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Welfare issues in the reproductive management of small ruminants
Animal Reproduction Science 130 (2012) 141–146
Contents lists available at SciVerse ScienceDirect
Animal Reproduction Science journal homepage: www.elsevier.com/locate/anireprosci
Welfare issues in the reproductive management of small ruminants夽 P.A. Roger Veterinary Consultancy Services, Victoria Cottage, Reeth, Richmond, North Yorkshire DL11 6SZ, United Kingdom
a r t i c l e
i n f o
Article history: Available online 28 January 2012 Keywords: Goat Goat welfare Reproductive management Sheep Sheep welfare Welfare and reproduction
a b s t r a c t Often, the welfare of sheep and goats is focussed on flock/herd management and the major issues surrounding parturition and early development of lambs/kids. There is an increased interest in the way we manage domestic species and small ruminants are perceived as having a green and welfare friendly image. The management of reproduction in these species has the potential to affect this perception and the limiting factors for these procedures are discussed. Discussion of genetic modification and manipulation has become a focal point in the critical appraisal of the management of farmed livestock and the importance of the consideration of the mental health and well being of the animal is considered as an important part of this analysis. The diversity of options that are available for this analysis and the application of these options is discussed. © 2012 Elsevier B.V. All rights reserved.
1. Introduction Welfare issues in the reproductive management of small ruminants reflect to some extent the direct effect management has on the modification of natural behaviour. This is evidenced in a number of ways: (i) direct impact of management strategies on natural behaviour through restriction, (ii) direct impact of management strategies through modification of natural behaviour or (iii) commercial or breeding outputs desired by the flock or herd owner. However, it has been recognised that there should be a proper assessment of welfare, not only for novel or existing technologies, but also for conventional breeding programmes. It is within the area of conventional breeding that some serious and extensive farm animal welfare problems are currently found in commercial agriculture (Farm Animal Welfare Council, 2004). The contents of this paper will be directed to the management of breeding and will not address the problems
夽 This paper is part of the special issue entitled: Reproductive Health Management of Sheep and Goats, Guest Edited by G.S. Amiridis and G.C. Fthenakis. E-mail address: [email protected] 0378-4320/$ – see front matter © 2012 Elsevier B.V. All rights reserved. doi:10.1016/j.anireprosci.2012.01.007
raised by considering the impact of breeding strategies which may pose larger ethical questions. In fact, it has been recorded that animal biotechnology causes worries in public perception. Questions such as “what sort of animals should there be?” are outside the remit of this discussion. 2. Welfare concerns and behavioural responses to management practice Whay (2007) suggests that changes leading to a sustained improvement in animal welfare, need to assure animal carers that the changes they are making will have effect. This will be governed by the individual’s perception of the problem and by the perceived benefits of the intervention as well as the perceived barriers to the implementation of that intervention (Rosenstock, 1974). An Agricultural and Environment Biotechnology Committee (2002) report recommended that “a new strategic advisory body should be set up to examine issues raised by the use of genetic biotechnology on farm animals in the context of its use on other animals and current livestock farming practices”. As breeding came under the control of Man, sheep and goat characteristics began to be shaped by man’s requirements (Dwyer, 2008). It is a mark of the widespread
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P.A. Roger / Animal Reproduction Science 130 (2012) 141–146
acceptance of the close relationship between health and welfare that allows clinical evidence to be considered without specific mention of the potential impact on an individual’s welfare status (Lovatt, 2010). Dwyer (2008) outlines the well-developed social behaviour of both sheep and goats, which includes home range behaviour, social group size and strength of social attachment. This also engenders cultural knowledge for the flock or group. This knowledge is used to facilitate handling and in the manipulation of the flock particularly during movement (Dwyer, 2003). There is little agonistic activity in the female, except when protecting their young, but the male displays can be long-lasting and damaging; in that sense, horns act as rank symbols. Social recognition is based on visual and olfactory stimuli through scent glands on the feet and in the inguinal and facial areas (sheep) and on the hind feet and around the tail (goats). Sheep have a remarkable range of facial recognition and to be able to remember these images for at least 2 years (Kendrick et al., 2001). Sheep also show a wide variety of foraging and feeding behaviours dependent on climate, the range of food sources available, diet selection and social factors as well as variation between breeds and between husbandry type (e.g. hill or lowland) (Eskebo, 2011). Water is a daily requirement and although goats are better at conserving water and desert breeds of sheep (the fat-rumped and fat-tailed breeds) cope better in arid conditions, a water source remains a high priority for all flocks/herds. In fact, the high priorities to sheep and goats are proximity to escape terrain (Dwyer, 2004), the availability of suitable forage and a water supply. Sheep require access to shade and cope less well with heat, whereas goats have a lesser tolerance for cold. It is important to recognise these basic behavioural patterns and to bear them in mind when planning the breeding management of a flock or herd or a group of sheep or goats. Small ruminants are seasonally polyoestrous animals. Although there is some variation in the length of the oestrous cycle between individuals, the average length of the cycle is 16–17 days in sheep; which is much shorter than the cycle in cattle. The oestrous cycle in goats averages 21 days, which is closer to the average for cattle of 21–24 days. However, welfare considerations are wider than the mechanistic boundaries previously described in this paper and welfare status is now more fairly recognised as constituting both physical and mental attributes; the mixing of these attributes causes difficulties in establishing any objective repeatable analyses of welfare indices as it encompasses both qualitative and quantitative measures (Broom, 2007). The assessment of the emotional status of a sheep and its preferences, which allow the welfare status to move from the conceptual position of a ‘life worth living’ to a ‘good life’ are not easily established. Specific legislation on farm animal breeding procedures is now in force as a result of European Directive 98/58/EC concerning the protection of animals for farming purposes. In the United Kingdom, this is implemented by the Animal Welfare Act (2006) and by the Welfare of Farm Animals (England) Regulations (2007), as well as the equivalent Regulations for the devolved administrations, which state
that “natural or artificial breeding procedures which cause, or are likely to cause, suffering or injury to any of the animals concerned shall not be practised” and that: “no animal shall be kept for farming purposes unless it can reasonably be expected, on the basis of their genotype or phenotype, that they can be kept without detrimental effect on their health and welfare”. In the United Kingdom, the Sheep Veterinary Society (Hosie and Lowseck, 2005) and the British Cattle Veterinary Association (2010) have both produced guidelines on advanced breeding technologies, which recognise welfare concerns to reduce certain breeding-associated problems, but their impact on welfare will be determined by the extent to which they are adopted and applied in any given livestock sector. The Royal College of Veterinary Surgeons (2004) advises on artificial breeding techniques, including embryo collection and transfer, in its Guide to Professional Conduct. The advice is based upon the Bovine Embryo (Collection, Production and Transfer) Regulations (1995), but, through its professional guidance, the College extends the principles to other species and techniques used in advanced breeding technology. In these regulations, it is stressed that, at all stages in such procedures, the welfare of animals should be paramount. This advice is only applicable in techniques where veterinarians are directly involved or are responsible for supervision. Finally, on a European basis, the Code of Good Practice for European Farm Animal Breeding and Reproduction (CODE-EFABAR) is now available (European Forum of Farm Animal Breeders, 2000). Welfare is given a high priority within all these documents. These have the potential to enhance the prominence of animal welfare as a key issue in changing breeding strategies. However, it must be recognised that many breed organisations operate within world markets and this may constrain the degree to which such documents may address welfare concerns, particularly those which, in order to enhance welfare, might constrain the ability to achieve the gains that commercial sustainability usually requires. One of the continuing difficulties is the lack of a standard definition for welfare. Broom (1996) suggested welfare was the property of the individual and that it was reflected in the animal’s ability to cope with its environment and that this could be reflected by an arbitrary scale of welfare ranging from very bad to very good, but objective measurements are difficult to arrive at, particularly if focussed on inputs rather than outputs of a system. Webster (2011) expanded these ideas to describe good welfare as fit and feeling good bringing in the emotional qualitative assessment, which is a very important part of estimating welfare state, but is much more difficult to quantify as it presents a qualitative assessment and so can be used to direct quantitative values towards an appropriate end of the spectrum of welfare status. Quantitative measurements of behavioural, physiological, biochemical, pathological states need to be married with emotional and legal indicators to provide this information (Wemelsfelder and Farish, 2004; Dwyer, 2008; Roger, 2008). The report of the Banner Committee (1995) illustrated ethical concerns with a hypothetical example of a breeding strategy, the aim of which was to produce pigs of reduced
P.A. Roger / Animal Reproduction Science 130 (2012) 141–146
sentience and disinclined to engage in activity normal to them. The report stated that “even if this has no welfare implications (if welfare is understood narrowly as relating to an animal’s happiness), so that by any available measure such pigs are as content as any other pigs, still we would maintain that the proposed modification is morally objectionable in treating the animals as raw materials upon which our ends and purposes can be imposed regardless of the ends and purposes which are natural to them. The fact that the project promises an increase in profit, or any other desirable consequence, does not, and cannot, wipe out the intrinsically objectionable character of such an action”. A problem in the case of novel technologies is that many are developed from commercial sources. Technologies can be purchased by veterinary surgeons as part of ‘recognised veterinary practice’. These could become established within livestock farming, before there had been any proper evaluation of welfare implications. In the Banner report, ovum pickup was cited as a particular area of concern. This potential problem is also well illustrated by juvenile in vitro embryo transfer (JIVET), a technique which has been developed in Australia. JIVET is the mechanism through which follicle growth in juvenile animals (ewe-lambs or doe-kids, 6–8 weeks old) can be stimulated, offering the potential to substantially reduce generation intervals and produce multiple progeny. Practically, the technique requires hormone treatment of prepubertal animals, followed by oocyte recovery under general anaesthesia and via laparoscopy. Although this procedure, which presents clear ethical questions and may carry potential welfare problems, is not currently used in United Kingdom’s commercial agriculture, the possibility that this may become the case, just as in Australia, exists. Kent (2002) provides an example of the variation in legal controls across different countries around the world. Methods of detecting such uses remain important, as is the continued monitoring for an extended period ensures that welfare problems, which may exist, but may not be immediately obvious initially, are detected further down the line. Additional welfare problems may be associated with the implementation of breeding technologies already in existence. For example, there are no codes to govern the number of embryos, which may be implanted into ewes or does, or the number of times such a procedure may be performed. In the United Kingdom, surveillance (both passive and active) by various bodies, such as the Animal Health Veterinary Laboratories Agency (AHVLA) and the Food Standards Agency (FSA) (formerly covered by the State Veterinary Service, the Veterinary Laboratories Agency and the Meat Hygiene Service) may be effective in discovering welfare problems, but this is a reactive, rather than a proactive approach. Furthermore, current resources available to such agencies will limit the ability to detecting problems. The limitation of resources makes it impossible to inspect regularly and effectively a sufficient proportion of agricultural holdings. Compared with the situation in research establishments, where every licensed laboratory is subject to at least an annual visit by the competent authority, farms might go for many years without any inspection. This is a potential problem for both the
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detection of novel techniques applied, as well as for the monitoring of welfare problems that might arise in commercial farming. The opportunity and impact that proper implementation of farm health planning could have in this area is immense, providing proper levels of funding are introduced to recognise the benefits of surveillance and prevention for the common good. Data outlining common endemic disease status and statistics are not easily available and should be a priority for any animal health and welfare initiative. The Federation of Veterinarians in Europe (1999) suggested that “it may become difficult or impossible for natural copulation or parturition to occur; offspring produced by selective breeding for certain specific characteristics may be unable to express their natural behaviour; or they may be predisposed to hereditary, congenital, metabolic or infectious disease, disability or early death. The introduction of such selective breeding programmes may make it impossible for the breed to be maintained by natural means” and then continued “the use of new and emerging technologies in artificial breeding, such as ovum and embryo transplantation and genetic manipulation, may also be a source of concern, and it is likely that some future advances in science will also have animal welfare implications. The technique used may carry inherent welfare risks for the animal (e.g. the particular method by which semen or ova are obtained); the intended outcome of the procedure may be intrinsically objectionable (e.g. the development of animals with unnatural physical or behavioural characteristics); and offspring may be produced with welfare disadvantages such as those mentioned above”. Growing commercial interest in the potential of markerassisted selection will likely accelerate the rate of genetic change to livestock by conventional selection methods. The primary focus of attention will be for production-related traits (Farm Animal Welfare Council, 1998). There are research groups using marker-assisted selection for animals with greater levels of disease resistance or resilience, for example, parasite resistance in sheep. Whilst this will have obvious welfare benefits, it is important that the development of such strains is not used to disguise welfare threatening conditions, which would, otherwise, produce disease and does not discourage the development of higher standards of stockmanship and provision of a good quality environment. However, breeding-related welfare problems cannot be viewed in isolation, because most are inextricably linked with the environment in which animals are kept. Of fundamental importance is the quality of management of any animal throughout its life, but there are many other aspects of the environment, which, if inappropriate for a particular genotype, may have consequences for welfare which are just as serious as poor management. Webster et al. (2004) noted that, although good agreement could be achieved on identifying and measuring particular welfare issues, the implementation of improvements as evidenced by assurance was still uncertain. For example, welfare problems may arise where a particular breed of animal is poorly suited to the environment where it is reared. There remains concern about the
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potential problems associated with changes in breed structure in response to the commercial demand for different carcase conformation characteristics. Changes in breed or breed-type can only be contemplated in challenging extensive conditions where replacement is with one that is sufficiently well adapted to the environment. This also reflects concerns about the future sustainability of the current structure of the sheep industry. In the United Kingdom, the traditional approach to the sheep year and the traditional approach to the transfer of breeding stock mean that risk management for disease control is severely compromised and proper quarantine and isolation regimens are practically not possible to deliver. The industry needs to restructure, in order to meet acceptable standards in terms of responsibility and cost sharing and in maintaining a sustainable future for the industry. Research on sheep breeding programs at the Scottish Agriculture College has incorporated traits that are important for being a ‘good’ ewe alongside those important for being a ‘good’ lamb, in addition to key sustainability traits, such as lamb survival and ewe longevity. The new breeding indices developed are intended to improve flock efficiency without detriment to mothering ability and survival characteristics in extensive farming situations (Goddard, 2008). The researchers recognise the value of the research to the wider hill sheep industry, where, in order to offset falling incomes, there has been a trend to increase the number of sheep per shepherd and to reduce the amount of veterinary care used for disease prevention and treatment. The standard of management is an aspect of the environment in which an animal is kept, and, with improved management, many of the genotypes with greater production potential can often be reared without major welfare concerns. There remains a necessity of the amount of skill required by those persons responsible for some genotypes given the known variation in standards of management across farms. For example, Scott et al. (2009) described manipulation of production by use of melatonin implants in commercial sheep flocks and highlight the need for good husbandry and management of the flock, if this is to be used successfully. Also, they emphasised the importance of an effective veterinary health plan to support a beneficial treatment effect. Goddard (2010) emphasises the importance of having sheep that are adapted for being managed in specific production system, of the right breed and type suited to the terrain and environmental conditions. The Banner Committee (1995) considered a procedure may be intrinsically objectionable for any one of the following reasons: (i) it results in very severe or lasting pain on the animals concerned, (ii) it involves an unacceptable violation of the integrity of an animal, (iii) it is associated with the mixing of kinds of animals to an extent which is unacceptable and (iv) it generates living beings whose sentience has been reduced to an excessive extent. Whilst points (i) and (iii) should be adequately catered for under current welfare regulations, decisions about unacceptable violation of integrity or reduction in sentience are not.
Both conventional and novel breeding techniques have the capacity to produce animals, whose ability to adapt has been altered to an unacceptable degree. Animal breeding and the use of breeding technologies is a dynamic and growing field that has the potential to influence animal welfare in a positive manner but progress must not compromise welfare. Practical breeding management focuses on a number of areas: (i) breed selection, (ii) individual selection, (iii) nutrition and (iv) breeding strategy. Each of these areas can enhance elements of concern with regard to welfare. This can be from a risk of exposure to poor welfare through increased disease risk, through behavioural limitation in controlled breeding programmes or through the use of potentially aversive techniques associated with planned breeding. Control of nutritional plane and correction of dietary intake also remove a degree of autonomy from the sheep. Finally, routine preparations can expose sheep to aversive situations in the build up to the start of tupping. Equally, management depends on: (i) knowledgeable workforce, (ii) sustainable approach and (iii) environmental awareness. Waterhouse (1996) has shown how technological advances have allowed hill sheep ewe and lamb mortality figures to be halved over the last four decades. Dwyer (2008) points out that these practices overcome some of the deficiencies in a more traditional approach by confronting the often fatalistic acceptance of misfortune. Breeding technique, often, may not be the primary contributor for poorer welfare, but feed and other resources may warrant particular attention; the effect on lamb birth weight may be the most important output indicator in these situations. Abecia et al. (2011) have summarised issues with the different methods used to manipulate the breeding season; these include: (i) melatonin implants, with which issues arise with site of implant, skill of administration, need for ram numbers to be proportionately present, and (ii) intra-vaginal inserts, with which issues arise for the reasons above and also include a greater likelihood of local infection and/or adhesion formation, complicating their use. Murray and Ward (1993) reviewed welfare implications of new reproductive technologies available at that time and these were further considered in the Banner Committee (1995) report. It was concluded that, although laparoscopic techniques may be effective in decreasing timescales for genetic improvement rates, the restraint and adverse experience for the female animal may compound the welfare insult of hormonal control and not add to any improved quality of life. Hence, it becomes evident that there is always a conflict between commercial gain and welfare impact. Some of the impact on the ram is evidenced through the collection and assessment of semen. Collection of semen through the use of an artificial vagina and ‘teaser’ ewe or through electro-ejaculation result obviously result in well-recognisable welfare impact, as well as in reduced quality in sample collection, that being especially true in semen samples collected after electro-ejaculation. Stafford et al. (1996) suggest electro-ejaculation is no more aversive than part-shearing, but this perception may not be widely shared.
P.A. Roger / Animal Reproduction Science 130 (2012) 141–146
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Table 1 The ethical matrix as applied to the production of food from animals (Webster, 2011). Respect for
Beneficence (health and welfare)
Autonomy (freedom and choice)
Justice (fairness)
Farm animals Producers Consumers Living environment
Animal welfare Farmer welfare Safe wholesome food Conservation
Telos Choice of system Choice/labelling Biodiversity
Duty of care Fair trade and law Affordable food Sustainability of populations
Table 2 Stakeholder analysis and the four principles (an ethical framework common to human medicine).
System
Stocksman
Animal
Consumer
Autonomy
Beneficence
Non maleficence
Justice
Intensive systems: lessen choice – Extensive systems: enlarge choice Limited by system and knowledge
Provision of shelter, safety, food and water
Absence of harms
Fair in terms of return needed
Trained in husbandry
Obeying published codes
Limits to autonomy considerable as pay-back to advantages of domestication Choice of source of foods
Provision of essentials
Only performing interventions for which trained Only necessary mutilations performed
Ability to select for higher welfare standards through cost
Able to direct production through buying habits
Legal limits of husbandry defined and best practices promoted Aware of rights and of safe food production – Interest in sustainability
Table 3 Simple analysis of different husbandry systems using the five freedoms (after Webster, 2011). Factor
Hunger and thirst Comfort Disease and pain Stress Fear Natural behaviour
Production system Housed
In-bye
Extensive
Adequate Good Low risk biosecurity and hygiene Boredom; interactions necessary Low, provided empathetic stockspersons Restricted by pen size and numbers
Variable, but controlled Variable – Management important Low risk More interest Low Controlled
Variable Variable choice available Risk increased – Delayed detection Interest, but exposed to increased risks Low, but gathering likely to be very aversive Most natural for most breeds
Technologies progress and with improvement they may have a lesser impact on welfare. An example of this is the increasingly widespread use of ultrasonographic equipment for pregnancy diagnosis, which can be performed on standing ewe, reducing welfare costs for gathering and handling. Russel and Goddard (1995) reported on the widespread use of this technique and Scott (2007) has advocated its increased use in clinical diagnosis as well as for pregnancy detection. It is often useful to describe welfare impacts through the application of ethical framework analysis and the use of the common human clinical framework of ‘Autonomy’, ‘Beneficence’, ‘Non-maleficence’ and ‘Justice’ (i.e. the four principles approach) (Mepham, 2005) may be a helpful tool here (Table 1). Stakeholder analysis also aids in focussing welfare impacts and considers all contributors in a particular situation to help derive an answer to limits of procedure (Table 2). Table 3 shows how all contributors can focus on welfare impacts to try to derive an answer to procedural limits. 3. Concluding remarks At the same time as welfare is considered across the flock/herd, it must be remembered that the indicators developed to assess welfare are developed in a
relatively small number of animals and that it is likely that widespread individual variation between breeds and between individuals within those breeds exists. Hence, it is important that measures used are recognised with their limitations and not given absolute status. For the introduction of new techniques to the industry, the type of analysis described above can help to provide limits to the use or abuse of the technique. Equally important is a reflection on current practice and these analytical tools aid the revisiting of the ethical concerns raised in our manipulation of animal reproduction at the flock or individual animal level. The concern for the individual highlights a need to understand the relative importance to the animal of the varying parameters that are presently used to describe welfare attributes. Because of the difficulties involved in these assessments, we tend to apply the perceived wisdom across the species and perhaps fail to understand the important variations that any population of individuals possess; this further complicates our ability to assess welfare impact on the individual of any given procedure. Just as cost-benefit has been demonstrated not to be the driving priority behind the implementation and continuation of farm health plans, other drivers may be more important to small ruminants and, although perception would probably exclude benefits from team-work, it would
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recognise the cognitive ability of these animals to appreciate a more favourable welfare condition. Reproductive performance is a key part of successful small ruminant health management and must be supported by transparent standards promoting high welfare to maintain the green image of the industries. We need to provide more opportunity for sheep and goats to indicate prime strategies directed at moving welfare status from ‘a life worth living’ to ‘a good life’ and, at the same time, it must be acknowledged that no life is without challenge from stressors, such as fear and distress. Animal welfare is paramount to sustainable and productive systems; where we choose to place arbitrary controls on the continuum from very good welfare to very poor welfare remains an area in which legislation, education and continuing research need to provide clear universal guidance and delineation. Conflict of interest statement The author has no conflicts of interest to declare. References Abecia, J.A., Forcada, F., Gonzalez-Bulnes, A., 2011. Pharmaceutical control of reproduction in sheep and goats. Vet. Clin. N. Am. Food Anim. Pract. 27, 67–79. Agricultural and Environment Biotechnology Committee, 2002. Animals and Biotechnology. Department of Food and Rural Environment, London, 88 pp. Animal Welfare Act, 2006. http://www.legislation.gov.uk/ukpga/2006/ 45/contents. Banner Committee, 1995. Report of the Committee to Consider the Ethical Implications of Emerging Technologies in the Breeding of Farm Animals. Ministry of Agriculture, Fisheries and Food, London. Bovine Embryo (Collection, Production and Transfer) Regulations, 1995. http://www.legislation.gov.uk/uksi/1995/2478/contents. British Cattle Veterinary Association, 2010. http://www.bcva.eu/bcva/ content/welfare. Broom, D.M., 1996. Animal welfare defined in terms of attempts to cope with the environment. Acta Agric. Scand. 27, 22–28. Broom, D.M., 2007. Quality of life means welfare: how is it related to other concepts and assessed? Anim. Welf. 16S, 45–53. Dwyer, C.M., 2003. Behavioural development in the neonatal lamb: effect of maternal and birth-related factors. Theriogenology 59, 1027–1050. Dwyer, C.M., 2004. How has the risk of predation shaped the behavioural responses of sheep to fear and distress? Anim. Welf. 13, 269–281. Dwyer, C., 2008. The Welfare of Sheep. Springer, Berlin, 386 pp. European Forum of Farm Animal Breeders, 2000. EFABAR Code., http://www.effab.org. Eskebo, I., 2011. Farm Animal Behaviour. Characteristics for Assessment of Health and Welfare. CABI, Oxford, 248 pp.
Farm Animal Welfare Council, 1998. Report on the Implications of Cloning for the Welfare of Farmed Livestock. Department of Food and Rural Environment, London, 38 pp. Farm Animal Welfare Council, 2004. Report on the Welfare Implications of Animal Breeding and Breeding Technologies in Commercial Agriculture. Department of Food and Rural Environment, London, 48 pp. Federation of Veterinarians in Europe, 1999. FVE Policy on Genetic Modifications in Animals. FVE, Brussels, 32 pp. Goddard, P.J., 2008. Welfare goals from the perspective of extensively managed sheep. In: Proceedings of a Workshop, Aberdeen, p. 92. Goddard, P.J., 2010. Welfare assessment in sheep. In: Biancifiori, F. (Ed.), Animal Welfare. , pp. 215–244. Hosie, B.D., Lowseck, L.J., 2005. Sheep Veterinary Society policy statement on sheep welfare. In: Proceedings of the Sheep Veterinary Society, vol. 29, 2005, p. 65. Kendrick, K.M., da Costa, A.P., Hinton, M.R., Broad, K.D., Skinner, J.D., 2001. Sheep don’t forget a face. Nature 414, 165–166. Kent, J.E., 2002. Elective Surgeries (Mutilations): A Comparison of the Legislative Control of their Use in Farm Animals in the United Kingdom, America and New Zealand. A Report to the Sir Winston Churchill Memorial Trust, Canberra City. Lovatt, F.M., 2010. Clinical examination of sheep. Small Rumin. Res. 92, 72–77. Mepham, B., 2005. Bioethics. An Introduction for the Biosciences. Oxford University Press, Oxford, p. 402. Murray, R.D., Ward, W.R., 1993. Welfare implications of modern artificial breeding techniques for dairy cattle and sheep. Vet. Rec. 133, 283–286. Roger, P.A., 2008. The impact of disease and disease prevention on sheep welfare. Small Rumin. Res. 76, 104–111. Royal College of Veterinary Surgeons, 2004. Guide to Professional Conduct. The Royal College of Veterinary Surgeons, London. Rosenstock, I.M., 1974. The health belief model and preventive health behaviour. Health Educ. Monogr. 2, 354–386. Russel, A.J.F., Goddard, P.J., 1995. Small ruminant reproductive ultrasonography. In: Goddard, P.J. (Ed.), Veterinary Ultrasonography. CABI, Oxford, pp. 257–274. Scott, P.R., 2007. Sheep Medicine. Manson Publishing, London. Scott, P.R., Sargison, N.D., Macrae, A.I., Gough, M.R., 2009. Melatonin treatment prior to the normal breeding season increases the fetal number in United Kingdom sheep flocks. Vet. J. 182, 198–202. Stafford, K.J., Spoorenberg, J., West, D.M., Vermunt, J.J., Petrie, N., Lawoko, C.R.O., 1996. The effect of electro-ejaculation on aversive behaviour and plasma cortisol concentration in rams. N. Z. Vet. J. 44, 95–98. Waterhouse, A., 1996. Animal welfare and sustainability of production under extensive conditions – a European perspective. Appl. Anim. Behav. Sci. 49, 29–40. Wemelsfelder, F., Farish, M., 2004. Qualitative categories for the interpretation of sheep welfare: a review. Anim. Welf. 13, 261–268. Webster, A.J.F., 2011. Management and Welfare of Farm Animals – The UFAW Farm Handbook, 5th ed. Wiley, Oxford, 616 pp. Webster, A.J.F., Main, D.C.J., Whay, H.R., 2004. Welfare assessment: indices from clinical observation. Anim. Welf. 13, S93–S98. Welfare of Farm Animals (England) Regulations, 2007. http://www. legislation.gov.uk/uksi/2007/2078/pdfs/uksi 20072078 en.pdf. Whay, H.R., 2007. The journey to animal welfare improvement. Anim. Welf. 16, 117–122.
Contents lists available at SciVerse ScienceDirect
Animal Reproduction Science journal homepage: www.elsevier.com/locate/anireprosci
Welfare issues in the reproductive management of small ruminants夽 P.A. Roger Veterinary Consultancy Services, Victoria Cottage, Reeth, Richmond, North Yorkshire DL11 6SZ, United Kingdom
a r t i c l e
i n f o
Article history: Available online 28 January 2012 Keywords: Goat Goat welfare Reproductive management Sheep Sheep welfare Welfare and reproduction
a b s t r a c t Often, the welfare of sheep and goats is focussed on flock/herd management and the major issues surrounding parturition and early development of lambs/kids. There is an increased interest in the way we manage domestic species and small ruminants are perceived as having a green and welfare friendly image. The management of reproduction in these species has the potential to affect this perception and the limiting factors for these procedures are discussed. Discussion of genetic modification and manipulation has become a focal point in the critical appraisal of the management of farmed livestock and the importance of the consideration of the mental health and well being of the animal is considered as an important part of this analysis. The diversity of options that are available for this analysis and the application of these options is discussed. © 2012 Elsevier B.V. All rights reserved.
1. Introduction Welfare issues in the reproductive management of small ruminants reflect to some extent the direct effect management has on the modification of natural behaviour. This is evidenced in a number of ways: (i) direct impact of management strategies on natural behaviour through restriction, (ii) direct impact of management strategies through modification of natural behaviour or (iii) commercial or breeding outputs desired by the flock or herd owner. However, it has been recognised that there should be a proper assessment of welfare, not only for novel or existing technologies, but also for conventional breeding programmes. It is within the area of conventional breeding that some serious and extensive farm animal welfare problems are currently found in commercial agriculture (Farm Animal Welfare Council, 2004). The contents of this paper will be directed to the management of breeding and will not address the problems
夽 This paper is part of the special issue entitled: Reproductive Health Management of Sheep and Goats, Guest Edited by G.S. Amiridis and G.C. Fthenakis. E-mail address: [email protected] 0378-4320/$ – see front matter © 2012 Elsevier B.V. All rights reserved. doi:10.1016/j.anireprosci.2012.01.007
raised by considering the impact of breeding strategies which may pose larger ethical questions. In fact, it has been recorded that animal biotechnology causes worries in public perception. Questions such as “what sort of animals should there be?” are outside the remit of this discussion. 2. Welfare concerns and behavioural responses to management practice Whay (2007) suggests that changes leading to a sustained improvement in animal welfare, need to assure animal carers that the changes they are making will have effect. This will be governed by the individual’s perception of the problem and by the perceived benefits of the intervention as well as the perceived barriers to the implementation of that intervention (Rosenstock, 1974). An Agricultural and Environment Biotechnology Committee (2002) report recommended that “a new strategic advisory body should be set up to examine issues raised by the use of genetic biotechnology on farm animals in the context of its use on other animals and current livestock farming practices”. As breeding came under the control of Man, sheep and goat characteristics began to be shaped by man’s requirements (Dwyer, 2008). It is a mark of the widespread
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acceptance of the close relationship between health and welfare that allows clinical evidence to be considered without specific mention of the potential impact on an individual’s welfare status (Lovatt, 2010). Dwyer (2008) outlines the well-developed social behaviour of both sheep and goats, which includes home range behaviour, social group size and strength of social attachment. This also engenders cultural knowledge for the flock or group. This knowledge is used to facilitate handling and in the manipulation of the flock particularly during movement (Dwyer, 2003). There is little agonistic activity in the female, except when protecting their young, but the male displays can be long-lasting and damaging; in that sense, horns act as rank symbols. Social recognition is based on visual and olfactory stimuli through scent glands on the feet and in the inguinal and facial areas (sheep) and on the hind feet and around the tail (goats). Sheep have a remarkable range of facial recognition and to be able to remember these images for at least 2 years (Kendrick et al., 2001). Sheep also show a wide variety of foraging and feeding behaviours dependent on climate, the range of food sources available, diet selection and social factors as well as variation between breeds and between husbandry type (e.g. hill or lowland) (Eskebo, 2011). Water is a daily requirement and although goats are better at conserving water and desert breeds of sheep (the fat-rumped and fat-tailed breeds) cope better in arid conditions, a water source remains a high priority for all flocks/herds. In fact, the high priorities to sheep and goats are proximity to escape terrain (Dwyer, 2004), the availability of suitable forage and a water supply. Sheep require access to shade and cope less well with heat, whereas goats have a lesser tolerance for cold. It is important to recognise these basic behavioural patterns and to bear them in mind when planning the breeding management of a flock or herd or a group of sheep or goats. Small ruminants are seasonally polyoestrous animals. Although there is some variation in the length of the oestrous cycle between individuals, the average length of the cycle is 16–17 days in sheep; which is much shorter than the cycle in cattle. The oestrous cycle in goats averages 21 days, which is closer to the average for cattle of 21–24 days. However, welfare considerations are wider than the mechanistic boundaries previously described in this paper and welfare status is now more fairly recognised as constituting both physical and mental attributes; the mixing of these attributes causes difficulties in establishing any objective repeatable analyses of welfare indices as it encompasses both qualitative and quantitative measures (Broom, 2007). The assessment of the emotional status of a sheep and its preferences, which allow the welfare status to move from the conceptual position of a ‘life worth living’ to a ‘good life’ are not easily established. Specific legislation on farm animal breeding procedures is now in force as a result of European Directive 98/58/EC concerning the protection of animals for farming purposes. In the United Kingdom, this is implemented by the Animal Welfare Act (2006) and by the Welfare of Farm Animals (England) Regulations (2007), as well as the equivalent Regulations for the devolved administrations, which state
that “natural or artificial breeding procedures which cause, or are likely to cause, suffering or injury to any of the animals concerned shall not be practised” and that: “no animal shall be kept for farming purposes unless it can reasonably be expected, on the basis of their genotype or phenotype, that they can be kept without detrimental effect on their health and welfare”. In the United Kingdom, the Sheep Veterinary Society (Hosie and Lowseck, 2005) and the British Cattle Veterinary Association (2010) have both produced guidelines on advanced breeding technologies, which recognise welfare concerns to reduce certain breeding-associated problems, but their impact on welfare will be determined by the extent to which they are adopted and applied in any given livestock sector. The Royal College of Veterinary Surgeons (2004) advises on artificial breeding techniques, including embryo collection and transfer, in its Guide to Professional Conduct. The advice is based upon the Bovine Embryo (Collection, Production and Transfer) Regulations (1995), but, through its professional guidance, the College extends the principles to other species and techniques used in advanced breeding technology. In these regulations, it is stressed that, at all stages in such procedures, the welfare of animals should be paramount. This advice is only applicable in techniques where veterinarians are directly involved or are responsible for supervision. Finally, on a European basis, the Code of Good Practice for European Farm Animal Breeding and Reproduction (CODE-EFABAR) is now available (European Forum of Farm Animal Breeders, 2000). Welfare is given a high priority within all these documents. These have the potential to enhance the prominence of animal welfare as a key issue in changing breeding strategies. However, it must be recognised that many breed organisations operate within world markets and this may constrain the degree to which such documents may address welfare concerns, particularly those which, in order to enhance welfare, might constrain the ability to achieve the gains that commercial sustainability usually requires. One of the continuing difficulties is the lack of a standard definition for welfare. Broom (1996) suggested welfare was the property of the individual and that it was reflected in the animal’s ability to cope with its environment and that this could be reflected by an arbitrary scale of welfare ranging from very bad to very good, but objective measurements are difficult to arrive at, particularly if focussed on inputs rather than outputs of a system. Webster (2011) expanded these ideas to describe good welfare as fit and feeling good bringing in the emotional qualitative assessment, which is a very important part of estimating welfare state, but is much more difficult to quantify as it presents a qualitative assessment and so can be used to direct quantitative values towards an appropriate end of the spectrum of welfare status. Quantitative measurements of behavioural, physiological, biochemical, pathological states need to be married with emotional and legal indicators to provide this information (Wemelsfelder and Farish, 2004; Dwyer, 2008; Roger, 2008). The report of the Banner Committee (1995) illustrated ethical concerns with a hypothetical example of a breeding strategy, the aim of which was to produce pigs of reduced
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sentience and disinclined to engage in activity normal to them. The report stated that “even if this has no welfare implications (if welfare is understood narrowly as relating to an animal’s happiness), so that by any available measure such pigs are as content as any other pigs, still we would maintain that the proposed modification is morally objectionable in treating the animals as raw materials upon which our ends and purposes can be imposed regardless of the ends and purposes which are natural to them. The fact that the project promises an increase in profit, or any other desirable consequence, does not, and cannot, wipe out the intrinsically objectionable character of such an action”. A problem in the case of novel technologies is that many are developed from commercial sources. Technologies can be purchased by veterinary surgeons as part of ‘recognised veterinary practice’. These could become established within livestock farming, before there had been any proper evaluation of welfare implications. In the Banner report, ovum pickup was cited as a particular area of concern. This potential problem is also well illustrated by juvenile in vitro embryo transfer (JIVET), a technique which has been developed in Australia. JIVET is the mechanism through which follicle growth in juvenile animals (ewe-lambs or doe-kids, 6–8 weeks old) can be stimulated, offering the potential to substantially reduce generation intervals and produce multiple progeny. Practically, the technique requires hormone treatment of prepubertal animals, followed by oocyte recovery under general anaesthesia and via laparoscopy. Although this procedure, which presents clear ethical questions and may carry potential welfare problems, is not currently used in United Kingdom’s commercial agriculture, the possibility that this may become the case, just as in Australia, exists. Kent (2002) provides an example of the variation in legal controls across different countries around the world. Methods of detecting such uses remain important, as is the continued monitoring for an extended period ensures that welfare problems, which may exist, but may not be immediately obvious initially, are detected further down the line. Additional welfare problems may be associated with the implementation of breeding technologies already in existence. For example, there are no codes to govern the number of embryos, which may be implanted into ewes or does, or the number of times such a procedure may be performed. In the United Kingdom, surveillance (both passive and active) by various bodies, such as the Animal Health Veterinary Laboratories Agency (AHVLA) and the Food Standards Agency (FSA) (formerly covered by the State Veterinary Service, the Veterinary Laboratories Agency and the Meat Hygiene Service) may be effective in discovering welfare problems, but this is a reactive, rather than a proactive approach. Furthermore, current resources available to such agencies will limit the ability to detecting problems. The limitation of resources makes it impossible to inspect regularly and effectively a sufficient proportion of agricultural holdings. Compared with the situation in research establishments, where every licensed laboratory is subject to at least an annual visit by the competent authority, farms might go for many years without any inspection. This is a potential problem for both the
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detection of novel techniques applied, as well as for the monitoring of welfare problems that might arise in commercial farming. The opportunity and impact that proper implementation of farm health planning could have in this area is immense, providing proper levels of funding are introduced to recognise the benefits of surveillance and prevention for the common good. Data outlining common endemic disease status and statistics are not easily available and should be a priority for any animal health and welfare initiative. The Federation of Veterinarians in Europe (1999) suggested that “it may become difficult or impossible for natural copulation or parturition to occur; offspring produced by selective breeding for certain specific characteristics may be unable to express their natural behaviour; or they may be predisposed to hereditary, congenital, metabolic or infectious disease, disability or early death. The introduction of such selective breeding programmes may make it impossible for the breed to be maintained by natural means” and then continued “the use of new and emerging technologies in artificial breeding, such as ovum and embryo transplantation and genetic manipulation, may also be a source of concern, and it is likely that some future advances in science will also have animal welfare implications. The technique used may carry inherent welfare risks for the animal (e.g. the particular method by which semen or ova are obtained); the intended outcome of the procedure may be intrinsically objectionable (e.g. the development of animals with unnatural physical or behavioural characteristics); and offspring may be produced with welfare disadvantages such as those mentioned above”. Growing commercial interest in the potential of markerassisted selection will likely accelerate the rate of genetic change to livestock by conventional selection methods. The primary focus of attention will be for production-related traits (Farm Animal Welfare Council, 1998). There are research groups using marker-assisted selection for animals with greater levels of disease resistance or resilience, for example, parasite resistance in sheep. Whilst this will have obvious welfare benefits, it is important that the development of such strains is not used to disguise welfare threatening conditions, which would, otherwise, produce disease and does not discourage the development of higher standards of stockmanship and provision of a good quality environment. However, breeding-related welfare problems cannot be viewed in isolation, because most are inextricably linked with the environment in which animals are kept. Of fundamental importance is the quality of management of any animal throughout its life, but there are many other aspects of the environment, which, if inappropriate for a particular genotype, may have consequences for welfare which are just as serious as poor management. Webster et al. (2004) noted that, although good agreement could be achieved on identifying and measuring particular welfare issues, the implementation of improvements as evidenced by assurance was still uncertain. For example, welfare problems may arise where a particular breed of animal is poorly suited to the environment where it is reared. There remains concern about the
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potential problems associated with changes in breed structure in response to the commercial demand for different carcase conformation characteristics. Changes in breed or breed-type can only be contemplated in challenging extensive conditions where replacement is with one that is sufficiently well adapted to the environment. This also reflects concerns about the future sustainability of the current structure of the sheep industry. In the United Kingdom, the traditional approach to the sheep year and the traditional approach to the transfer of breeding stock mean that risk management for disease control is severely compromised and proper quarantine and isolation regimens are practically not possible to deliver. The industry needs to restructure, in order to meet acceptable standards in terms of responsibility and cost sharing and in maintaining a sustainable future for the industry. Research on sheep breeding programs at the Scottish Agriculture College has incorporated traits that are important for being a ‘good’ ewe alongside those important for being a ‘good’ lamb, in addition to key sustainability traits, such as lamb survival and ewe longevity. The new breeding indices developed are intended to improve flock efficiency without detriment to mothering ability and survival characteristics in extensive farming situations (Goddard, 2008). The researchers recognise the value of the research to the wider hill sheep industry, where, in order to offset falling incomes, there has been a trend to increase the number of sheep per shepherd and to reduce the amount of veterinary care used for disease prevention and treatment. The standard of management is an aspect of the environment in which an animal is kept, and, with improved management, many of the genotypes with greater production potential can often be reared without major welfare concerns. There remains a necessity of the amount of skill required by those persons responsible for some genotypes given the known variation in standards of management across farms. For example, Scott et al. (2009) described manipulation of production by use of melatonin implants in commercial sheep flocks and highlight the need for good husbandry and management of the flock, if this is to be used successfully. Also, they emphasised the importance of an effective veterinary health plan to support a beneficial treatment effect. Goddard (2010) emphasises the importance of having sheep that are adapted for being managed in specific production system, of the right breed and type suited to the terrain and environmental conditions. The Banner Committee (1995) considered a procedure may be intrinsically objectionable for any one of the following reasons: (i) it results in very severe or lasting pain on the animals concerned, (ii) it involves an unacceptable violation of the integrity of an animal, (iii) it is associated with the mixing of kinds of animals to an extent which is unacceptable and (iv) it generates living beings whose sentience has been reduced to an excessive extent. Whilst points (i) and (iii) should be adequately catered for under current welfare regulations, decisions about unacceptable violation of integrity or reduction in sentience are not.
Both conventional and novel breeding techniques have the capacity to produce animals, whose ability to adapt has been altered to an unacceptable degree. Animal breeding and the use of breeding technologies is a dynamic and growing field that has the potential to influence animal welfare in a positive manner but progress must not compromise welfare. Practical breeding management focuses on a number of areas: (i) breed selection, (ii) individual selection, (iii) nutrition and (iv) breeding strategy. Each of these areas can enhance elements of concern with regard to welfare. This can be from a risk of exposure to poor welfare through increased disease risk, through behavioural limitation in controlled breeding programmes or through the use of potentially aversive techniques associated with planned breeding. Control of nutritional plane and correction of dietary intake also remove a degree of autonomy from the sheep. Finally, routine preparations can expose sheep to aversive situations in the build up to the start of tupping. Equally, management depends on: (i) knowledgeable workforce, (ii) sustainable approach and (iii) environmental awareness. Waterhouse (1996) has shown how technological advances have allowed hill sheep ewe and lamb mortality figures to be halved over the last four decades. Dwyer (2008) points out that these practices overcome some of the deficiencies in a more traditional approach by confronting the often fatalistic acceptance of misfortune. Breeding technique, often, may not be the primary contributor for poorer welfare, but feed and other resources may warrant particular attention; the effect on lamb birth weight may be the most important output indicator in these situations. Abecia et al. (2011) have summarised issues with the different methods used to manipulate the breeding season; these include: (i) melatonin implants, with which issues arise with site of implant, skill of administration, need for ram numbers to be proportionately present, and (ii) intra-vaginal inserts, with which issues arise for the reasons above and also include a greater likelihood of local infection and/or adhesion formation, complicating their use. Murray and Ward (1993) reviewed welfare implications of new reproductive technologies available at that time and these were further considered in the Banner Committee (1995) report. It was concluded that, although laparoscopic techniques may be effective in decreasing timescales for genetic improvement rates, the restraint and adverse experience for the female animal may compound the welfare insult of hormonal control and not add to any improved quality of life. Hence, it becomes evident that there is always a conflict between commercial gain and welfare impact. Some of the impact on the ram is evidenced through the collection and assessment of semen. Collection of semen through the use of an artificial vagina and ‘teaser’ ewe or through electro-ejaculation result obviously result in well-recognisable welfare impact, as well as in reduced quality in sample collection, that being especially true in semen samples collected after electro-ejaculation. Stafford et al. (1996) suggest electro-ejaculation is no more aversive than part-shearing, but this perception may not be widely shared.
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Table 1 The ethical matrix as applied to the production of food from animals (Webster, 2011). Respect for
Beneficence (health and welfare)
Autonomy (freedom and choice)
Justice (fairness)
Farm animals Producers Consumers Living environment
Animal welfare Farmer welfare Safe wholesome food Conservation
Telos Choice of system Choice/labelling Biodiversity
Duty of care Fair trade and law Affordable food Sustainability of populations
Table 2 Stakeholder analysis and the four principles (an ethical framework common to human medicine).
System
Stocksman
Animal
Consumer
Autonomy
Beneficence
Non maleficence
Justice
Intensive systems: lessen choice – Extensive systems: enlarge choice Limited by system and knowledge
Provision of shelter, safety, food and water
Absence of harms
Fair in terms of return needed
Trained in husbandry
Obeying published codes
Limits to autonomy considerable as pay-back to advantages of domestication Choice of source of foods
Provision of essentials
Only performing interventions for which trained Only necessary mutilations performed
Ability to select for higher welfare standards through cost
Able to direct production through buying habits
Legal limits of husbandry defined and best practices promoted Aware of rights and of safe food production – Interest in sustainability
Table 3 Simple analysis of different husbandry systems using the five freedoms (after Webster, 2011). Factor
Hunger and thirst Comfort Disease and pain Stress Fear Natural behaviour
Production system Housed
In-bye
Extensive
Adequate Good Low risk biosecurity and hygiene Boredom; interactions necessary Low, provided empathetic stockspersons Restricted by pen size and numbers
Variable, but controlled Variable – Management important Low risk More interest Low Controlled
Variable Variable choice available Risk increased – Delayed detection Interest, but exposed to increased risks Low, but gathering likely to be very aversive Most natural for most breeds
Technologies progress and with improvement they may have a lesser impact on welfare. An example of this is the increasingly widespread use of ultrasonographic equipment for pregnancy diagnosis, which can be performed on standing ewe, reducing welfare costs for gathering and handling. Russel and Goddard (1995) reported on the widespread use of this technique and Scott (2007) has advocated its increased use in clinical diagnosis as well as for pregnancy detection. It is often useful to describe welfare impacts through the application of ethical framework analysis and the use of the common human clinical framework of ‘Autonomy’, ‘Beneficence’, ‘Non-maleficence’ and ‘Justice’ (i.e. the four principles approach) (Mepham, 2005) may be a helpful tool here (Table 1). Stakeholder analysis also aids in focussing welfare impacts and considers all contributors in a particular situation to help derive an answer to limits of procedure (Table 2). Table 3 shows how all contributors can focus on welfare impacts to try to derive an answer to procedural limits. 3. Concluding remarks At the same time as welfare is considered across the flock/herd, it must be remembered that the indicators developed to assess welfare are developed in a
relatively small number of animals and that it is likely that widespread individual variation between breeds and between individuals within those breeds exists. Hence, it is important that measures used are recognised with their limitations and not given absolute status. For the introduction of new techniques to the industry, the type of analysis described above can help to provide limits to the use or abuse of the technique. Equally important is a reflection on current practice and these analytical tools aid the revisiting of the ethical concerns raised in our manipulation of animal reproduction at the flock or individual animal level. The concern for the individual highlights a need to understand the relative importance to the animal of the varying parameters that are presently used to describe welfare attributes. Because of the difficulties involved in these assessments, we tend to apply the perceived wisdom across the species and perhaps fail to understand the important variations that any population of individuals possess; this further complicates our ability to assess welfare impact on the individual of any given procedure. Just as cost-benefit has been demonstrated not to be the driving priority behind the implementation and continuation of farm health plans, other drivers may be more important to small ruminants and, although perception would probably exclude benefits from team-work, it would
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recognise the cognitive ability of these animals to appreciate a more favourable welfare condition. Reproductive performance is a key part of successful small ruminant health management and must be supported by transparent standards promoting high welfare to maintain the green image of the industries. We need to provide more opportunity for sheep and goats to indicate prime strategies directed at moving welfare status from ‘a life worth living’ to ‘a good life’ and, at the same time, it must be acknowledged that no life is without challenge from stressors, such as fear and distress. Animal welfare is paramount to sustainable and productive systems; where we choose to place arbitrary controls on the continuum from very good welfare to very poor welfare remains an area in which legislation, education and continuing research need to provide clear universal guidance and delineation. Conflict of interest statement The author has no conflicts of interest to declare. References Abecia, J.A., Forcada, F., Gonzalez-Bulnes, A., 2011. Pharmaceutical control of reproduction in sheep and goats. Vet. Clin. N. Am. Food Anim. Pract. 27, 67–79. Agricultural and Environment Biotechnology Committee, 2002. Animals and Biotechnology. Department of Food and Rural Environment, London, 88 pp. Animal Welfare Act, 2006. http://www.legislation.gov.uk/ukpga/2006/ 45/contents. Banner Committee, 1995. Report of the Committee to Consider the Ethical Implications of Emerging Technologies in the Breeding of Farm Animals. Ministry of Agriculture, Fisheries and Food, London. Bovine Embryo (Collection, Production and Transfer) Regulations, 1995. http://www.legislation.gov.uk/uksi/1995/2478/contents. British Cattle Veterinary Association, 2010. http://www.bcva.eu/bcva/ content/welfare. Broom, D.M., 1996. Animal welfare defined in terms of attempts to cope with the environment. Acta Agric. Scand. 27, 22–28. Broom, D.M., 2007. Quality of life means welfare: how is it related to other concepts and assessed? Anim. Welf. 16S, 45–53. Dwyer, C.M., 2003. Behavioural development in the neonatal lamb: effect of maternal and birth-related factors. Theriogenology 59, 1027–1050. Dwyer, C.M., 2004. How has the risk of predation shaped the behavioural responses of sheep to fear and distress? Anim. Welf. 13, 269–281. Dwyer, C., 2008. The Welfare of Sheep. Springer, Berlin, 386 pp. European Forum of Farm Animal Breeders, 2000. EFABAR Code., http://www.effab.org. Eskebo, I., 2011. Farm Animal Behaviour. Characteristics for Assessment of Health and Welfare. CABI, Oxford, 248 pp.
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