This article was downloaded by: [Colorado College] On: 30 March 2015, At: 15:57 Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK
New Zealand Veterinary Journal Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/tnzv20
Scientific assessment of animal welfare a
b
c
PH Hemsworth , DJ Mellor , GM Cronin & AJ Tilbrook
ad
a
Animal Welfare Science Centre, University of Melbourne, Parkville, Victoria 3010, Australia b
Animal Welfare Science and Bioethics Centre, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North 4442, New Zealand c
Faculty of Veterinary Science, University of Sydney, Camden, NSW 2570, Australia
d
South Australian Research and Development Institute, University of Adelaide, Roseworthy, South Australia 5371, Australia Accepted author version posted online: 29 Sep 2014.Published online: 11 Dec 2014.
Click for updates To cite this article: PH Hemsworth, DJ Mellor, GM Cronin & AJ Tilbrook (2015) Scientific assessment of animal welfare, New Zealand Veterinary Journal, 63:1, 24-30, DOI: 10.1080/00480169.2014.966167 To link to this article: http://dx.doi.org/10.1080/00480169.2014.966167
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
24
New Zealand Veterinary Journal 63(1), 24–30, 2015
Review Article
Scientific assessment of animal welfare PH Hemsworth*§, DJ Mellor†, GM Cronin‡ and AJ Tilbrook*#
Downloaded by [Colorado College] at 15:57 30 March 2015
Abstract Animal welfare is a state within the animal and a scientific perspective provides methodologies for evidence-based assessment of an animal’s welfare. A simplistic definition of animal welfare might be how the animal feels now. Affective experiences including emotions, are subjective states so cannot be measured directly in animals, but there are informative indirect physiological and behavioural indices that can be cautiously used to interpret such experiences. This review enunciates several key science-based frameworks for understanding animal welfare. The biological functioning and affective state frameworks were initially seen as competing, but a recent more unified approach is that biological functioning is taken to include affective experiences and affective experiences are recognised as products of biological functioning, and knowledge of the dynamic interactions between the two is considered to be fundamental to managing and improving animal welfare. The value of these two frameworks in understanding the welfare of group-housed sows is reviewed. The majority of studies of the welfare of group-housed sows have employed the biological functioning framework to infer compromised sow welfare, on the basis that suboptimal biological functioning accompanies negative affective states such as sow hunger, pain, fear, helplessness, frustration and anger. Group housing facilitates social living, but group housing of gestating sows raises different welfare considerations to stall housing, such as high levels of aggression, injuries and stress, at least for several days after mixing, as well as subordinate sows being underfed due to competition at feeding. This paper highlights the challenges and potential opportunities for the continued improvement in sow management through well-focused research and multidisciplinary assessment of animal welfare. In future the management of sentient animals will require the promotion of positive affective experiences in animals and this is likely to be
* Animal Welfare Science Centre, University of Melbourne, Parkville, Victoria 3010, Australia † Animal Welfare Science and Bioethics Centre, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North 4442, New Zealand ‡ Faculty of Veterinary Science, University of Sydney, Camden, NSW 2570, Australia # South Australian Research and Development Institute, University of Adelaide, Roseworthy, South Australia 5371, Australia § Author for correspondence. Email: [email protected] http://dx.doi.org/10.1080/00480169.2014.966167 © 2014 New Zealand Veterinary Association
a major focus for animal welfare science activity in the early twenty-first century. KEY WORDS: Animal welfare, assessment, behaviour, stress, emotions, animal ethics, sow welfare
Introduction The publication of Ruth Harrison’s book “Animal Machines” in 1964 led to debate in many industrialised countries about the confinement of farm animals. In response the British Government established the Brambell Committee (Brambell et al. 1965) which defined welfare as a wide term that embraces both the physical and mental well-being of the animal. Furthermore, the Committee stated that “any attempt to evaluate welfare therefore must take into account the scientific evidence available concerning the feelings of animals that can be derived from their structure and functions and also from their behaviour.” Amongst its numerous recommendations, the Committee also called for research into veterinary medicine, stress physiology, animal science and, in particular, animal behaviour. The Brambell Committee thus provided an agenda for animal welfare science (Fraser 2008), which has over the subsequent 50 years, focused welfare research and in turn led to the recognition of a new discipline, animal welfare science. Science has an important role in underpinning societal decisions on animal use and the acceptability or otherwise of attendant conditions and compromises. Exclusion of science can result in emotive or self-interested arguments from sectional groups dominating community debate. This is not to say that such arguments should be ruled out; quite the reverse, as they reflect, in part, current community values. However, they should contribute to, not pre-empt, the debate (Hemsworth et al. 2007). Ultimately such questions are ethical ones in which scientific facts need to be considered together with other beliefs and principles if we are to formulate supportable answers (Levy 2004; Fisher and Mellor 2008; Mellor 2013). Of course, societal interests in animal welfare also include consideration of wider issues such as human health, economic and social implications, as well as environmental impacts (Fisher and Mellor 2008; Mellor and Bayvel 2008). Decisions on acceptable animal use can therefore involve difficult and complex choices and consequently they may remain controversial. This review aims to clarify various aspects of the current scientific understanding of animal welfare. It enunciates three science-based frameworks that have influenced the orientation of animal welfare assessments, and then illustrates briefly how two of these frameworks have been applied to improving the welfare of grouphoused sows. It ends by considering some of the significant challenges facing animal welfare science.
Hemsworth et al.
New Zealand Veterinary Journal, 2015
Science-based views of animal welfare A scientific perspective of animal welfare
Downloaded by [Colorado College] at 15:57 30 March 2015
Provided here is an integrated understanding of what animal welfare represents that is now widely accepted in the published literature (e.g. see reviews by Boissy et al. 2007; Mellor et al. 2009; Mellor 2012). Although management procedures applied to the animal or features of the animal’s environment may affect its welfare, animal welfare is a state within the animal. For an animal’s welfare to be affected, the animal must be sentient, i.e. it must have a brain with sufficient functional sophistication to transduce impulses in sensory and other nerves into experienced sensations. It is generally agreed that animal welfare relates to experienced sensations, so the animal must also be conscious (Mellor et al. 2009). These experiences arise as the integrated outcomes of sensory and other neural inputs from within the animal’s body and from its environment. These inputs are processed and interpreted by the animal’s brain according to its species-specific and individual nature, and its past experience. The integrated outcomes of this processing represent the animal’s current experience, i.e. its welfare status, and this changes as the balance and nature of the inputs change. These experiences are all subjective, varying in their emotional or affective contents and, based on human experience, are likely to include negative affective or emotional experiences such as breathlessness, thirst, hunger, nausea, pain and fear, and positive affective experiences such as satiety, contentment, companionship, curiosity and playfulness. Many of these experiences motivate animals to engage in behaviours that are critical for survival and thus also have longer-term welfare implications (Fraser and Duncan 1998). As subjective states they cannot be measured directly, but there are informative indirect indices of such experiences. These indices, which are based on established knowledge of physiological and behavioural responses to specific welfare challenges, have been critically evaluated as useful and relevant in many contexts (see reviews by Boissy et al. 2007; Mellor et al. 2009; Mellor 2012). Thus the welfare status of an animal at any one time may vary on a continuum between very bad to very good. Conceptual frameworks for assessment of animal welfare
There are basically three conceptual frameworks that are used to assess animal welfare, namely, biological functioning, affective state and natural living (Fraser 2003). It is of interest that these approaches use to varying degrees the disciplines that the Brambell Committee called for in assessing animal welfare (Brambell et al. 1965), i.e. veterinary medicine, stress physiology, animal science and particularly animal behaviour science. Biological functioning The rationale underpinning this conceptual framework is that difficult or inadequate adaptation will generate welfare problems for animals (Hemsworth and Coleman 2011). This concept aligns with the definition of Broom (1986, 2000) that the welfare of an animal is its state as regards its attempts to cope with its environment. This state refers to the extent of biological activity underlying attempts to cope, including the involvement of body repair systems, immunological defences and physiological stress responses, as well as a variety of behavioural responses. While research has led to a better understanding of the causation of these behavioural responses, such as stereotypies, redirected behaviours and displacement activities, the function and, thus,
25
adaptive significance of these behavioural responses are often poorly understood (Olsson et al. 2011; Lauber et al. 2012). The physiological stress responses to challenges are also varied and complex. Nonetheless, these responses nearly always include activation of the sympatho-adrenal medullary system and the hypothalamo-pituitary adrenal axis, with the consequent increase in synthesis of catecholamines and glucocorticoids, respectively (Turner et al. 2012). Further, this state in Broom’s definition refers to the extent to which these coping attempts are or are not succeeding, and this includes any biological costs to the animal, such as deterioration in growth efficiency, reproduction and health (injury or disease). Thus this conceptual framework emphasises that animals use a range of behavioural and physiological responses to assist them to cope with challenges, and while biological regulation in response to challenges occurs continuously, successful adaptation is not always possible (Barnett and Hemsworth 2009; Hemsworth and Coleman 2011). Marked challenges may overwhelm an individual’s capacity to adapt and lead to its death. However, less severe challenges can still have significant biological costs, leading to growth, reproductive, health and other impairments, which may reflect and/or result in welfare problems for the animal. Conceptualised in these terms, it is the biological cost of stress that is the key to understanding the associated welfare implications (Moberg 2000; Barnett 2003). How well an animal is coping with the challenges it faces will be reflected in the normality of its biological functioning and fitness, with severe risks to welfare associated with the most extreme coping attempts (Hemsworth and Coleman 2011). A common criticism of this conceptual framework in assessing animal welfare is that it does not adequately include emotions. This would only be valid if emotions are independent of other biological processes, but there is no doubt that emotions are associated with activations of both the sympatho-adrenal medullary and hypothalamo-pituitary adrenal axes (Dantzer 1988; Kaltas and Chrousos 2007). Affective state The second conceptual framework emphasises that the welfare of an animal derives from its capacity for affective experiences (Duncan and Fraser 1997). Thus, the welfare state is likely to be negative when the predominant affects experienced are unpleasant, and vice versa. However, affective experiences were considered to be inaccessible to scientific inquiry for many decades, a view that is being challenged by a growing body of evidence showing that brain structure and chemistry, and behaviour, are similar in humans and in a large number of animal species (Panksepp 2005; Boissy et al. 2007; Mellor 2015a). For example: other mammals are attracted to the same environmental rewards and drugs of abuse as humans; human and animal emotional experiences appear to depend on very similar sub-cortical brain systems situated in deep brain regions where evolutionarily homologous instinctual neural systems exist; and artificial activations of the deep brain systems elicit emotional actions that are liked and disliked by animals, as measured by a host of approach and avoidance responses (Panksepp 2005). This and other evidence contributes neuroscience support for cautiously interpreting particular animal behaviours in terms of an animal’s negative or positive affective experiences, such as, during the pursuit of its behavioural goals and failure or success in achieving those goals (Panksepp 2005). Importantly, it is also well recognised that such affective experiences are generated both by sensory inputs
26
New Zealand Veterinary Journal, 2015
Downloaded by [Colorado College] at 15:57 30 March 2015
that reflect the animal’s internal physical/functional state and by other sensory inputs that reflect the animal’s perception of its external circumstances (Denton et al. 2009; Mellor 2012, 2015a). Preference research, in which the strength of the preference for a chosen environmental option or the motivation to perform a type of behaviour are measured, has been used by some scientists to make inferences about animal welfare on the assumption that animals make choices that are in their best interest (Fraser and Nicol 2011). While it is likely that animals will avoid aversive stimuli and choose positive stimuli, caution is recommended in view of conceptual and methodological concerns that have been raised about the preference and motivation tests themselves (Nicol et al. 2009; Fraser and Nicol 2011). For example: familiarity with a resource may affect choice; a choice at one point in time may not reflect interactions of different motivational states over time; a positive resource may remind the animal of a resource that it may not otherwise miss; the choices devised for a test may not be within the animal’s cognitive capacity; and vigilance behaviour may be misinterpreted as a choice. Furthermore, as several authors have proposed, further research is needed to clarify the link between preferences and other indicators of animal welfare (Fraser and Nicol 2011). Nevertheless, the results of many such tests, cautiously interpreted, have proved to be informative (Fraser 2008). Other approaches utilised in assessing affective experiences include measures of behaviour, cognitive bias and physiology (Boissy et al. 2007; Mendl et al. 2009), as well as employing the intuitive perception of human observers using an approach known as Qualitative Behavioural Assessment (Wemelsfelder and Mullan 2014). However, while methods to assess negative affective experiences have been developed based on physiology and behaviour (Boissy et al. 2007; Mendl et al. 2009), validated ways to assess positive affective experiences are still being sought, largely by evaluating a significant body of neuroscience evidence now accumulating on the behaviours that animals find rewarding (Panksepp 2005; Burgdorf and Panksepp 2006; Boissy et al. 2007). Natural living This conceptual framework, albeit not often well enunciated in the literature, is predicated on the view that the welfare of animals is improved when they can express their normal behaviour. For some people this also implies that the animal should be raised in a “natural” environment and allowed to behave in “natural” ways (Fraser 2008). The notion that animals should perform their full repertoire of behaviour was common in early welfare research and is still common today, for example in material advocating so-called “welfare-friendly” production systems (Hemsworth and Coleman 2011). However, the concept of natural is usually too poorly defined to provide a sound basis for animal welfare assessment, and thus when applied uncritically it may lead to poorer welfare instead of an improvement (Mellor 2015c). There is a need to define natural behaviours that are desirable or undesirable in terms of animal welfare and to clarify the rationale for their inclusion or exclusion (Barnett and Hemsworth 2009; Hemsworth and Coleman 2011). Some progress is being made in this area via increasing neuroscience evidence which supports previous behavioural science observations that animals find undertaking particular behaviours rewarding (Panksepp 2005; Mellor 2015a,b). These behaviours include elements of
Hemsworth et al.
exploration, hunting or foraging, affiliative interactions, maternal care of young, play and sexual activity (Mellor 2015a,b). As reward equates to positive affect, these considerations contribute to the affective state conceptual framework. Overall therefore, although the concept of natural living does not provide a rigorous basis for welfare assessment, it usefully draws attention to the potential welfare benefits of providing opportunities to engage in such natural behaviours (Mellor 2015c). Integrating the biological functioning and affective state frameworks The interpretation of the physiological and behavioural indices of both biological functioning and affective states provide the basis for inferences regarding an animal’s welfare status. Each researcher’s concept of animal welfare clearly underscores the methodology they use to judge or assess it, which highlights the twoway interaction between concept and methodology whereby fresh concepts may generate innovative methodologies, and vice versa. Although the biological functioning and affective state frameworks were initially seen as competing, a more unified orientation has now emerged where biological functioning is taken to include affective experiences, affective experiences are recognised as products of biological functioning, and knowledge of the dynamic interactions between the two is considered to be fundamental to managing and improving animal welfare (Boissy et al. 2007; Barnett and Hemsworth 2009; Green and Mellor 2011). Thus, it is understood that affective experiences are generated by sensory inputs that reflect the animal’s internal physical/functional state, that other sensory inputs contribute to the animal’s perception of its external circumstances, and that those perceptions can affect the physical/functional state within the animal (Mellor 2012, 2015a). For example, while food deprivation leads to the affective experience of hunger, affective experiences generated in fear-provoking conditions, such as aversive handling, lead to activation of the sympatho-adrenal medullary system and the hypothalamo-pituitary adrenal axis, and, as with food deprivation, can adversely affect the physical/functional state within the animal if the condition is prolonged (Hemsworth and Coleman 2011). This resolution shows that, despite the development of initially competing animal welfare frameworks, all the phenomena studied in fact take place in an animal functioning as an integrated whole, and that, eventually, the dynamic linkages between them will be revealed and will contribute to significant advances in understanding.
The value of the integrated biological functioning framework in understanding the welfare of group-housed sows Increasing community concern about confinement housing of livestock has led to legislative, consumer, and retailer pressure to increase the use of group housing of gestating sows (Fraser 2008; Hemsworth and Coleman 2011). Although group housing facilitates social living, group housing of gestating sows raises different welfare considerations to stall housing, such as high levels of aggression, injuries and stress for several days after mixing at least, as well as subordinate sows being underfed due to competition at feeding (Barnett et al. 2003). Consequently, as the pork industry has increasingly adopted group housing of gestating sows, research has investigated factors that may contribute to compromised welfare in such situations.
Hemsworth et al.
New Zealand Veterinary Journal, 2015
Downloaded by [Colorado College] at 15:57 30 March 2015
The majority of studies on this topic have employed the biological functioning framework to infer compromised sow welfare on the basis that suboptimal biological functioning accompanies negative affective states, such as sow hunger, pain, fear, helplessness, frustration and anger (Green and Mellor 2011; Mellor 2015a,b). The measures used have included: behavioural variables, such as aggression; physiological variables, such as circulating concentrations of cortisol and neutrophil:lymphocyte ratio; and fitness variables, such as lameness, skin lesions, liveweight change and reproductive performance. Few studies have used preference and motivation tests to investigate what resources or behaviours are important to sows in groups, and which, by implication, might provide “relief” by reducing the intensity of some negative affects or “benefit” by increasing opportunities to experience positive affects (Mellor 2012, 2015a,b). Motivation tests have been used to assess sow hunger (Bergeron et al. 2000). Apart from one study, which examined how motivated sows were to gain access to a pen and was inconclusive (Kirkden and Pajor 2006), there are few reports on the preferences of sows for features of group housing. Nevertheless, significant advances in understanding have been made, some of which are considered briefly below. Group housing and sow welfare
High levels of aggression are commonly observed in newly formed groups of sows after mixing (Velarde 2007; Bench et al. 2013a). This aggression, especially if intense and prolonged, has obvious welfare implications particularly for subordinate sows because of injuries and stress caused (Mendl et al. 1992; Nicholson et al. 1993; Verdon et al. 2013) and their probable links to pain and fear. Aggression is a basic feature of the formation of a dominance hierarchy in groups of sows, but once established, the hierarchy functions to reduce the need for aggression (Lindberg 2001). However, although this may reduce fighting-induced injuries and any associated pain in subordinate sows, these sows might nevertheless remain fearful. Thus, reference below to aggression, injuries and stress should be understood to imply their negative affective consequences, including pain and fear. Floor space Reducing floor space available for gilts and sows within the range of 1.0–3.0 m2/animal increases aggression and stress, as assessed by behaviour and concentrations of cortisol in plasma, and reduces both immune competence (in some studies), as reflected in cell-mediated responses, and reproductive performance. In gilts, for example, aggression at times was higher at a space allowance of 1.0 than at 3.0 m2/gilt (Barnett et al. 1992; Barnett 1997) and stress was higher at 1.0 than at 1.4, 2.0 or 3.0 m2/gilt (Hemsworth et al. 1986; Barnett et al. 1992; Barnett 1997). In sows, aggression was generally higher at 2.0 than at 2.4, 3.6 or 4.8 m2/sow (Weng et al. 1998) and at 2.25 than at 3.0 m2/sow (Remience et al. 2008), and within the range of 1.4–3.0 m2/ sow, significant negative relationships have been shown between space allowance and aggression, stress and farrowing rate (Hemsworth et al. 2013). Effects of space on the prevalence of skin injuries have been observed in some of these studies (Weng et al. 1998; SalakJohnson et al. 2007; Remience et al. 2008) but not in others (Barnett et al. 1992; Barnett 1997; Hemsworth et al. 2013). These observations on space, particularly those on aggression and stress, indicate that a space allowance for gilts and sows of 1.4 m2 per animal is likely too small and that significant
27
improvements in these respects are likely to be achieved with space allowances for gilts and sows in the range of 2.0–2.4 m2/ animal. Furthermore, the effects of space on aggression and stress are most pronounced soon after mixing (Hemsworth et al. 2013). In addition to increased floor space, modifying pen design by providing escape areas allows subordinates to avoid dominant sows. The incorporation of barriers in pens has been shown to reduce aggression in pigs (see Gonyou 2001; Marchant-Forde and Marchant-Forde 2005). Furthermore, as considered in the section on competitive feeding, the incorporation of feeding stalls in pens has been shown to reduce aggression and stress in gilts. Group size There is no evidence that large group sizes of 30 or 80 sows affect stress (Hemsworth et al. 2013), but reports on effects of group size on aggression and injuries are contradictory. The duration of aggression, but not the prevalence of injuries, increased in larger groups in one large study (Taylor et al. 1997), whereas injuries, but not frequency of aggressive interactions and stress, increased in larger groups in another (Hemsworth et al. 2013). Thus, other factors such as floor space and competition for feed or feeding space may have a greater impact on aggression, injuries and stress than group size. Competitive feeding While floor feeding is competitive, accessing feeding stalls or electronic sow feeder stalls also leads to competition between grouphoused sows. For instance, in non-gated stalls, aggression often occurs during feeding periods, and in electronic sow feeder systems, queuing and injurious vulva biting may occur to gain access to feeding stalls (Bench et al. 2013b). Nevertheless, in comparison to floor feeding, providing group-housed pregnant gilts with feeding stalls, particularly full body-length stalls, reduces aggression, injuries (in some studies) and stress in the long term (Barnett et al. 1992; Barnett 1997; Andersen et al. 1999). In contrast, there appear to be no effects of feeding stalls on aggression or injuries immediately post-mixing (Barnett et al. 1993; Barnett 1997). It is of interest that floor space, either total space or the space outside the feeding stalls, affects levels of aggression and stress (Barnett et al. 1992; Barnett 1997), highlighting the importance of floor space irrespective of the feeding system. Apart from observations on skin and vulva injuries, no rigorous comparison of the effects of electronic sow feeders and other feeding systems has been conducted. Hunger The restricted diet commonly fed to pregnant sows is not an issue relevant only to group housing and commonly results in hunger, as assessed by motivation testing (Barnett et al. 2003), and between-sow variation in hunger will be increased in groups that compete at feeding. Operant conditioning studies have shown that sows fed at commercial feeding levels are prepared to work for feed (reward) to a degree that suggests hunger persists through the day (Hutson 1991; Lawrence and Terlouw 1993; Bergeron et al. 2000). Oral stereotypies have been shown to develop in feed-restricted sows (Terlouw et al. 1991; Spoolder et al. 1995; Bergeron et al. 2000), but there is no consistent evidence of increased aggression or skin injuries (Spoolder et al. 1995), or stress, as assessed by concentrations of cortisol in plasma and urine (Meunier-Salaun et al. 2001).
28
New Zealand Veterinary Journal, 2015
Downloaded by [Colorado College] at 15:57 30 March 2015
There is limited evidence that provision of straw can reduce stereotypies, but not aggression. For example, high levels of chain and bar manipulation in restrictively fed, group-housed sows can be prevented by providing straw in individual feeding stalls (Spoolder et al. 1995). This finding supports the view that the development of oral stereotypies in food restricted sows is largely based on an inability to express foraging behaviour rather than hunger per se (Lawrence and Terlouw 1993). However, provision of straw either on the floor or in racks increased aggression in grouphoused sows (Whittaker et al. 1999; Stewart et al. 2008). The incorporation of fibre in sow diets may reduce hunger, as assessed by motivation testing (Meunier-Salaun et al. 2001). Genetics Research on sows at mixing has shown that the heritability for severe aggressive behaviours is intermediate (h2=0.24; Løvendahl et al. 2005). Selection for reduced aggression in pigs is feasible and desirable, but other behaviours, such as general activity and resistance to handling, may have a correlated response to some degree (D’Eath et al. 2009), with possible implications for animal production and welfare. Conclusions
Most of the research on the welfare of sows in groups has employed the biological functioning framework to infer compromised sow welfare on the basis that suboptimal biological functioning accompanies negative affective states, such as sow hunger, pain, fear, helplessness, frustration and anger. The studies reviewed here show that reducing floor space available for gilts and sows within the range of 3.0–1.0 m2/animal increases aggression and stress, and reduces immune competence and reproductive performance. In addition to the quantity of floor space, the quality of the space also has implications for sow welfare, particularly for subordinate animals, because visual or physical barriers and feeding stalls can allow animals to avoid one another. The restricted diet commonly fed to pregnant sows results in hunger, and between-sow variation in hunger is increased in groups with competition at feeding. Thus optimising floor space and pen design features such as feeding stalls and barriers, appear to be important in minimising risks to sow welfare by reducing aggression and stress at mixing and beyond. As with space, the feeding system can affect aggression and stress, but design of these systems, in terms of feeding stall length and ease of access to and from feeding stalls, is likely to affect sow welfare. The effects of foraging substrates and the incorporation of fibre in diets on sow welfare require further research. Genetic selection for reduced aggression has the potential to produce welfare benefits, but an understanding of the broader welfare implications for both the individual and group is necessary.
General challenges for animal welfare science Multidisciplinary assessment of animal welfare
Animal welfare science has made major contributions to understanding animal welfare and its assessment, often by the use of multiple indicators from multiple disciplines (Fraser et al. 2013), but their relative importance has yet to be clarified (Fraser 2008; Nicol et al. 2011). As noted above, scientists have used two main conceptual frameworks for understanding animal welfare, biological functioning and affective state, which,
Hemsworth et al.
in their origin and current methodology, draw on disciplines that include animal behaviour science, immunology, neurophysiology, psychology, stress physiology, animal science and veterinary science. It is likely that the different methodologies aligned with these two frameworks will continue to be used to assess animal welfare and the validity of the derived welfare criteria will be tested in two main ways (Barnett and Hemsworth 2009). The first, by demonstrating whether or not conclusions about effects on the animal are similar when obtained with measures aligned with each of the two frameworks. And the second, by evaluating whether or not an intuitively aversive or rewarding condition in fact reduces or improves animal welfare as assessed by measures derived from both frameworks. Indeed, some evidence for their relatedness already exists in that animals are known to be motivated to choose those resources or engage in behaviours that maintain normal biological functioning in terms of behaviour, physiology and health (Stevens et al. 2009; Nicol et al. 2009, 2011). Finally, it is noted that, at present, any argument that welfare is impaired by restricting a resource or behaviour would be strengthened by evidence that animals are highly motivated to access the resource or perform the behaviour, as well as evidence of disruption to biological function such as the occurrence of abnormal behaviour, increased stress and poor health. Assessing positive affective experiences
Animal welfare, as a state experienced by an animal, can vary on a continuum from very bad to very good. As considered earlier, there is growing evidence showing that brain structure and chemistry, and behaviour, are similar in humans and in a number of mammalian species. The extent of this similarity and other evidence are providing increasing neuroscience support for cautiously interpreting particular animal behaviours in terms of what the animals are apparently intending to achieve, and the negative or positive affects they may experience during the attempt and when it succeeds or fails (Panksepp 2005; Boissy et al. 2007; Mellor 2015a). Most research during at least the last 40 years concentrated on preventing and ameliorating negative states, as reflected in codes of welfare or practice (Mellor et al. 2009; Green and Mellor 2011). However, there is increasing societal interest in providing domesticated animals with the opportunity for positive affective experiences (Tannenbaum 2001) and increasing research focused on positive welfare states in these animals (Fraser and Duncan 1998; Duncan 2005). Considerations such as these provide a context for investigating particular behaviours that may be accompanied by positive affects as, for example, evaluated by Boissy et al. (2007). While vocalisations have long been used as markers of negative emotions in animals, some specific vocalisations are produced by rats, cats and sheep in intuitively positive contexts, such as copulation, winning fights, play, grooming and licking, and nursing offspring, but they are inhibited by negative situations. There is also evidence to suggest that play is a rewarding activity. For example, animals actively seek out play partners and solicit play behaviour; the opportunity to play can be used as a reward in place preference conditioning experiments; and thwarting of play often leads to a rebound when the opportunity arises. Allogrooming, which is seen in farm animals such as cattle, horses and pigs, and is associated with reinforcing social bonds and in reducing tension in groups of animals, appears to be rewarding in the short term. The solicitation of social licking demonstrates the rewarding
Hemsworth et al.
New Zealand Veterinary Journal, 2015
function of the behaviour, at least for the receiver. Soothing effects of allogrooming in terms of a reduction in heart rate have been demonstrated in cattle, horses and primates, but the evidence for this in pigs is less convincing (Boissy et al. 2007). Further examples are available elsewhere (Mellor 2012, 2015a,b).
Downloaded by [Colorado College] at 15:57 30 March 2015
Welfare differences between individuals
There are situations in which decisions on animal welfare need to recognise between-animal variation, as noted previously (Fraser 2003). As indicated above, and in other studies using an extended range of functional and production indices (Mendl et al. 1992; Nicholson et al. 1993; Verdon et al. 2013), social rank may affect how individual sows perform in groups from both welfare and productivity perspectives. Thus, group housing of sows allows all of them more freedom of movement, exploration and socialisation, but a few may suffer from excessive aggression, stress and injuries. While it is obviously important to reduce aggression and stress at a group level, it is also important to appreciate the welfare implications for individuals. Where individuals are at risk, decisions need to be made about what priority to attach to different classes of animals: the majority, the most vulnerable or the most productive (Fraser 2003).
Conclusions The agenda set by the Brambell Committee in 1965 was that animal welfare should be evaluated using scientific evidence about the feelings of animals as indicated by their structure and function and their behaviour, and that this should occur via research into veterinary medicine, stress physiology, animal science and animal behaviour. The Brambell Committee’s agenda was an extraordinarily insightful direction that has been followed by animal welfare scientists for nearly five decades and gave rise to the biological functioning, affective state and natural-living conceptual frameworks. Consideration of our duties towards animals, as well as matters related to human health, and economic, social, environmental and other factors, are all involved in resolving the question of whether or not a particular animal use is acceptable, but science provides the means to understand the impact of each animal use on the animal. That is, science has a prominent role in underpinning decisions on animal use and the attendant conditions and compromises. This is illustrated here by brief reference to some aspects of pregnant sow housing, mainly researched by the application of the biological functioning conceptual framework, extended to emphasise affective outcomes for the animals. There are challenges and potential opportunities for the continued improvement in animal welfare through well-focused research and multidisciplinary welfare assessment. Methods to assess negative emotional experiences or affective states have been developed based on physiology and behaviour, but there is a growing body of neuroscience evidence that supports cautiously interpreting particular behaviours in terms of positive affects that animals may experience. This is anticipated to increasingly direct attention towards positive welfare states, thereby extending the almost exclusive focus of the last 40 years on preventing and ameliorating negative states. Accordingly, the future management of sentient animals will also require the promotion of positive affective experiences and this is likely to be a major focus for animal welfare science activity in the early twenty-first century.
29
References Andersen IL, Bøe KE, Kristiansen AL. The influence of different feeding arrangements and food type on competition at feeding in pregnant sows. Applied Animal Behaviour Science 65, 91–104, 1999 *Barnett JL. Modifying the design of group pens with individual feeding places affects the welfare of pigs. In: Bottcher RW, Hoff SJ (eds). Livestock Environment V, Volume II. Pp 613–18. American Society of Agricultural Engineers, St Joseph, Michigan, USA, 1997 *Barnett JL. Studying stress to assess animal welfare. In: Paterson JE (eds). Manipulating Pig Production IX. Pp 107–20. Australasian Pig Science Association, Werribee, Australia, 2003 Barnett JL, Hemsworth PH. Welfare monitoring schemes: using research to safeguard the welfare of animals on the farm. Journal of Applied Animal Welfare Science 12, 114–31, 2009 Barnett JL, Hemsworth PH, Cronin GM, Newman EA, McCallum TH, Chilton D. Effects of pen size, partial stalls and method of feeding on welfare-related behavioural and physiological responses of group-housed pigs. Applied Animal Behaviour Science 34, 207–20, 1992 Barnett JL, Cronin GM, McCallum TH, Newman EA. Effects of pen size/shape and design on aggression when grouping unfamiliar adult pigs. Applied Animal Behaviour Science 36, 111–22, 1993 Bench CJ, Rioja-Lang FC, Hayne SM, Gonyou HW. Group gestation housing with individual feeding—I: How feeding regime, resource allocation, and genetic factors affect sow welfare. Livestock Science 152, 208–17, 2013a Bench CJ, Rioja-Lang FC, Hayne SM, Gonyou HW. Group gestation housing with individual feeding—II: How space allowance, group size and composition, and flooring affect sow welfare. Livestock Science 152, 218–27, 2013b Bergeron R, Bolduc J, Ramonet Y, Meunier-Salaun MC, Robert S. Feeding motivation and stereotypies in pregnant sows fed increasing levels of fibre and/or food. Applied Animal Behaviour Science 70, 27–40, 2000 Boissy A, Manteuffel G, Jensen MB, Oppermann M, Spruijt B, Keeling LJ, Winckler C, Forkman B, Dimitrov I, Langbein J, et al. Assessment of positive emotions in animals to improve their welfare. Physiology and Behaviour 92, 375–97, 2007 *Brambell FWR, Barbour DS, Barnett MB, Ewer TK, Hobson A, Pitchforth H, Smith WR, Thorpe WH, Winship FJW. Report of the Technical Committee to Enquire into the Welfare of Animals Kept Under Intensive Husbandry Systems. Her Majesty’s Stationery Office, London, United Kingdom, 1965 Broom DM. Indicators of poor welfare. British Veterinary Journal 142, 524–6, 1986 *Broom DM. Coping, stress and welfare. In: Broom DM (eds). Coping with Challenge: Welfare in Animals including Humans. Pp 1–9. Daglem University Press, Berlin, Germany, 2000 Burgdorf J, Panksepp J. The neurobiology of positive emotions. Neuroscience and Biobehavioral Reviews 30, 173–87, 2006 Dantzer, R. Les émotions. P 21. Presses Universitaires de France, Paris, 1988 D’Eath RB, Roehe R, Turner SP, Ison SH, Farish M, Jack MC, Lawrence AB. Genetics of animal temperament: aggressive behaviour at mixing is genetically associated with the response to handling in pigs. Animal 3, 1544–54, 2009 Denton DA, McKinley MJ, Farrell M, Egan GF. The role of primordial emotions in the evolutionary origin of consciousness. Consciousness and Cognition 18, 500–14, 2009 Duncan IJH. Science-based assessment of animal welfare: Farm animals. Scientific and Technical Review, Office International des Epizooties 24, 483–92, 2005 *Duncan IJH, Fraser D. Understanding animal welfare. In: Appleby MC, Hughes BO (eds). Animal Welfare. Pp 19–31. CAB International, Wallingford, Oxfordshire, United Kingdom, 1997 Fisher MW, Mellor DJ. Developing a systematic strategy incorporating ethical, animal welfare and practical principles to guide the genetic improvement of dairy cattle. New Zealand Veterinary Journal 65, 100–6, 2008 Fraser D. Assessing animal welfare at the farm and group level: the interplay of science and values. Animal Welfare 12, 433–43, 2003. *Fraser D. Understanding Animal Welfare: The Science in its Cultural Context. Wiley-Blackwell, Chichester, West Sussex, United Kingdom, 2008 Fraser D, Duncan IJH. “Pleasures”, “pains” and animal welfare; towards a natural history of affect. Animal Welfare 7, 383–96, 1998 *Fraser D, Nicol CJ. Preference and motivation research. In: Appleby MC, Mench JA, Olsson IAS, Hughes BO (eds). Animal Welfare. Pp 183–99. CAB International, Oxon, United Kingdom, 2011 Fraser D, Duncan IJH, Edwards SA, Grandin T, Gregory NG, Guyonnet V, Hemsworth PH, Huertas SM, Huzzey JM, Mellor DJ, et al. General principles for the welfare of animals in production systems: The underlying science and its application. The Veterinary Journal 198, 19–27, 2013
Downloaded by [Colorado College] at 15:57 30 March 2015
30
New Zealand Veterinary Journal, 2015
*Gonyou HW. The social behaviour of pigs. In: Keeling LJ, Gonyou HW (eds). Social Behaviour in Farm Animals. Pp 147–76. CAB International, Oxon, United Kingdom, 2001 Green TC, Mellor DJ. Extending ideas about animal welfare assessment to include ‘quality of life’ and related concepts. New Zealand Veterinary Journal 59, 263– 71, 2011 *Hemsworth PH, Coleman GJ. Human-Livestock Interactions: the Stockperson and the Productivity and Welfare of Farmed Animals. 2nd Edtn. CAB International, Oxon, United Kingdom, 2011 Hemsworth PH, Barnett JL, Hansen C, Winfield CG. Effects of social environment on welfare status and sexual behaviour of female pigs. II. Effects of space allowance. Applied Animal Behaviour Science 16, 259–67, 1986 *Hemsworth PH, Barnett JL, Rickard M, Coleman GJ. Australia’s research and development capacity in animal welfare. Farm Policy Journal 4 (4), 23–31, 2007 Hemsworth PH, Rice M, Nash J, Giri K, Butler KL, Tilbrook AJ, Morrison RS. Effects of group size and floor space allowance on grouped sows: aggression, stress, skin injuries and reproductive performance. Journal of Animal Science 91, 1–12, 2013 Hutson GD. A note on hunger in the pig: sows on restricted rations will sustain an energy deficit to gain additional food. Animal Production 52, 233–5, 1991 *Kaltas GA, Chrousos GP. The neuroendorinology of stress. In: Cacioppo JT, Tassinary LG and Berntson GG (eds). Handbook of Psychophysiology. Pp 303–18. Cambridge University, Cambridge, UK, 2007 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 Lauber M, Nash JA, Gatt A, Hemsworth PH. Prevalence and incidence of abnormal behaviours in individually housed sheep. Animals 2, 27–37, 2012 Lawrence AB, Terlouw EMC. A review of behavioural factors involved in the development and continued performance of stereotypic behaviours in pigs. Journal of Animal Science 71, 2815–25, 1993 *Levy N. What Makes Us Moral?. Crossing the Boundaries of Biology. Oneworld, Oxford, United Kingdom, 2004 *Lindberg AC. Group life. In: Keeling LJ, Gonyou HW (eds). Social Behaviour in Farm Animals. Pp 37–58. CAB International, Wallingford, Oxfordshire, United Kingdom, 2001 Løvendahl P, Damgaard LH, Nielsen BL, Thodberg K, Su G, Rydhmer L. Aggressive behaviour of sows at mixing and maternal behaviour are heritable and genetically correlated traits. Livestock Production Science 93, 73–85, 2005 *Marchant-Forde JN, Marchant-Forde RM. Minimizing inter-pig aggression during mixing. Pig News and Information 26, 63N–71N, 2005 Mellor DJ. Animal emotions, behaviour and the promotion of positive welfare states. New Zealand Veterinary Journal 60, 1–8, 2012 *Mellor DJ. Production Animals: Ethical and welfare issues raised by productionfocused management of newborn livestock. In: Wathes CM, Corr SA, May SA, McCulloch SP, Whiting MC (eds). Veterinary and Animal Ethics: Proceedings of the first International Conference on Veterinary and Animal Ethics. Pp 174–87. Wiley-Blackwell, Oxford, United Kingdom, 2013 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. Positive animal welfare states and reference standards for welfare assessment. New Zealand Veterinary Journal 63, 17–23, 2015c 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, Patterson-Kane E, Stafford KJ. The Sciences of Animal Welfare. Wiley-Blackwell Publishing, Oxford, United Kingdom, 2009 Mendl M, Zanella AJ, Broom DM. Physiological and reproductive correlates of behavioural strategies in female domestic pigs. Animal Behaviour 44, 1107– 21, 1992 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 Meunier-Salaün MC, Edwards SA, Robert S. Effect of dietary fibre on the behaviour and health of the restricted sow. Animal Feed Science and Technology 90, 53–69, 2001 *Moberg GP. Biological response to stress: Implications for animal welfare. In Moberg GP, Mench GA (eds). The Biology of Animal Stress; Basic Principles
Hemsworth et al.
and Applications for Animal Welfare. Pp 1–21. CABI Publishing, Wallingford, United Kingdom, 2000 Nicol CJ, Caplen G, Edgar J, Browne WJ. Associations between welfare indicators and environmental choice in laying hens. Animal Behaviour 78, 413–24, 2009 Nicol CJ, Caplen G, Statham P, Browne WJ. Decisions about foraging and risk trade-offs in chickens are associated with individual somatic response profiles. Animal Behaviour 82, 255–62, 2011 *Nicholson RI, McGlone JJ, Reid LN. Quantification of stress in sows: comparison of individual housing versus social penning. Journal of Animal Science 71 (Suppl. 1), 112, 1993 *Olsson IAS, Wurbell H, Mench JA. Behaviour. In: Appleby MC, Mench JA, Olsson IAS, Hughes BO (eds.) Animal Welfare. Pp 138–154. CABI International, Wallingford, Oxfordshire, United Kingdom, 2011 Panksepp J. Affective consciousness: Core emotional feelings in animals and humans. Consciousness and Cognition 14, 30–80, 2005 Remience V, Wavreille J, Canart B, Meunier-Salaün MC, Prunier A, BartiauxThill N, Nicks B, Vandenheede M. Effects of space allowance on the welfare of dry sows kept in dynamic groups and fed with electronic sow feeder. Applied Animal Behaviour Science 112, 284–96, 2008 Salak-Johnson JL, Niekamp SR, Rodriguez-Zas SL, Ellis M, Curtis SE. Space allowance for dry, pregnant sows in pens: body condition, skin lesions and performance. Journal of Animal Science 85, 1758–69, 2007 Spoolder HAM, Burbidge JA, Edwards SA, Simmins PH, Lawrence AL. Provision of straw as a foraging substrate reduces the development of excessive chain and bar manipulation in food restricted sows. Applied Animal Behaviour Science 43, 249–62, 1995 *Stevens B, Barnett JL, Tilbrook AJ, Hemsworth PH. Effects of deprivation of a preferred resource (feed or social contact) on the biological functioning of pigs. In: van Barneveld RJ (eds). Manipulating Pig Production XII. P 28. Australasian Pig Science Association, Werribee, Victoria, Australia, 2009 Stewart CL, O’Connell NE, Boyle L. Influence of access to straw provided in racks on the welfare of sows in large dynamic groups. Applied Animal Behaviour Science 112, 235–47, 2008 *Tannenbaum J. The paradigm shift toward animal happiness: what it is, why it is happening, and what it portends for medical research. In: Paul EF and Paul J (eds). Why Animal Experimentation Matters: The use of Animals in Medical Research. Pp 93–130. Transaction Publishers, Somerset, New Jersey, USA, 2001 *Taylor IA, Barnett JL, Cronin GM. Optimum group size for pigs. In: Bottcher RW, Hoff SJ (eds). Livestock Environment V, Volume II. Pp 965–71. American Society of Agricultural Engineers, St Joseph, Michigan, USA, 1997 Terlouw EM, Lawrence AB, Illius AW. Influences of feeding level and physical restriction on development of stereotypies in sows. Animal Behaviour 42, 981–91, 1991 *Turner AI, Keating C, Tilbrook AJ. Sex differences and the role of sex steroids in sympatho-adrenal medullary system the hypothalamo-pituitary adrenal axis responses to stress. In: Kahn SM (eds). Sex Steroids. Pp 115–36. In Tech Publishing, Rijeka, Croatia, 2012 *Verdon M, Morrison R, Rice M, Hemsworth PH. Group-housed sows who engage in aggression after mixing have reduced injuries and gain more weight. Proceedings of the 47th International Society of Applied Ethology. P 68. Wageningen Academic Publishers, Wageningen, The Netherlands, Florianopolis, Brazil, 2013 *Verlarde A. Agonistic behaviour. In: Verlarde A, Geers R (eds). On Farm Monitoring of Pig Welfare. Pp 53–6. Wageningen Academic Press, Wageningen, The Netherlands, 2007 Wemelsfelder F, Mullan S. Applying ethological and health indictors to practical animal welfare assessment. Scientific and Technical Review, Office International des Epizooties 33, 111–20, 2014 Weng RC, Edwards SA, English PR. Behaviour, social interactions and lesion score of group-housed sows in relation to floor space allowance. Applied Animal Behaviour Science 59, 307–16, 1998 Whittaker X, Edwards SA, Spoolder HAM. Lawrence AB, Corning S. Effects of straw bedding and high fibre diets on the behaviour of floor fed group-housed sows. Applied Animal Behaviour Science 63, 25–39, 1999
Submitted 12 November 2013 Accepted for publication 10 September 2014 First published online 29 September 2014
*Non-peer-reviewed
New Zealand Veterinary Journal Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/tnzv20
Scientific assessment of animal welfare a
b
c
PH Hemsworth , DJ Mellor , GM Cronin & AJ Tilbrook
ad
a
Animal Welfare Science Centre, University of Melbourne, Parkville, Victoria 3010, Australia b
Animal Welfare Science and Bioethics Centre, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North 4442, New Zealand c
Faculty of Veterinary Science, University of Sydney, Camden, NSW 2570, Australia
d
South Australian Research and Development Institute, University of Adelaide, Roseworthy, South Australia 5371, Australia Accepted author version posted online: 29 Sep 2014.Published online: 11 Dec 2014.
Click for updates To cite this article: PH Hemsworth, DJ Mellor, GM Cronin & AJ Tilbrook (2015) Scientific assessment of animal welfare, New Zealand Veterinary Journal, 63:1, 24-30, DOI: 10.1080/00480169.2014.966167 To link to this article: http://dx.doi.org/10.1080/00480169.2014.966167
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
24
New Zealand Veterinary Journal 63(1), 24–30, 2015
Review Article
Scientific assessment of animal welfare PH Hemsworth*§, DJ Mellor†, GM Cronin‡ and AJ Tilbrook*#
Downloaded by [Colorado College] at 15:57 30 March 2015
Abstract Animal welfare is a state within the animal and a scientific perspective provides methodologies for evidence-based assessment of an animal’s welfare. A simplistic definition of animal welfare might be how the animal feels now. Affective experiences including emotions, are subjective states so cannot be measured directly in animals, but there are informative indirect physiological and behavioural indices that can be cautiously used to interpret such experiences. This review enunciates several key science-based frameworks for understanding animal welfare. The biological functioning and affective state frameworks were initially seen as competing, but a recent more unified approach is that biological functioning is taken to include affective experiences and affective experiences are recognised as products of biological functioning, and knowledge of the dynamic interactions between the two is considered to be fundamental to managing and improving animal welfare. The value of these two frameworks in understanding the welfare of group-housed sows is reviewed. The majority of studies of the welfare of group-housed sows have employed the biological functioning framework to infer compromised sow welfare, on the basis that suboptimal biological functioning accompanies negative affective states such as sow hunger, pain, fear, helplessness, frustration and anger. Group housing facilitates social living, but group housing of gestating sows raises different welfare considerations to stall housing, such as high levels of aggression, injuries and stress, at least for several days after mixing, as well as subordinate sows being underfed due to competition at feeding. This paper highlights the challenges and potential opportunities for the continued improvement in sow management through well-focused research and multidisciplinary assessment of animal welfare. In future the management of sentient animals will require the promotion of positive affective experiences in animals and this is likely to be
* Animal Welfare Science Centre, University of Melbourne, Parkville, Victoria 3010, Australia † Animal Welfare Science and Bioethics Centre, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North 4442, New Zealand ‡ Faculty of Veterinary Science, University of Sydney, Camden, NSW 2570, Australia # South Australian Research and Development Institute, University of Adelaide, Roseworthy, South Australia 5371, Australia § Author for correspondence. Email: [email protected] http://dx.doi.org/10.1080/00480169.2014.966167 © 2014 New Zealand Veterinary Association
a major focus for animal welfare science activity in the early twenty-first century. KEY WORDS: Animal welfare, assessment, behaviour, stress, emotions, animal ethics, sow welfare
Introduction The publication of Ruth Harrison’s book “Animal Machines” in 1964 led to debate in many industrialised countries about the confinement of farm animals. In response the British Government established the Brambell Committee (Brambell et al. 1965) which defined welfare as a wide term that embraces both the physical and mental well-being of the animal. Furthermore, the Committee stated that “any attempt to evaluate welfare therefore must take into account the scientific evidence available concerning the feelings of animals that can be derived from their structure and functions and also from their behaviour.” Amongst its numerous recommendations, the Committee also called for research into veterinary medicine, stress physiology, animal science and, in particular, animal behaviour. The Brambell Committee thus provided an agenda for animal welfare science (Fraser 2008), which has over the subsequent 50 years, focused welfare research and in turn led to the recognition of a new discipline, animal welfare science. Science has an important role in underpinning societal decisions on animal use and the acceptability or otherwise of attendant conditions and compromises. Exclusion of science can result in emotive or self-interested arguments from sectional groups dominating community debate. This is not to say that such arguments should be ruled out; quite the reverse, as they reflect, in part, current community values. However, they should contribute to, not pre-empt, the debate (Hemsworth et al. 2007). Ultimately such questions are ethical ones in which scientific facts need to be considered together with other beliefs and principles if we are to formulate supportable answers (Levy 2004; Fisher and Mellor 2008; Mellor 2013). Of course, societal interests in animal welfare also include consideration of wider issues such as human health, economic and social implications, as well as environmental impacts (Fisher and Mellor 2008; Mellor and Bayvel 2008). Decisions on acceptable animal use can therefore involve difficult and complex choices and consequently they may remain controversial. This review aims to clarify various aspects of the current scientific understanding of animal welfare. It enunciates three science-based frameworks that have influenced the orientation of animal welfare assessments, and then illustrates briefly how two of these frameworks have been applied to improving the welfare of grouphoused sows. It ends by considering some of the significant challenges facing animal welfare science.
Hemsworth et al.
New Zealand Veterinary Journal, 2015
Science-based views of animal welfare A scientific perspective of animal welfare
Downloaded by [Colorado College] at 15:57 30 March 2015
Provided here is an integrated understanding of what animal welfare represents that is now widely accepted in the published literature (e.g. see reviews by Boissy et al. 2007; Mellor et al. 2009; Mellor 2012). Although management procedures applied to the animal or features of the animal’s environment may affect its welfare, animal welfare is a state within the animal. For an animal’s welfare to be affected, the animal must be sentient, i.e. it must have a brain with sufficient functional sophistication to transduce impulses in sensory and other nerves into experienced sensations. It is generally agreed that animal welfare relates to experienced sensations, so the animal must also be conscious (Mellor et al. 2009). These experiences arise as the integrated outcomes of sensory and other neural inputs from within the animal’s body and from its environment. These inputs are processed and interpreted by the animal’s brain according to its species-specific and individual nature, and its past experience. The integrated outcomes of this processing represent the animal’s current experience, i.e. its welfare status, and this changes as the balance and nature of the inputs change. These experiences are all subjective, varying in their emotional or affective contents and, based on human experience, are likely to include negative affective or emotional experiences such as breathlessness, thirst, hunger, nausea, pain and fear, and positive affective experiences such as satiety, contentment, companionship, curiosity and playfulness. Many of these experiences motivate animals to engage in behaviours that are critical for survival and thus also have longer-term welfare implications (Fraser and Duncan 1998). As subjective states they cannot be measured directly, but there are informative indirect indices of such experiences. These indices, which are based on established knowledge of physiological and behavioural responses to specific welfare challenges, have been critically evaluated as useful and relevant in many contexts (see reviews by Boissy et al. 2007; Mellor et al. 2009; Mellor 2012). Thus the welfare status of an animal at any one time may vary on a continuum between very bad to very good. Conceptual frameworks for assessment of animal welfare
There are basically three conceptual frameworks that are used to assess animal welfare, namely, biological functioning, affective state and natural living (Fraser 2003). It is of interest that these approaches use to varying degrees the disciplines that the Brambell Committee called for in assessing animal welfare (Brambell et al. 1965), i.e. veterinary medicine, stress physiology, animal science and particularly animal behaviour science. Biological functioning The rationale underpinning this conceptual framework is that difficult or inadequate adaptation will generate welfare problems for animals (Hemsworth and Coleman 2011). This concept aligns with the definition of Broom (1986, 2000) that the welfare of an animal is its state as regards its attempts to cope with its environment. This state refers to the extent of biological activity underlying attempts to cope, including the involvement of body repair systems, immunological defences and physiological stress responses, as well as a variety of behavioural responses. While research has led to a better understanding of the causation of these behavioural responses, such as stereotypies, redirected behaviours and displacement activities, the function and, thus,
25
adaptive significance of these behavioural responses are often poorly understood (Olsson et al. 2011; Lauber et al. 2012). The physiological stress responses to challenges are also varied and complex. Nonetheless, these responses nearly always include activation of the sympatho-adrenal medullary system and the hypothalamo-pituitary adrenal axis, with the consequent increase in synthesis of catecholamines and glucocorticoids, respectively (Turner et al. 2012). Further, this state in Broom’s definition refers to the extent to which these coping attempts are or are not succeeding, and this includes any biological costs to the animal, such as deterioration in growth efficiency, reproduction and health (injury or disease). Thus this conceptual framework emphasises that animals use a range of behavioural and physiological responses to assist them to cope with challenges, and while biological regulation in response to challenges occurs continuously, successful adaptation is not always possible (Barnett and Hemsworth 2009; Hemsworth and Coleman 2011). Marked challenges may overwhelm an individual’s capacity to adapt and lead to its death. However, less severe challenges can still have significant biological costs, leading to growth, reproductive, health and other impairments, which may reflect and/or result in welfare problems for the animal. Conceptualised in these terms, it is the biological cost of stress that is the key to understanding the associated welfare implications (Moberg 2000; Barnett 2003). How well an animal is coping with the challenges it faces will be reflected in the normality of its biological functioning and fitness, with severe risks to welfare associated with the most extreme coping attempts (Hemsworth and Coleman 2011). A common criticism of this conceptual framework in assessing animal welfare is that it does not adequately include emotions. This would only be valid if emotions are independent of other biological processes, but there is no doubt that emotions are associated with activations of both the sympatho-adrenal medullary and hypothalamo-pituitary adrenal axes (Dantzer 1988; Kaltas and Chrousos 2007). Affective state The second conceptual framework emphasises that the welfare of an animal derives from its capacity for affective experiences (Duncan and Fraser 1997). Thus, the welfare state is likely to be negative when the predominant affects experienced are unpleasant, and vice versa. However, affective experiences were considered to be inaccessible to scientific inquiry for many decades, a view that is being challenged by a growing body of evidence showing that brain structure and chemistry, and behaviour, are similar in humans and in a large number of animal species (Panksepp 2005; Boissy et al. 2007; Mellor 2015a). For example: other mammals are attracted to the same environmental rewards and drugs of abuse as humans; human and animal emotional experiences appear to depend on very similar sub-cortical brain systems situated in deep brain regions where evolutionarily homologous instinctual neural systems exist; and artificial activations of the deep brain systems elicit emotional actions that are liked and disliked by animals, as measured by a host of approach and avoidance responses (Panksepp 2005). This and other evidence contributes neuroscience support for cautiously interpreting particular animal behaviours in terms of an animal’s negative or positive affective experiences, such as, during the pursuit of its behavioural goals and failure or success in achieving those goals (Panksepp 2005). Importantly, it is also well recognised that such affective experiences are generated both by sensory inputs
26
New Zealand Veterinary Journal, 2015
Downloaded by [Colorado College] at 15:57 30 March 2015
that reflect the animal’s internal physical/functional state and by other sensory inputs that reflect the animal’s perception of its external circumstances (Denton et al. 2009; Mellor 2012, 2015a). Preference research, in which the strength of the preference for a chosen environmental option or the motivation to perform a type of behaviour are measured, has been used by some scientists to make inferences about animal welfare on the assumption that animals make choices that are in their best interest (Fraser and Nicol 2011). While it is likely that animals will avoid aversive stimuli and choose positive stimuli, caution is recommended in view of conceptual and methodological concerns that have been raised about the preference and motivation tests themselves (Nicol et al. 2009; Fraser and Nicol 2011). For example: familiarity with a resource may affect choice; a choice at one point in time may not reflect interactions of different motivational states over time; a positive resource may remind the animal of a resource that it may not otherwise miss; the choices devised for a test may not be within the animal’s cognitive capacity; and vigilance behaviour may be misinterpreted as a choice. Furthermore, as several authors have proposed, further research is needed to clarify the link between preferences and other indicators of animal welfare (Fraser and Nicol 2011). Nevertheless, the results of many such tests, cautiously interpreted, have proved to be informative (Fraser 2008). Other approaches utilised in assessing affective experiences include measures of behaviour, cognitive bias and physiology (Boissy et al. 2007; Mendl et al. 2009), as well as employing the intuitive perception of human observers using an approach known as Qualitative Behavioural Assessment (Wemelsfelder and Mullan 2014). However, while methods to assess negative affective experiences have been developed based on physiology and behaviour (Boissy et al. 2007; Mendl et al. 2009), validated ways to assess positive affective experiences are still being sought, largely by evaluating a significant body of neuroscience evidence now accumulating on the behaviours that animals find rewarding (Panksepp 2005; Burgdorf and Panksepp 2006; Boissy et al. 2007). Natural living This conceptual framework, albeit not often well enunciated in the literature, is predicated on the view that the welfare of animals is improved when they can express their normal behaviour. For some people this also implies that the animal should be raised in a “natural” environment and allowed to behave in “natural” ways (Fraser 2008). The notion that animals should perform their full repertoire of behaviour was common in early welfare research and is still common today, for example in material advocating so-called “welfare-friendly” production systems (Hemsworth and Coleman 2011). However, the concept of natural is usually too poorly defined to provide a sound basis for animal welfare assessment, and thus when applied uncritically it may lead to poorer welfare instead of an improvement (Mellor 2015c). There is a need to define natural behaviours that are desirable or undesirable in terms of animal welfare and to clarify the rationale for their inclusion or exclusion (Barnett and Hemsworth 2009; Hemsworth and Coleman 2011). Some progress is being made in this area via increasing neuroscience evidence which supports previous behavioural science observations that animals find undertaking particular behaviours rewarding (Panksepp 2005; Mellor 2015a,b). These behaviours include elements of
Hemsworth et al.
exploration, hunting or foraging, affiliative interactions, maternal care of young, play and sexual activity (Mellor 2015a,b). As reward equates to positive affect, these considerations contribute to the affective state conceptual framework. Overall therefore, although the concept of natural living does not provide a rigorous basis for welfare assessment, it usefully draws attention to the potential welfare benefits of providing opportunities to engage in such natural behaviours (Mellor 2015c). Integrating the biological functioning and affective state frameworks The interpretation of the physiological and behavioural indices of both biological functioning and affective states provide the basis for inferences regarding an animal’s welfare status. Each researcher’s concept of animal welfare clearly underscores the methodology they use to judge or assess it, which highlights the twoway interaction between concept and methodology whereby fresh concepts may generate innovative methodologies, and vice versa. Although the biological functioning and affective state frameworks were initially seen as competing, a more unified orientation has now emerged where biological functioning is taken to include affective experiences, affective experiences are recognised as products of biological functioning, and knowledge of the dynamic interactions between the two is considered to be fundamental to managing and improving animal welfare (Boissy et al. 2007; Barnett and Hemsworth 2009; Green and Mellor 2011). Thus, it is understood that affective experiences are generated by sensory inputs that reflect the animal’s internal physical/functional state, that other sensory inputs contribute to the animal’s perception of its external circumstances, and that those perceptions can affect the physical/functional state within the animal (Mellor 2012, 2015a). For example, while food deprivation leads to the affective experience of hunger, affective experiences generated in fear-provoking conditions, such as aversive handling, lead to activation of the sympatho-adrenal medullary system and the hypothalamo-pituitary adrenal axis, and, as with food deprivation, can adversely affect the physical/functional state within the animal if the condition is prolonged (Hemsworth and Coleman 2011). This resolution shows that, despite the development of initially competing animal welfare frameworks, all the phenomena studied in fact take place in an animal functioning as an integrated whole, and that, eventually, the dynamic linkages between them will be revealed and will contribute to significant advances in understanding.
The value of the integrated biological functioning framework in understanding the welfare of group-housed sows Increasing community concern about confinement housing of livestock has led to legislative, consumer, and retailer pressure to increase the use of group housing of gestating sows (Fraser 2008; Hemsworth and Coleman 2011). Although group housing facilitates social living, group housing of gestating sows raises different welfare considerations to stall housing, such as high levels of aggression, injuries and stress for several days after mixing at least, as well as subordinate sows being underfed due to competition at feeding (Barnett et al. 2003). Consequently, as the pork industry has increasingly adopted group housing of gestating sows, research has investigated factors that may contribute to compromised welfare in such situations.
Hemsworth et al.
New Zealand Veterinary Journal, 2015
Downloaded by [Colorado College] at 15:57 30 March 2015
The majority of studies on this topic have employed the biological functioning framework to infer compromised sow welfare on the basis that suboptimal biological functioning accompanies negative affective states, such as sow hunger, pain, fear, helplessness, frustration and anger (Green and Mellor 2011; Mellor 2015a,b). The measures used have included: behavioural variables, such as aggression; physiological variables, such as circulating concentrations of cortisol and neutrophil:lymphocyte ratio; and fitness variables, such as lameness, skin lesions, liveweight change and reproductive performance. Few studies have used preference and motivation tests to investigate what resources or behaviours are important to sows in groups, and which, by implication, might provide “relief” by reducing the intensity of some negative affects or “benefit” by increasing opportunities to experience positive affects (Mellor 2012, 2015a,b). Motivation tests have been used to assess sow hunger (Bergeron et al. 2000). Apart from one study, which examined how motivated sows were to gain access to a pen and was inconclusive (Kirkden and Pajor 2006), there are few reports on the preferences of sows for features of group housing. Nevertheless, significant advances in understanding have been made, some of which are considered briefly below. Group housing and sow welfare
High levels of aggression are commonly observed in newly formed groups of sows after mixing (Velarde 2007; Bench et al. 2013a). This aggression, especially if intense and prolonged, has obvious welfare implications particularly for subordinate sows because of injuries and stress caused (Mendl et al. 1992; Nicholson et al. 1993; Verdon et al. 2013) and their probable links to pain and fear. Aggression is a basic feature of the formation of a dominance hierarchy in groups of sows, but once established, the hierarchy functions to reduce the need for aggression (Lindberg 2001). However, although this may reduce fighting-induced injuries and any associated pain in subordinate sows, these sows might nevertheless remain fearful. Thus, reference below to aggression, injuries and stress should be understood to imply their negative affective consequences, including pain and fear. Floor space Reducing floor space available for gilts and sows within the range of 1.0–3.0 m2/animal increases aggression and stress, as assessed by behaviour and concentrations of cortisol in plasma, and reduces both immune competence (in some studies), as reflected in cell-mediated responses, and reproductive performance. In gilts, for example, aggression at times was higher at a space allowance of 1.0 than at 3.0 m2/gilt (Barnett et al. 1992; Barnett 1997) and stress was higher at 1.0 than at 1.4, 2.0 or 3.0 m2/gilt (Hemsworth et al. 1986; Barnett et al. 1992; Barnett 1997). In sows, aggression was generally higher at 2.0 than at 2.4, 3.6 or 4.8 m2/sow (Weng et al. 1998) and at 2.25 than at 3.0 m2/sow (Remience et al. 2008), and within the range of 1.4–3.0 m2/ sow, significant negative relationships have been shown between space allowance and aggression, stress and farrowing rate (Hemsworth et al. 2013). Effects of space on the prevalence of skin injuries have been observed in some of these studies (Weng et al. 1998; SalakJohnson et al. 2007; Remience et al. 2008) but not in others (Barnett et al. 1992; Barnett 1997; Hemsworth et al. 2013). These observations on space, particularly those on aggression and stress, indicate that a space allowance for gilts and sows of 1.4 m2 per animal is likely too small and that significant
27
improvements in these respects are likely to be achieved with space allowances for gilts and sows in the range of 2.0–2.4 m2/ animal. Furthermore, the effects of space on aggression and stress are most pronounced soon after mixing (Hemsworth et al. 2013). In addition to increased floor space, modifying pen design by providing escape areas allows subordinates to avoid dominant sows. The incorporation of barriers in pens has been shown to reduce aggression in pigs (see Gonyou 2001; Marchant-Forde and Marchant-Forde 2005). Furthermore, as considered in the section on competitive feeding, the incorporation of feeding stalls in pens has been shown to reduce aggression and stress in gilts. Group size There is no evidence that large group sizes of 30 or 80 sows affect stress (Hemsworth et al. 2013), but reports on effects of group size on aggression and injuries are contradictory. The duration of aggression, but not the prevalence of injuries, increased in larger groups in one large study (Taylor et al. 1997), whereas injuries, but not frequency of aggressive interactions and stress, increased in larger groups in another (Hemsworth et al. 2013). Thus, other factors such as floor space and competition for feed or feeding space may have a greater impact on aggression, injuries and stress than group size. Competitive feeding While floor feeding is competitive, accessing feeding stalls or electronic sow feeder stalls also leads to competition between grouphoused sows. For instance, in non-gated stalls, aggression often occurs during feeding periods, and in electronic sow feeder systems, queuing and injurious vulva biting may occur to gain access to feeding stalls (Bench et al. 2013b). Nevertheless, in comparison to floor feeding, providing group-housed pregnant gilts with feeding stalls, particularly full body-length stalls, reduces aggression, injuries (in some studies) and stress in the long term (Barnett et al. 1992; Barnett 1997; Andersen et al. 1999). In contrast, there appear to be no effects of feeding stalls on aggression or injuries immediately post-mixing (Barnett et al. 1993; Barnett 1997). It is of interest that floor space, either total space or the space outside the feeding stalls, affects levels of aggression and stress (Barnett et al. 1992; Barnett 1997), highlighting the importance of floor space irrespective of the feeding system. Apart from observations on skin and vulva injuries, no rigorous comparison of the effects of electronic sow feeders and other feeding systems has been conducted. Hunger The restricted diet commonly fed to pregnant sows is not an issue relevant only to group housing and commonly results in hunger, as assessed by motivation testing (Barnett et al. 2003), and between-sow variation in hunger will be increased in groups that compete at feeding. Operant conditioning studies have shown that sows fed at commercial feeding levels are prepared to work for feed (reward) to a degree that suggests hunger persists through the day (Hutson 1991; Lawrence and Terlouw 1993; Bergeron et al. 2000). Oral stereotypies have been shown to develop in feed-restricted sows (Terlouw et al. 1991; Spoolder et al. 1995; Bergeron et al. 2000), but there is no consistent evidence of increased aggression or skin injuries (Spoolder et al. 1995), or stress, as assessed by concentrations of cortisol in plasma and urine (Meunier-Salaun et al. 2001).
28
New Zealand Veterinary Journal, 2015
Downloaded by [Colorado College] at 15:57 30 March 2015
There is limited evidence that provision of straw can reduce stereotypies, but not aggression. For example, high levels of chain and bar manipulation in restrictively fed, group-housed sows can be prevented by providing straw in individual feeding stalls (Spoolder et al. 1995). This finding supports the view that the development of oral stereotypies in food restricted sows is largely based on an inability to express foraging behaviour rather than hunger per se (Lawrence and Terlouw 1993). However, provision of straw either on the floor or in racks increased aggression in grouphoused sows (Whittaker et al. 1999; Stewart et al. 2008). The incorporation of fibre in sow diets may reduce hunger, as assessed by motivation testing (Meunier-Salaun et al. 2001). Genetics Research on sows at mixing has shown that the heritability for severe aggressive behaviours is intermediate (h2=0.24; Løvendahl et al. 2005). Selection for reduced aggression in pigs is feasible and desirable, but other behaviours, such as general activity and resistance to handling, may have a correlated response to some degree (D’Eath et al. 2009), with possible implications for animal production and welfare. Conclusions
Most of the research on the welfare of sows in groups has employed the biological functioning framework to infer compromised sow welfare on the basis that suboptimal biological functioning accompanies negative affective states, such as sow hunger, pain, fear, helplessness, frustration and anger. The studies reviewed here show that reducing floor space available for gilts and sows within the range of 3.0–1.0 m2/animal increases aggression and stress, and reduces immune competence and reproductive performance. In addition to the quantity of floor space, the quality of the space also has implications for sow welfare, particularly for subordinate animals, because visual or physical barriers and feeding stalls can allow animals to avoid one another. The restricted diet commonly fed to pregnant sows results in hunger, and between-sow variation in hunger is increased in groups with competition at feeding. Thus optimising floor space and pen design features such as feeding stalls and barriers, appear to be important in minimising risks to sow welfare by reducing aggression and stress at mixing and beyond. As with space, the feeding system can affect aggression and stress, but design of these systems, in terms of feeding stall length and ease of access to and from feeding stalls, is likely to affect sow welfare. The effects of foraging substrates and the incorporation of fibre in diets on sow welfare require further research. Genetic selection for reduced aggression has the potential to produce welfare benefits, but an understanding of the broader welfare implications for both the individual and group is necessary.
General challenges for animal welfare science Multidisciplinary assessment of animal welfare
Animal welfare science has made major contributions to understanding animal welfare and its assessment, often by the use of multiple indicators from multiple disciplines (Fraser et al. 2013), but their relative importance has yet to be clarified (Fraser 2008; Nicol et al. 2011). As noted above, scientists have used two main conceptual frameworks for understanding animal welfare, biological functioning and affective state, which,
Hemsworth et al.
in their origin and current methodology, draw on disciplines that include animal behaviour science, immunology, neurophysiology, psychology, stress physiology, animal science and veterinary science. It is likely that the different methodologies aligned with these two frameworks will continue to be used to assess animal welfare and the validity of the derived welfare criteria will be tested in two main ways (Barnett and Hemsworth 2009). The first, by demonstrating whether or not conclusions about effects on the animal are similar when obtained with measures aligned with each of the two frameworks. And the second, by evaluating whether or not an intuitively aversive or rewarding condition in fact reduces or improves animal welfare as assessed by measures derived from both frameworks. Indeed, some evidence for their relatedness already exists in that animals are known to be motivated to choose those resources or engage in behaviours that maintain normal biological functioning in terms of behaviour, physiology and health (Stevens et al. 2009; Nicol et al. 2009, 2011). Finally, it is noted that, at present, any argument that welfare is impaired by restricting a resource or behaviour would be strengthened by evidence that animals are highly motivated to access the resource or perform the behaviour, as well as evidence of disruption to biological function such as the occurrence of abnormal behaviour, increased stress and poor health. Assessing positive affective experiences
Animal welfare, as a state experienced by an animal, can vary on a continuum from very bad to very good. As considered earlier, there is growing evidence showing that brain structure and chemistry, and behaviour, are similar in humans and in a number of mammalian species. The extent of this similarity and other evidence are providing increasing neuroscience support for cautiously interpreting particular animal behaviours in terms of what the animals are apparently intending to achieve, and the negative or positive affects they may experience during the attempt and when it succeeds or fails (Panksepp 2005; Boissy et al. 2007; Mellor 2015a). Most research during at least the last 40 years concentrated on preventing and ameliorating negative states, as reflected in codes of welfare or practice (Mellor et al. 2009; Green and Mellor 2011). However, there is increasing societal interest in providing domesticated animals with the opportunity for positive affective experiences (Tannenbaum 2001) and increasing research focused on positive welfare states in these animals (Fraser and Duncan 1998; Duncan 2005). Considerations such as these provide a context for investigating particular behaviours that may be accompanied by positive affects as, for example, evaluated by Boissy et al. (2007). While vocalisations have long been used as markers of negative emotions in animals, some specific vocalisations are produced by rats, cats and sheep in intuitively positive contexts, such as copulation, winning fights, play, grooming and licking, and nursing offspring, but they are inhibited by negative situations. There is also evidence to suggest that play is a rewarding activity. For example, animals actively seek out play partners and solicit play behaviour; the opportunity to play can be used as a reward in place preference conditioning experiments; and thwarting of play often leads to a rebound when the opportunity arises. Allogrooming, which is seen in farm animals such as cattle, horses and pigs, and is associated with reinforcing social bonds and in reducing tension in groups of animals, appears to be rewarding in the short term. The solicitation of social licking demonstrates the rewarding
Hemsworth et al.
New Zealand Veterinary Journal, 2015
function of the behaviour, at least for the receiver. Soothing effects of allogrooming in terms of a reduction in heart rate have been demonstrated in cattle, horses and primates, but the evidence for this in pigs is less convincing (Boissy et al. 2007). Further examples are available elsewhere (Mellor 2012, 2015a,b).
Downloaded by [Colorado College] at 15:57 30 March 2015
Welfare differences between individuals
There are situations in which decisions on animal welfare need to recognise between-animal variation, as noted previously (Fraser 2003). As indicated above, and in other studies using an extended range of functional and production indices (Mendl et al. 1992; Nicholson et al. 1993; Verdon et al. 2013), social rank may affect how individual sows perform in groups from both welfare and productivity perspectives. Thus, group housing of sows allows all of them more freedom of movement, exploration and socialisation, but a few may suffer from excessive aggression, stress and injuries. While it is obviously important to reduce aggression and stress at a group level, it is also important to appreciate the welfare implications for individuals. Where individuals are at risk, decisions need to be made about what priority to attach to different classes of animals: the majority, the most vulnerable or the most productive (Fraser 2003).
Conclusions The agenda set by the Brambell Committee in 1965 was that animal welfare should be evaluated using scientific evidence about the feelings of animals as indicated by their structure and function and their behaviour, and that this should occur via research into veterinary medicine, stress physiology, animal science and animal behaviour. The Brambell Committee’s agenda was an extraordinarily insightful direction that has been followed by animal welfare scientists for nearly five decades and gave rise to the biological functioning, affective state and natural-living conceptual frameworks. Consideration of our duties towards animals, as well as matters related to human health, and economic, social, environmental and other factors, are all involved in resolving the question of whether or not a particular animal use is acceptable, but science provides the means to understand the impact of each animal use on the animal. That is, science has a prominent role in underpinning decisions on animal use and the attendant conditions and compromises. This is illustrated here by brief reference to some aspects of pregnant sow housing, mainly researched by the application of the biological functioning conceptual framework, extended to emphasise affective outcomes for the animals. There are challenges and potential opportunities for the continued improvement in animal welfare through well-focused research and multidisciplinary welfare assessment. Methods to assess negative emotional experiences or affective states have been developed based on physiology and behaviour, but there is a growing body of neuroscience evidence that supports cautiously interpreting particular behaviours in terms of positive affects that animals may experience. This is anticipated to increasingly direct attention towards positive welfare states, thereby extending the almost exclusive focus of the last 40 years on preventing and ameliorating negative states. Accordingly, the future management of sentient animals will also require the promotion of positive affective experiences and this is likely to be a major focus for animal welfare science activity in the early twenty-first century.
29
References Andersen IL, Bøe KE, Kristiansen AL. The influence of different feeding arrangements and food type on competition at feeding in pregnant sows. Applied Animal Behaviour Science 65, 91–104, 1999 *Barnett JL. Modifying the design of group pens with individual feeding places affects the welfare of pigs. In: Bottcher RW, Hoff SJ (eds). Livestock Environment V, Volume II. Pp 613–18. American Society of Agricultural Engineers, St Joseph, Michigan, USA, 1997 *Barnett JL. Studying stress to assess animal welfare. In: Paterson JE (eds). Manipulating Pig Production IX. Pp 107–20. Australasian Pig Science Association, Werribee, Australia, 2003 Barnett JL, Hemsworth PH. Welfare monitoring schemes: using research to safeguard the welfare of animals on the farm. Journal of Applied Animal Welfare Science 12, 114–31, 2009 Barnett JL, Hemsworth PH, Cronin GM, Newman EA, McCallum TH, Chilton D. Effects of pen size, partial stalls and method of feeding on welfare-related behavioural and physiological responses of group-housed pigs. Applied Animal Behaviour Science 34, 207–20, 1992 Barnett JL, Cronin GM, McCallum TH, Newman EA. Effects of pen size/shape and design on aggression when grouping unfamiliar adult pigs. Applied Animal Behaviour Science 36, 111–22, 1993 Bench CJ, Rioja-Lang FC, Hayne SM, Gonyou HW. Group gestation housing with individual feeding—I: How feeding regime, resource allocation, and genetic factors affect sow welfare. Livestock Science 152, 208–17, 2013a Bench CJ, Rioja-Lang FC, Hayne SM, Gonyou HW. Group gestation housing with individual feeding—II: How space allowance, group size and composition, and flooring affect sow welfare. Livestock Science 152, 218–27, 2013b Bergeron R, Bolduc J, Ramonet Y, Meunier-Salaun MC, Robert S. Feeding motivation and stereotypies in pregnant sows fed increasing levels of fibre and/or food. Applied Animal Behaviour Science 70, 27–40, 2000 Boissy A, Manteuffel G, Jensen MB, Oppermann M, Spruijt B, Keeling LJ, Winckler C, Forkman B, Dimitrov I, Langbein J, et al. Assessment of positive emotions in animals to improve their welfare. Physiology and Behaviour 92, 375–97, 2007 *Brambell FWR, Barbour DS, Barnett MB, Ewer TK, Hobson A, Pitchforth H, Smith WR, Thorpe WH, Winship FJW. Report of the Technical Committee to Enquire into the Welfare of Animals Kept Under Intensive Husbandry Systems. Her Majesty’s Stationery Office, London, United Kingdom, 1965 Broom DM. Indicators of poor welfare. British Veterinary Journal 142, 524–6, 1986 *Broom DM. Coping, stress and welfare. In: Broom DM (eds). Coping with Challenge: Welfare in Animals including Humans. Pp 1–9. Daglem University Press, Berlin, Germany, 2000 Burgdorf J, Panksepp J. The neurobiology of positive emotions. Neuroscience and Biobehavioral Reviews 30, 173–87, 2006 Dantzer, R. Les émotions. P 21. Presses Universitaires de France, Paris, 1988 D’Eath RB, Roehe R, Turner SP, Ison SH, Farish M, Jack MC, Lawrence AB. Genetics of animal temperament: aggressive behaviour at mixing is genetically associated with the response to handling in pigs. Animal 3, 1544–54, 2009 Denton DA, McKinley MJ, Farrell M, Egan GF. The role of primordial emotions in the evolutionary origin of consciousness. Consciousness and Cognition 18, 500–14, 2009 Duncan IJH. Science-based assessment of animal welfare: Farm animals. Scientific and Technical Review, Office International des Epizooties 24, 483–92, 2005 *Duncan IJH, Fraser D. Understanding animal welfare. In: Appleby MC, Hughes BO (eds). Animal Welfare. Pp 19–31. CAB International, Wallingford, Oxfordshire, United Kingdom, 1997 Fisher MW, Mellor DJ. Developing a systematic strategy incorporating ethical, animal welfare and practical principles to guide the genetic improvement of dairy cattle. New Zealand Veterinary Journal 65, 100–6, 2008 Fraser D. Assessing animal welfare at the farm and group level: the interplay of science and values. Animal Welfare 12, 433–43, 2003. *Fraser D. Understanding Animal Welfare: The Science in its Cultural Context. Wiley-Blackwell, Chichester, West Sussex, United Kingdom, 2008 Fraser D, Duncan IJH. “Pleasures”, “pains” and animal welfare; towards a natural history of affect. Animal Welfare 7, 383–96, 1998 *Fraser D, Nicol CJ. Preference and motivation research. In: Appleby MC, Mench JA, Olsson IAS, Hughes BO (eds). Animal Welfare. Pp 183–99. CAB International, Oxon, United Kingdom, 2011 Fraser D, Duncan IJH, Edwards SA, Grandin T, Gregory NG, Guyonnet V, Hemsworth PH, Huertas SM, Huzzey JM, Mellor DJ, et al. General principles for the welfare of animals in production systems: The underlying science and its application. The Veterinary Journal 198, 19–27, 2013
Downloaded by [Colorado College] at 15:57 30 March 2015
30
New Zealand Veterinary Journal, 2015
*Gonyou HW. The social behaviour of pigs. In: Keeling LJ, Gonyou HW (eds). Social Behaviour in Farm Animals. Pp 147–76. CAB International, Oxon, United Kingdom, 2001 Green TC, Mellor DJ. Extending ideas about animal welfare assessment to include ‘quality of life’ and related concepts. New Zealand Veterinary Journal 59, 263– 71, 2011 *Hemsworth PH, Coleman GJ. Human-Livestock Interactions: the Stockperson and the Productivity and Welfare of Farmed Animals. 2nd Edtn. CAB International, Oxon, United Kingdom, 2011 Hemsworth PH, Barnett JL, Hansen C, Winfield CG. Effects of social environment on welfare status and sexual behaviour of female pigs. II. Effects of space allowance. Applied Animal Behaviour Science 16, 259–67, 1986 *Hemsworth PH, Barnett JL, Rickard M, Coleman GJ. Australia’s research and development capacity in animal welfare. Farm Policy Journal 4 (4), 23–31, 2007 Hemsworth PH, Rice M, Nash J, Giri K, Butler KL, Tilbrook AJ, Morrison RS. Effects of group size and floor space allowance on grouped sows: aggression, stress, skin injuries and reproductive performance. Journal of Animal Science 91, 1–12, 2013 Hutson GD. A note on hunger in the pig: sows on restricted rations will sustain an energy deficit to gain additional food. Animal Production 52, 233–5, 1991 *Kaltas GA, Chrousos GP. The neuroendorinology of stress. In: Cacioppo JT, Tassinary LG and Berntson GG (eds). Handbook of Psychophysiology. Pp 303–18. Cambridge University, Cambridge, UK, 2007 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 Lauber M, Nash JA, Gatt A, Hemsworth PH. Prevalence and incidence of abnormal behaviours in individually housed sheep. Animals 2, 27–37, 2012 Lawrence AB, Terlouw EMC. A review of behavioural factors involved in the development and continued performance of stereotypic behaviours in pigs. Journal of Animal Science 71, 2815–25, 1993 *Levy N. What Makes Us Moral?. Crossing the Boundaries of Biology. Oneworld, Oxford, United Kingdom, 2004 *Lindberg AC. Group life. In: Keeling LJ, Gonyou HW (eds). Social Behaviour in Farm Animals. Pp 37–58. CAB International, Wallingford, Oxfordshire, United Kingdom, 2001 Løvendahl P, Damgaard LH, Nielsen BL, Thodberg K, Su G, Rydhmer L. Aggressive behaviour of sows at mixing and maternal behaviour are heritable and genetically correlated traits. Livestock Production Science 93, 73–85, 2005 *Marchant-Forde JN, Marchant-Forde RM. Minimizing inter-pig aggression during mixing. Pig News and Information 26, 63N–71N, 2005 Mellor DJ. Animal emotions, behaviour and the promotion of positive welfare states. New Zealand Veterinary Journal 60, 1–8, 2012 *Mellor DJ. Production Animals: Ethical and welfare issues raised by productionfocused management of newborn livestock. In: Wathes CM, Corr SA, May SA, McCulloch SP, Whiting MC (eds). Veterinary and Animal Ethics: Proceedings of the first International Conference on Veterinary and Animal Ethics. Pp 174–87. Wiley-Blackwell, Oxford, United Kingdom, 2013 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. Positive animal welfare states and reference standards for welfare assessment. New Zealand Veterinary Journal 63, 17–23, 2015c 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, Patterson-Kane E, Stafford KJ. The Sciences of Animal Welfare. Wiley-Blackwell Publishing, Oxford, United Kingdom, 2009 Mendl M, Zanella AJ, Broom DM. Physiological and reproductive correlates of behavioural strategies in female domestic pigs. Animal Behaviour 44, 1107– 21, 1992 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 Meunier-Salaün MC, Edwards SA, Robert S. Effect of dietary fibre on the behaviour and health of the restricted sow. Animal Feed Science and Technology 90, 53–69, 2001 *Moberg GP. Biological response to stress: Implications for animal welfare. In Moberg GP, Mench GA (eds). The Biology of Animal Stress; Basic Principles
Hemsworth et al.
and Applications for Animal Welfare. Pp 1–21. CABI Publishing, Wallingford, United Kingdom, 2000 Nicol CJ, Caplen G, Edgar J, Browne WJ. Associations between welfare indicators and environmental choice in laying hens. Animal Behaviour 78, 413–24, 2009 Nicol CJ, Caplen G, Statham P, Browne WJ. Decisions about foraging and risk trade-offs in chickens are associated with individual somatic response profiles. Animal Behaviour 82, 255–62, 2011 *Nicholson RI, McGlone JJ, Reid LN. Quantification of stress in sows: comparison of individual housing versus social penning. Journal of Animal Science 71 (Suppl. 1), 112, 1993 *Olsson IAS, Wurbell H, Mench JA. Behaviour. In: Appleby MC, Mench JA, Olsson IAS, Hughes BO (eds.) Animal Welfare. Pp 138–154. CABI International, Wallingford, Oxfordshire, United Kingdom, 2011 Panksepp J. Affective consciousness: Core emotional feelings in animals and humans. Consciousness and Cognition 14, 30–80, 2005 Remience V, Wavreille J, Canart B, Meunier-Salaün MC, Prunier A, BartiauxThill N, Nicks B, Vandenheede M. Effects of space allowance on the welfare of dry sows kept in dynamic groups and fed with electronic sow feeder. Applied Animal Behaviour Science 112, 284–96, 2008 Salak-Johnson JL, Niekamp SR, Rodriguez-Zas SL, Ellis M, Curtis SE. Space allowance for dry, pregnant sows in pens: body condition, skin lesions and performance. Journal of Animal Science 85, 1758–69, 2007 Spoolder HAM, Burbidge JA, Edwards SA, Simmins PH, Lawrence AL. Provision of straw as a foraging substrate reduces the development of excessive chain and bar manipulation in food restricted sows. Applied Animal Behaviour Science 43, 249–62, 1995 *Stevens B, Barnett JL, Tilbrook AJ, Hemsworth PH. Effects of deprivation of a preferred resource (feed or social contact) on the biological functioning of pigs. In: van Barneveld RJ (eds). Manipulating Pig Production XII. P 28. Australasian Pig Science Association, Werribee, Victoria, Australia, 2009 Stewart CL, O’Connell NE, Boyle L. Influence of access to straw provided in racks on the welfare of sows in large dynamic groups. Applied Animal Behaviour Science 112, 235–47, 2008 *Tannenbaum J. The paradigm shift toward animal happiness: what it is, why it is happening, and what it portends for medical research. In: Paul EF and Paul J (eds). Why Animal Experimentation Matters: The use of Animals in Medical Research. Pp 93–130. Transaction Publishers, Somerset, New Jersey, USA, 2001 *Taylor IA, Barnett JL, Cronin GM. Optimum group size for pigs. In: Bottcher RW, Hoff SJ (eds). Livestock Environment V, Volume II. Pp 965–71. American Society of Agricultural Engineers, St Joseph, Michigan, USA, 1997 Terlouw EM, Lawrence AB, Illius AW. Influences of feeding level and physical restriction on development of stereotypies in sows. Animal Behaviour 42, 981–91, 1991 *Turner AI, Keating C, Tilbrook AJ. Sex differences and the role of sex steroids in sympatho-adrenal medullary system the hypothalamo-pituitary adrenal axis responses to stress. In: Kahn SM (eds). Sex Steroids. Pp 115–36. In Tech Publishing, Rijeka, Croatia, 2012 *Verdon M, Morrison R, Rice M, Hemsworth PH. Group-housed sows who engage in aggression after mixing have reduced injuries and gain more weight. Proceedings of the 47th International Society of Applied Ethology. P 68. Wageningen Academic Publishers, Wageningen, The Netherlands, Florianopolis, Brazil, 2013 *Verlarde A. Agonistic behaviour. In: Verlarde A, Geers R (eds). On Farm Monitoring of Pig Welfare. Pp 53–6. Wageningen Academic Press, Wageningen, The Netherlands, 2007 Wemelsfelder F, Mullan S. Applying ethological and health indictors to practical animal welfare assessment. Scientific and Technical Review, Office International des Epizooties 33, 111–20, 2014 Weng RC, Edwards SA, English PR. Behaviour, social interactions and lesion score of group-housed sows in relation to floor space allowance. Applied Animal Behaviour Science 59, 307–16, 1998 Whittaker X, Edwards SA, Spoolder HAM. Lawrence AB, Corning S. Effects of straw bedding and high fibre diets on the behaviour of floor fed group-housed sows. Applied Animal Behaviour Science 63, 25–39, 1999
Submitted 12 November 2013 Accepted for publication 10 September 2014 First published online 29 September 2014
*Non-peer-reviewed
