Positive Welfare Indicators in Dairy Animals: Comparison
Please note this is a comparison between Version 2 by Panagiotis Simitzis and Version 1 by Panagiotis Simitzis.

Nowadays, there is growing interest in positive animal welfare not only from the view of scientists but also from that of society. The consumer demands more sustainable livestock production, and animal welfare is an essential part of sustainability, so there is interest in incorporating positive welfare indicators into welfare assessment schemes and legislation.

  • positive welfare indicator
  • cattle
  • sheep
  • goat
  • buffalo

1. Introduction

Positive animal welfare is not an innovative approach to animal welfare [1,2]. Nonetheless, it is a newer approach compared to the common welfare approach and attracts increasing attention. Welfare by definition includes positive aspects, but in animal welfare science, for decades, the focus had been mainly on alleviating poor welfare and not on promoting positive experiences [3]. Nowadays, the focus is moving gradually to also promoting positive experiences. Positive welfare focuses not only on the negative aspects of welfare, which should be alleviated and kept above a minimum standard [4,5], but also emphasizes the positive aspects of welfare that animals should be experiencing in their lives [4]. It is a topic that is gaining increasing interest not only from animal welfare scientists but also from the public, on both a national and international level since animal welfare is steadily incorporated in legislation, schemes, welfare assessment protocols, and the labelling of livestock products. Consumers demand sustainable production methods, and nowadays, animal welfare is considered an important component of sustainability [6,7]. It is not only that the consumer believes that it is ethically right to promote the enhanced welfare of livestock animals but also that animal welfare is an important part of sustainability and is becoming a necessary part of profitable livestock production that must follow the demands of the consumer [6].
Animal welfare has nowadays been recognized as a worldwide target of sustainable agricultural policy [8]. The United Nations Committee on World Food Security formally denoted animal welfare as a fundamental pillar of sustainable agricultural development, food security, and human nutrition together with the other classic domains, i.e., economics, society, and the environment [9]. At the same time, there is an increasing political modernization around the issue of animal welfare that is become apparent by the “One Health” or “One Welfare” concepts set by national non-governmental organizations (NGOs) and consumer groups [10,11]. More than 90% of EU citizens prioritize animal welfare, and more than half of them are ready to pay more for products derived from systems offering a high welfare status since they are considered healthier, safer, and more environmentally friendly [12].
Although animal welfare is increasingly viewed as a sustainable solution by the consumer, intensification in livestock species is still high. There is a growing demand for livestock products due to the rapid increase in the world population. Dairy animals, especially dairy cattle, are key species in animal husbandry. Milk production is rising globally, with cattle being responsible for 81% of world milk production [13]. According to FAOSTAT [14], since the 1960s, milk production has more than doubled in developing countries. World milk production is expected to increase by 1.7% over the next decade in almost all the regions of the world [15]. Millions of dairy animals are kept in various husbandry systems, mostly intensively. Can the welfare of these animals be composed of positive aspects so that they experience a good life, and if not, what changes should be made? To answer this question, the role of welfare science is crucial. Despite the debate between scientists, there is an intense need for incorporating gradually positive welfare indicators in welfare assessment schemes and legislation. It is the responsibility of all animal welfare scientists to communicate their knowledge in an understandable manner to all individuals in society [5], and animal welfare should be able to be incorporated into laws by focusing on the ethical part of welfare [16].

2. Positive Welfare Indicators

Twenty-four positive welfare indicators were retrieved, both behavioral and physiological, all animal based. They have been studied experimentally, on the farm level or proposed on a theoretical basis. The indicators, the dairy animals that they correspond to, and the literature findings are summarized in Table 1.
Table 1. Positive welfare indicators categorized by dairy animal.

3. Discussion

According to our findings, twenty-four indicators have been retrieved concerning the evaluation of positive welfare in dairy animals. All indicators have been studied in the field or under experimental conditions, apart from pro-social behaviors, proposed by Rault [34] and analyzed on a theoretical basis. They are all animal-based indicators, apart from access to pasture, which can be considered both as an animal-based and a resource-based indicator. Most of them are behavioral indicators and only two of them, nasal temperature and oxytocin, are physiological indicators. Most studies of positive welfare indicators have been applied on cattle, followed by sheep and goats, and finally buffaloes. The least studies have been performed on camels. The positive welfare indicators that presented the most results were pasture, exploration, lying/resting, play, and ear postures. All indicators that are included in welfare assessment protocols should be valid, meaning that they clearly indicate the impact on welfare between farms, in a reliable way, so that they provide consistent results (inter-, intra- and test–retest reliability) and feasible so that they can be applied in practice by the assessors easily and with limited training [164]. In addition, they should be examined regarding their cost, a determinant factor for their incorporation in welfare schemes. The indicators cited in our review are not analyzed regarding these factors, and many have been studied only theoretically or experimentally and not under farm conditions. Furthermore, there is a relationship between some indicators, but in general, the association between the indicators is not clear and more studies are necessary. Access to pasture is related to synchronization, comfort, exploration, [48,58,63,135,137] and wallowing in buffaloes [46] since it is linked to increased space and stimulation. However, the link between all other indicators is not yet clear and further research is warranted. Few indicators have been studied simultaneously to understand their connection. Mattiello et al. [23] have concluded that ear posture is a promising indicator in combination with eye white. On the other hand, visible eye white decreases in both negative and positive states of high arousal [101,105,107,151]. Ear and tail positions have also been studied a lot, and under the same experiments [92,98,101] but in different species and conditions. We can conclude that the results on positive welfare in dairy animals are scattered regarding the animal species, the husbandry conditions, the life stage of the animals, and even the experimental conditions. For these reasons, it is not possible to make proposals for key indicators, relation schemes, and incorporation in welfare assessment protocols. We can only make some conclusions and suggestions for the direction of future studies in the positive welfare indicators of dairy ruminants, as analyzed below in this section. Feeding, ruminating, comfort, lying, and resting behaviors have been proposed and studied on the farm level as positive welfare indicators for all dairy animals, and there is enough research to support their use (more research is necessary for camels). The animals also elicit high synchronicity when performing them, which is also a positive welfare indicator [29,30] [19,43]. It is easier to promote these behaviors at pasture, due to the increased allowance and the environmental stimulation, but they could be also promoted indoors by increasing space. Synchronicity is an indicator of enough space and resources for all animals that are raised both indoors and outdoors, especially the subordinated ones [27,63,81,82] [63,41,65,66]. A difficulty of incorporating some synchronized behaviors, such as lying behavior as proposed by Richmond et al. [82] [66] for the sheep in protocols, is that it may be lateralized at particular times of the day. Lying synchronicity is higher in cattle in the morning and the afternoon and so may be difficult to assess in practice [58,139] [36,125]. It should be highlighted that the promotion of exploration, play, comfort, lying, and resting is linked not only to space allowance but also to environmental complexity. Access to pasture is a type of environmental enrichment with stimulations for the ruminants [43]. Species-specific behaviors such as wallowing for buffaloes [61] should be taken into consideration and are promoted with access to pasture [46]. Exploration activity and play are also motivated by environmental stimulation [30] and have been studied a lot in cattle and small ruminants. Play may be considered a more appropriate behavior for juveniles since it decreases with age [32]. It also appears as a valid positive welfare indicator to judge if the energy intake of calves is adequate, after the first week after weaning [74,76]. It could be detected by accelerometers, making it an easily detected parameter [144,145], but this means a higher cost. In general, environmental enrichment and space allowance if not access to pasture are necessary and can be a simple start for promoting positive states,

especially in animals kept indoors. On the contrary, maternal care and mating behavior could not be easily assessed on the farm level since insemination takes place mostly artificially and offspring separation occurs soon in all livestock species. In dairy cattle specifically, the calf is reared group-housed, apart from its mother, separated just a few hours after birth. Promoting cow–calf bonding as a positive welfare indicator would mean reduced income for the farmer since the profit is higher when feeding the calf milk replacer [165]. Consumers are becoming concerned about cow–calf separation, although still, many are unaware of the practice. Some farmers in Germany and the UK have started keeping calves with their mothers, but the economic aspects of this husbandry system remain to be studied [165]. Social affiliative behaviors are also present in all dairy animals, although not studied enough in buffaloes and camels. Automatic brushes have positive results on cattle welfare and should be considered a promising way of promoting positive states [66,68,70,73] but in smaller husbandry systems may represent an expensive solution. Ear movements have also been studied a lot in cattle and small ruminants, but they are insufficient alone as emotional indicators. Still, they can be combined with other indicators and give a more holistic animal approach to positive welfare evaluation, and they are non-invasive, feasible, and easy to detect [92,94]. The same applies for vocalizations that can in addition be detected with microphones [39]. The nasal temperature also seems promising as a positive welfare indicator [105,118] but is a physical indicator that may be difficult to be applied in practice. Cognitive and attention bias and anticipatory tests could also be difficult to apply on a farm level since more time is required. The results show that QBA is a positive welfare indicator that is more often used for the on-farm assessment of positive emotions in dairy animals. It has been cited for cattle in the Welfare Quality protocol [40], and in the AWIN protocol for sheep [41] and goats [42]. QBA has also been studied on buffaloes [64,117] and has been proposed as a future study for camels [55]. Exploration, access to pasture, comfort, lying, resting, and synchronization are the most promising welfare indicators since they have been studied the most with results that agree but are not already used for the on-farm welfare assessment as much as QBA. A future research direction would be to try to also incorporate these indicators in schemes and protocols. It is also important to study the relationship between various positive indicators and combine them for a more holistic and valid approach of positive welfare evaluation. Especially indicators such as ear postures and social affiliative behaviors can be easily detected and combined with the above-mentioned indicators. In addition, there is a need for studies in different husbandry species of each dairy species. The positive welfare research that has been retrieved about camels and buffaloes is limited compared to other dairy animals. Furthermore, as far as our knowledge, there are no official welfare assessment protocols for these species Although the dairy industry of these animals is evolved, especially for camel husbandry, there is no official protocol for their welfare evaluation. Napolitano et al. [64] have proposed a protocol for buffaloes and in general the repertoire of these animals in various studies [87,141,166]. Regarding camels, an experimental protocol has only been studied by Padalino and Menchetti [55] and the regulations regarding legislation on camels are extremely limited [55,56]. Research on camels is generally limited, focusing mainly on food science and camel health, while research in management, nutrition, and welfare is scarce [25]. A direction for future studies could be to start examining potential positive welfare indicators such as exploration, synchronization, play, and ear postures that have already been studied for cattle and small

ruminants and then continue to species-specific behaviors. In order to promote positive welfare, we should undergo drastic changes in the husbandry systems of dairy animals regarding both management and handling procedures. The role of the consumer and public is crucial for these changes, since today animal welfare is driven more by the consumer than the regulations [3]. Animal welfare is considered and can be sustainable [6,7]. A positive welfare approach needs the support of consumers, farmers, and researchers [167]. Consumers are willing to pay more to buy animal products that focus on animal-based and not only resource-based measures, but the problem is that animal-based measures are more difficult to be communicated to the public [168]. Nonetheless, it is not easy to achieve the consumers’ willingness to pay for increased animal welfare in practice. The increase in public concern, in some cases, may not be enough to cover the increased price of the final product [169–172]. Other challenges can also be that the willingness to pay is influenced by various factors such as socio-demographic characteristics, gender, and educational level [169]. Still, in general, consumers are concerned about the animal welfare of food productions animal, and clean labelling and information can be a way of increasing the willingness to pay [169,172]. Furthermore, a collaborative approach to a positive welfare protocol between farmers and scientists is also important. Stokes et al. [173] developed a positive welfare assessment scheme for dairy cows based on the scientific literature, applied it on focus farms, consulted the farmers, received their feedback, refined the scheme according to farmers’ recommendations, and investigated the farmer’s attitude towards positive welfare. Farmers already valued positive indicators such as comfort and access to pasture, agreed with scientists on what could be promoted as positive aspects in the life of dairy cattle, and valued the life of their animals, supporting that they are linked to their wellbeing. They were willing to incorporate positive welfare aspects in the life of their animals, provided that they would receive adequate labeling and so business profit. Vigors and Lawrence [167] also support that positive welfare should be communicated and explained to farmers, since their concern is mostly for preventing the negatives and that, through this approach, positive experiences will arise naturally for their animals. They are willing to promote positive welfare, but they are concerned about whether their business will be economically sustainable. According to a meta-analysis by Clark et al. [171], the highest estimated consumers’ willingness to pay is for dairy and beef cattle, which is hopeful for the welfare of dairy cattle. Still, there are various challenges, as explained above. Positive welfare indicators should be incorporated in welfare assessment protocols, labeling schemes, and legislation, on a national and international level, to raise the level of welfare of all livestock species. This need is essential for all dairy animals, but especially for small ruminants, and mostly buffaloes and camels, since there is no official welfare assessment protocol for the welfare of these species. Particularly for camels, the research on welfare is limited, and on positive welfare, it is scarce.  
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