fully informative as indices because, individually or collectively, their aetiology is complex (Mason and Latham 2004; Mason and Rushen 2006) and they may access some aspects of impoverishment-induced welfare compromise, and not others. Moreover, if it were established that the welfare deprivations indicated by stereotypies were located mainly towards the strongly negative end of the welfare-suffering continuum, their use would leave undetected somewhat less severe welfare compromises which would also be of significant concern. Additional complementary approaches help to fill such gaps. One in common use is to determine whether enrichment also increases desirable behaviours such as exploration and play (Mason and Latham 2004; Mason et al. 2007). The matters considered in the second review (Mellor 2015b) suggest that an increased incidence of affiliative behaviours in addition to play might also be informative in this regard. A second approach involves skilled observers undertaking evaluations of the demeanour, appearance and activity of animals using what Wemelsfelder called Qualitative Behavioural Assessment (QBA) (Wemelsfelder 1997, 2007; Wemelsfelder et al. 2001). QBA formally describes, and potentially enhances, what for decades have been conducted as routine experience-based assessments by veterinarians, animal-based scientists, stock handlers, informed pet owners and others who have daily engagement with animals in clinical, production, scientific, domestic and other contexts (Anonymous 2009; Wathes 2010). To date, indices of negative welfare impacts such as depressive non-responsiveness and increased aggression have usually been detected in this way (Stevenson 1983; Wood-Gush and Vestergaard 1989). The conceptual foundation of such qualitative judgments is that they constitute an integrated whole animal perspective that recognises behaviour as being a dynamically expressive body language that provides a consistent basis for assessing the quality of an animal’s experience (Wemelsfelder 2007). It is suggested here that as understanding of the neuroscience/behaviour nexus improves it may help to support QBA both conceptually and as a formal methodology by providing a clearer indication of the limits of its application. Finally, a third approach, described in detail elsewhere (Mellor et al. 2009; Green and Mellor 2011; Beausoleil and Mellor 2012), is to make assessments of welfare status using the Five Domains model (Mellor and Reid 1994; Mellor 2004). Such assessments focus on well-established linkages between physical/ functional states and affective states such as hypercapnia leading to breathlessness, dehydration to thirst, negative energy balance to hunger, injury to pain, and a markedly restricted capacity to explore and forage to frustration or depressive withdrawal (Mellor 2012b). Using this model, differentiation of four physical/functional domains enables the potential impacts of nutritional, environmental, health and behavioural states on the associated affective experiences animals may have to be evaluated systematically within a fifth mental domain (Mellor et al. 2009). The effects of these mental impacts are taken to represent key facets of the animals’ welfare state. The Five Domains assessment model has been used in New Zealand since 1997 to rank the anticipated and observed negative
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impacts of every scientific procedure conducted on living mammals, birds and other vertebrates (Williams et al. 2006). It may also be applied to welfare assessments of the wide range of animals used or managed by people for other purposes, including farming, companionship, recreation, sports, service and motive power (Mellor et al. 2009). And finally, adaptations of the model have been developed to assess the acceptability or otherwise of vertebrate pest control methods in Australia (Sharp and Saunders 2008) and New Zealand (Beausoleil et al. 2012a), and have also been incorporated into a position statement focused on promoting positive welfare states in zoo and aquarium animals (Portas 2013). As the Five Domains approach and QBA have complementary strengths, it has been suggested that combining them would enhance welfare assessments (Beausoleil and Mellor 2012). In conclusion, the regulatory setting of baseline or minimum standards is intended to ensure that the welfare of animals managed to those standards will be acceptable (Mellor and Bayvel 2004, 2008). However, as most such standards in current codes of practice or welfare focus mainly on minimising or at best neutralising largely homeostasis-related negative affects by providing only the basic necessities of life, they alone can do little to promote positive welfare states (Mellor 2012a). This observation, and the capacity of animals to experience a range of positive affects (e.g. Fraser 2008b; Yeates and Main 2008; Mellor 2015a), suggest that minimum code standards should be expanded to at least include what are currently optional best practice recommendations that would provide greater opportunities for animals to experience positive affects. Some initiatives of this type are apparent, for example in Europe (Anonymous 2010a), New Zealand (Anonymous 2005, 2012) and the United States of America (Anonymous 2011). There is a clear need for such code enhancement to be accelerated, because, when judged in terms of opportunities to experience positive affects, the best welfare states achievable by full compliance with most present code minima may be rated as unacceptable.
What animals want as a welfare reference standard The discussion so far has emphasised behavioural indices of affective responses to stimulus-rich, somewhat enriched or impoverished environments. An alternative approach is to ascertain what animals want to achieve or avoid by applying behavioural tests aimed at revealing particular conditions they find rewarding or unpleasant (Dawkins 2006; Kirkden and Pajor 2006; Fraser 2008b). The appeal of this approach is that it offers the prospect of identifying specific resources or conditions that animals would choose themselves. These could then become candidates for use in improving their welfare to a greater extent than the approach of making small increments above minimum or baseline standards. The methodology involves tests to assess animals’ preferences and motivation, defined operationally as the tendency for them to perform a particular behaviour, but understood as reflecting their desire to behave in that way (Kirkden and Pajor 2006). Many of the design-specific subtleties and pitfalls of interpreting the outcomes of such tests have been clarified progressively over the 40 years since their introduction, and this has provided an increasingly secure conceptual foundation for their current use
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(Fraser, 2008b). In depth assessment of animals’ wants is now understood to require that four distinct research questions be addressed (Kirkden and Pajor 2006): first, whether an animal is motivated to obtain or avoid a particular resource, i.e. what the animal wants or does not want; second, whether it has a preference amongst alternative resources presented together, i.e. choosing what it wants among two or more options; third, how strong its motivation or preference is, i.e. how much it wants a resource; and fourth, whether its preference per se, or the strength of its preference, is altered by changes in its internal or external environment, i.e. the impacts of internal or external factors on its “wanting”. Some examples of resources that have been investigated and, in some cases, are well demonstrated as preferred by different species, are presented in Table 1. Of course, a key factor in deciding which resources should be provided in addition to basics such as water and food is the relative strength of animals’ preferences for each one, which represents a combination of the second and third questions above, but significant conceptual and experimental design complexities remain and may hinder interpretation of the results (Dawkins 1990; Kirkden et al. 2003; Kirkden and Pajor 2006; Richter et al. 2010). Nevertheless, it appears that methods for rigorously demonstrating animals’ preferences, aversions and priorities have already led to significant changes in resource provision and management strategies directed at welfare improvement (e.g. Anonymous 2010a, 2011, 2013) and that they may become even more influential after further development (Kirkden and Pajor 2006). A criticism of the notion of wants is that animals may not distinguish between welfare-enhancing preferences and those that are not in their long-term best interests (Webster 1994; Yeates and Main 2008) resulting, for example, in obesity-induced ill health in pet dogs that are allowed to over eat. A related concern, specifically regarding commercial livestock enterprises, is that poorly defined minimum standards based on wants may lead to unnecessary production costs. In the present context,
Table 1. Some preferences of different species for particular resources that have been investigated which have influenced thinking about their welfare management. Species Layer hens
Food, perches, scratch pads, nest boxes, dust runs Cool floors in hot weather, straw-insulated floors in cold weather, access to substrate for rooting or nest building, group housing
Dairy cows
Bedding material, opportunity to rest, shade in hot
Beef cattle
Soft as opposed to hard slatted flooring
Blue foxes
Sand floor, nest box, gnawing bones, extra space
weather
(Vulpes lagopus) Mink (Mustela vison) Mice and rats
however, the term wants is taken to mean an animal’s expectations of being rewarded allied to its potential to experience particular types of positive affects (Mellor 2015a). Thus, provided that significant medium- and long-term harm can be ruled out, giving animals opportunities to behave in ways that achieve such wanted positive affects would be welfare enhancing. Understood in this way, determining what animals want is relevant to both commercial and non-commercial contexts.
Cognitive bias assessment and animal welfare status Interest has been growing recently in the assessment of cognitive bias in animals. The term originates from human psychological research (Paul et al. 2005). It refers to effects of affective state on cognitive processes, showing, for example, that negative emotional states may be accompanied by greater attention to threatening stimuli and more pessimistic interpretations of ambiguous information, whereas positive states may be accompanied by more optimistic judgements (Paul et al. 2005; Mendl et al. 2009). Conceptual and methodological approaches to experimental design have been developed for animal studies (Paul et al. 2005; Mendl et al. 2009, 2010b). However, it seems likely that these approaches will be modified as their limitations are explored further (Doyle et al. 2010a, 2010b, 2011), as potentially confounding impacts of genetically determined differences in temperament are investigated (Beausoleil et al. 2008, 2012b), and as they are used in additional contexts or species (Mendl et al. 2010a; Bethell et al. 2012; Douglas et al. 2012). Further validation therefore appears to be merited, notwithstanding some behavioural evidence that is consistent with the potential for such cognitive biases to exist in a range of species, including rhesus monkeys, dogs, pigs, sheep and domestic chickens (for references see: Mendl et al. 2009, 2010a; Bethell et al. 2012; Douglas et al. 2012). If such validation were to be forthcoming, demonstrating the presence of positive or negative cognitive biases in particular circumstances could provide an additional means of determining the acceptability or otherwise of different animal management systems.
Preferred resources
bathing substrate, litter-covered floors, outdoor Pigs
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Use of a tunnel, raised observation platform, alternative nest box or a small swimming pool Food, options for exercise, nest building substrate, social contact
Sources: Matthews and Ladewig 1987; Fraser and Matthews 1997; Widowski and Duncan 2000; Mason et al. 2001; Balcombe 2006; Kendall et al. 2006; Fraser 2008b; Koistinen et al. 2009a, 2009b; Arnold and Matthews 2010; Wechsler 2007, 2011.
Discussion The growing neuroscience support for behavioural science inferences regarding the wide range of affective experiences animals may have (Panksepp 2005; Boissy et al. 2007) has made it increasingly apparent that sentient animals are potentially much more sensitive to their environmental and social circumstances than was previously thought to be the case. Thus, while acknowledging that welfare trade-offs are virtually inevitable when managing animals for human purposes (Fraser 2008b; Mellor et al. 2009; Webster 2011), it seems likely that both the range and magnitude of some trade-offs have been underestimated even when minimalistic but arguably well-intentioned attempts have been made to maintain high levels of welfare. The present analysis, supported by the two previous reviews (Mellor 2015a, b), suggests that this may be the case in particular with regard to animals having limited opportunities to engage in welfare-enhancing exploratory, foraging and affiliative behaviours, and therefore that, often, the benefits of them experiencing related positive affective
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engagement have unwittingly been neglected. It follows that welfare reference standards should now be chosen to more strongly reflect a need for such opportunities to be provided.
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Revisions to regulatory welfare codes, when they occur, usually include some worthwhile increments in minimum standards, the magnitudes of which vary with the animal-use sector involved. For example, parts of the intensive farming sector have often resisted all but quite limited environmental enrichment initiatives, viewing many of them as scientifically unsupported, impractical, and potentially costly impositions. This raises a question for policy makers: Is merely meeting the survival needs of farm animals by only addressing their homeostasis-related negative affects a supportable benchmark for determining minimum welfare standards? A clear implication of the present analysis, and those of others (Yeates and Main 2008), is that it is not, and that providing opportunities for animals to experience more of the positive affects of which they are capable must be given greater attention. There have been some recent promising developments of this type in New Zealand, in line with similar ones elsewhere (e.g. Anonymous 2010a, 2011). For example, group housing of sows, which allows better behavioural expression, is set to replace gestation stalls (Anonymous 2010b). Also in progress is a phased replacement of conventional cages with much larger colony cages having height, floor area and “furnishing” standards that will enable layer hens to engage in a wider range of their natural behaviours (Anonymous 2012, 2013). In contrast to the intensive farming sector, the zoo and aquarium sector in Australasia is already strongly committed to environmental enrichment to mitigate negative impacts of the confinement management of many of their species (e.g. Anonymous 2005). Moreover, this sector has recently made policy decisions based on some of the present insights to re-evaluate and, wherever practicable, to further improve their enrichment procedures (Portas 2013). Extensive grazing of pastorally farmed deer, goats, sheep and beef cattle potentially offers them more opportunities to engage in behaviours that may be accompanied by positive exploratory, foraging and affiliative affects. This is beneficial from a welfare perspective. However, the negative affective impacts of conditions such as extreme weather events and protracted drought (see above), when they occur, would act to overshadow such positive affects. Accordingly, the welfare codes for these species rightly give significant attention to the avoidance or mitigation of such imposts. Of course, some outdoor grazing systems are in fact forms of intensive management and cannot easily secure such welfare benefits. A good example is strip grazing of animals at high densities behind electric fences in order to make efficient use of pasture or root crops. The laudable intention here is to maintain higher nutritional levels over longer periods. However, the welfare benefits of this might be negated by space restrictions limiting freely ranging exploration and foraging, and by the potential for hunger levels to rise markedly if the pasture or other forages are allowed to be consumed almost completely before the animals are given access to the next strip. Consideration should be given to expanding Code standards to address such concerns. The framing of codes of welfare in terms that accommodate the production complexities of each farming or management system and incorporate sufficient validated current understanding of the determinants of acceptable welfare states is well known to be an
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extremely complex enterprise (Mellor and Bayvel 2004, 2008; Fraser 2008b). The foregoing analysis suggests that the following questions might assist when considering initiatives to promote positive welfare states. To what extent have carefully considered natural living perspectives ruled out unacceptable approaches and ruled in validated greater opportunities for animals to experience positive affective engagement? Have the benchmark comparators for baseline or minimum standards been set high enough to achieve meaningful and not merely cosmetic improvements in environmental conditions? How has understanding of what animals want, based on neuroscience/behaviour science support for their preferences, aversions and priorities, been incorporated into standards that relate in particular to environment-focused and animal-to-animal interactive behaviours? An additional set of such questions may be derived from a combination of the Farm Animal Welfare Council characterisation of what would constitute a good life for animals (Anonymous 2009) and related implications of the present analysis. Overall, what opportunities have been provided for the animals’ comfort, pleasure, interest and confidence? More specifically, what provisions have been made to ensure that consuming the food provided will be an enjoyable experience? How will expressions of normal behaviour be encouraged and harmless wants met? What environmental choices will be available that will encourage exploratory and food acquisition activities which are rewarding? And what provisions have been made to enable social species to engage in bonding and bond affirming activities and, as appropriate, other affiliative interactions such as maternal and group care of young, play behaviour and sexual activity? Recently, the quality of life of animals has been characterised in terms of a four-tier scale, i.e. a life not worth living, a life worth avoiding, a life worth living and a good life (Green and Mellor 2011; Yeates 2011). It is suggested here that using the questions outlined above to modulate the application of different reference standards to the formulation of welfare codes would help to ensure that animals have more opportunities to experience satisfying, rewarding or pleasurable affects, and this could offer a means to transform lives otherwise dominated by negative experiences into lives worth living and, preferably, good lives.
Acknowledgements I am indebted to the following colleagues who assisted during the preparation of this paper: in New Zealand, Ngaio Beausoleil, Corrin Hulls, Craig Johnson, Nikki Kells and Kevin Stafford (Massey University), Mark Fisher and Cheryl O’Connor (Ministry for Primary Industries), and Jim Webster (AgResearch); in Australia, Andrew Fisher, Paul Hemsworth, Ellen Jongman and Jean-Loup Rault (Animal Welfare Science Centre, Melbourne) and Susan Hazel (University of Adelaide); and in Canada, David Fraser (Animal Welfare Program, University of British Columbia).
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Submitted 6 June 2013 Accepted for publication 14 May 2014 First published online 30 May 2014
*Non-peer-reviewed
