Journal of Animal Research and Nutrition

Animal Welfare Science began to gradually develop in the 60 ´s, probably as a consequence of the publication of the book “Animal Machines” by Ruth Harrison [1], which denounced several practices that were done without regard for animal suffering. Since then, much research has been conducted aiming to identify the welfare states of animals. Firstly, an animal was considered to have good welfare when it was physically healthy, feeding, and producing well. Everyone can easily understand the importance of these characteristics and believe they may be part of animal welfare considerations, but welfare may not be restricted to this. How the animal behaves may also indicate if it is in a better or a worse condition. Thus, a healthy and productive animal or even an animal that is feeding well may be in a poor welfare condition if it is, for example, expressing some stereotypic behaviour. Stereotypies are defined as a series of movements regularly repeated with no apparent purpose or goal [2], probably induced by frustration, repeated attempts to cope and/or brain dysfunction [3].

However, we should consider that even an animal behaving “naturally” does not necessarily have good welfare, and that the opposite may also be true [4]. For example, an animal fleeing from a predator is behaving naturally, but it should not be considered to have good welfare in that moment. Moreover, how can we be sure that some behaviours are natural and others are unnatural, stereotypic or otherwise abnormal? How can we be sure that an animal expressing some abnormal behaviour is in a worse situation than an animal not expressing it? If we consider that the expression of an abnormal behaviour could be a coping strategy used to deal with the restrictions of the captivity [5], and that an animal not expressing it could be in such an intense state of frustration or depression that it is simply unable to do so, we will not likely be sure of our answers. Similarly, according to Hill & Broom [6], natural behaviours should not necessarily be expected in environments that are more restricted than natural ones as captivity. Moreover, some studies contested stereotypies as unequivocal indicators of poor welfare conditions (e.g. De Passillé et al. [7]).

Furthermore, some aspects of animal welfare are difficult to measure: emotional states, including positive internal states such as pleasure and negative internal states such as fear or pain. There are many papers demonstrating that different animal species are able to feel pain, including fish species (for a review about pain in fish, see Braithwaite & Huntingford, [8]), and other papers indicating that animals are often afraid of handling and human beings [9,10]. Such negative emotional states are detrimental to animal welfare, but, as I mentioned above, the emotional component of animal welfare is not restricted to unpleasant feelings. The absence of pain and any another kind of suffering is not an indicator per se that the animal is in a good welfare state. The animal may not be suffering in any way, but it might not be experiencing any pleasure either. Does this mean that the animal is in a good welfare condition? Moreover, what do we know about the pleasure animals feel, for example, when interacting with a resource they are highly motivated to reach? Much more research is necessary to identify positive emotions in animals.

Thus, identifying animal welfare indicators that are unequivocal has not been an easy task. Considering these issues, Marian Dawkins [11,12] has proposed that we should turn our attention to what the animal wants instead of looking for such welfare indicators. In this context, Volpato et al. [13] has defined good welfare as the internal state of an animal when it is in a situation that it freely chose. Dawkins [12] has extended this idea, by defining good animal welfare as a condition in which the animal is healthy and has what it wants. Thus, many papers have focused on evaluating the animal’s preferences through choice tests, where two (binary tests) or more (multiple-choice tests) options are available for the animal to choose. Considering this approach, much progress has been made. The researchers have identified the preferences of many animal species for different environmental resources, such as sucrose [14], habitats [15], sexual partners [16-19], temperature [20] and many other resources.

In addition to this idea, Duncan [21] recommended identifying not only preferred and non-preferred conditions, but also the intensity of the responses. Thus, many papers have evaluated the intensity of the animals’ motivation to access environmental resources, and some progress has also been made towards this goal. The studies have evaluated the animal motivation for different resources, such as contact with conspecifics [22]; additional space [23]; dust-baths [24]; motivation to reach many different items [25] and even to express a stereotypic behaviour [26] (e.g. Duncan and Kite, 1987 [27]) or the number of times that a pre-conditioned behaviour (such as push a switch; e.g. sherwin, [23]) needs to be repeated to access a specific resource. In these tests, fodd is usually used as a benchmark to compare the motivation of the animals to reach other resources, since it is considered the resource the animal is most motivated to access. 

Although these approaches seem to be promising, some caution is necessary to apply and interpret preference and motivation tests. For instance, an animal may choose an available option because of a bias of the test apparatus or of the surrounding environment, or even because it was distracted by something (for review, see Volpato et al. [13]). In addition, the animals may choose what is good at the moment, but not necessarily what will be good for welfare in the long-term. Considering the motivation tests, Hovland et al. [28] has demonstrated that the food resource, usually used as a benchmark, may even elicit an aversion response if it is made available in excess. Thus, using food as a parameter to compare the animal motivation to reach other resources is an approach that also needs caution. Furthermore, basically most preference and motivation studies are concentrated on farm and lab animals. Considering that zoo and other captive animals may also suffer from poor welfare conditions, it is also relevant to evaluate their preferences and motivation for the resources. When applying environmental enrichment, which is a technique widely used to improve the welfare conditions of zoo animals, why not give the animals what they prefer or are very motivated to have? Thus, although preference and motivation tests are promising in improving the welfare conditions of the animals, some caution is needed and we still have a long way to go.

Acknowledgments

I thank Dr. Rebecca Meagher for her great help with the English edition of the manuscript.

References

1. Harrison R (1964) Animal Machines: The new factory farming industry. Vincent Stuart Publishers, London. p: 186.
2. Dantzer R, Mormed P (1983) The arousal properties of stereotypical behavior. Applied Animal Ethology 10: 233-44.
3. Mason G (2006) Stereotypic behaviour in captive animals: fundamentals and implications for welfare and beyond. In: Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare. (2ndedn) Wallingford: CAB International, pp: 325-356.
4. Volpato GL, Giaquinto PC, Castilho MF, Barreto RE, Freitas EG (2009) Animal welfare: from concepts to reality. Oecologia Brasiliensis 13: 5-15.
5. Swaisgood RR, Shepherdson DJ (2005) Scientific approaches to enrichment and stereotypies in zoo animals: what’s been done and where should we go next? Zoo Biology 24: 499-518.
6. Hill SP, Broom DM (2009) Measuring zoo animal welfare: theory and practice. Zoo Biology 28: 531-544.
7. De Passilé AMB, Christopherson, R, Rushen J (1993) Non-nutritive sucking by the calf and postprandial secretion of insulin, CCK and gastrin. Physiol Behav 54: 1069-1073.
8. Braithwaite VA, Huntingford FA (2004) Fish and welfare: do fish have the capacity for pain perception and suffering? Animal Welfare 13: S87-S92.
9. Hemsworth PH, Brand, A, Willems P (1981) The behavioral response of sows to the presence of human beings and relation to productivity. Livestock Production Science 8: 67-74.
10. Grandin, T, Shivley C (2015) How animals react and perceive stressful situations such as handling, restraint, and transport. Animals 5(4): 1233-1251.
11. Dawkins MS (2006) Through animal eyes: what behaviour tell us. Applied Animal Behaviour Science 100: 4-10.
12. Dawkins MS (2008) The science of animal suffering. Ethology 114: 937-945.
13. Volpato GL, Freitas EG, Castilho MF (2007) Insights into the concept of fish welfare. Diseases of Aquatic Organisms 75: 165-171.
14. Bartoshuk LM, Harned MA, Parks LA (1971) Taste of water in the cat: effects of sucrose preference. Science 171: 699-701.
15. Johnsson JI, Carlsson, M, Sundstrom LF (2000) Habitat preference increases territorial defence in brown trout (Salmo trutta). Behavioral Ecology and Sociobiology 48: 373-377.
16. Ryan MJ (1980) Female mate choice in a neotropical frog. Science 209: 523-525.
17. Basolo AL (1990) Female preference predates the evolution of the sword in swordtail fish. Science 250: 808-810.
18. Braithwaite VA, Barber I (2000) Limitations to colour-based sexual preferences in threespined sticklebacks (Gasterosteus aculeatus). Behavioral Ecology and Sociobiology 47: 413-416.
19. Branch CL, Kozlovsky DY, Pravosudov VV (2015) Elevation-related differences in female mate preference in mountain chickadees: are smart chickadees choosier? Animal Behaviour 99: 89-94.
20. Girguis PR, Lee RW (2006) Thermal preference and tolerance of alvinellids. Science 312: 231.
21. Duncan IJH (2006) The changing concept of animal sentience. Applied Animal Behaviour Science 100: 11-19.
22. Matthews LR, Ladewig J (1994) Environmental requirements of pigs measured by behavioral demand-functions. Animal Behaviour 47: 713-719.
23. Sherwin CM (2004) The motivation of group-housed laboratory mice Mus musculus foradditional space. Animal Behaviour 67: 711-717.
24. Colson, S, Arnold, C, Michel V (2007) Motivation to dust-bathe of laying hens in cages and in aviaries. Animal 1: 433-437.
25. Mason GJ, Cooper, J, Clarebrough C (2001) Frustrations of fur-farmed mink. Nature 410: 35-36.
26. Houpt KA (2012) Motivation for cribbing by horses. Animal Welfare 21: 1-7.
27. Duncan IJH, Kite VG (1987) Some investigations into motivation in the domestic fowl. Applied Animal Behaviour Science 18: 387-388.
28. Hovland AL, Mason G, Ahlstrøm Ø, Bakken M (2007) Responses of farmed silver foxes (Vulpes vulpes) to excessive food availability: Implications for using food as a yardstick resource in motivation tests. Applied Animal Behaviour Science 108: 170-178.