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Review: Assessing fish welfare in research and aquaculture, with a focus on European directives

  • M. Toni (a1), A. Manciocco (a2), E. Angiulli (a1), E. Alleva (a3), C. Cioni (a1) and S. Malavasi (a4)...


The number of farmed fish in the world has increased considerably. Aquaculture is a growing industry that will in the future provide a large portion of fishery products. Moreover, in recent years, the number of teleost fish used as animal models for scientific research in both biomedical and ecological fields has increased. Therefore, it is increasingly important to implement measures designed to enhance the welfare of these animals. Currently, a number of European rules exist as requirements for the establishment, care and accommodation of fish maintained for human purposes. As far as (teleost) fish are concerned, the fact that the number of extant species is much greater than that of all other vertebrates must be considered. Of further importance is that each species has its own specific physical and chemical requirements. These factors make it difficult to provide generalized recommendations or requirements for all fish species. An adequate knowledge is required of the physiology and ecology of each species bred. This paper integrates and discusses, in a single synthesis, the current issues related to fish welfare, considering that teleosts are target species for both aquaculture and experimental models in biological and biomedical research. We first focus on the practical aspects, which must be considered when assessing fish welfare in both research and aquaculture contexts. Next, we address husbandry and the care of fish housed in research laboratories and aquaculture facilities in relation to their physiological and behavioural requirements, as well as in reference to the suggestions provided by European regulations. Finally, to evaluate precisely which parameters described by Directive 2010/63/EU are reported in scientific papers, we analysed 82 articles published by European researchers in 2014 and 2015. This review found that there is a general lack of information related to the optimal environmental conditions that should be provided for the range of species covered by this directive.

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Ashley, PJ 2007. Fish welfare: current issues in aquaculture. Applied Animal Behaviour Science 104, 199235.
Avdesh, A, Chen, M, Martin-Iverson, MT, Mondal, L, Ong, D, Rainey-Smith, S, Taddei, K, Lardelli, M, Groth, DM, Verdile, G and Martins, RN 2012. Regular care and maintenance of a zebrafish (Danio rerio) laboratory: an introduction. Journal of Visualized experiments 69, e4196.
Baker, D, Lidster, K, Sottomayor, A and Amor, S 2014. Two years later: journals are not yet enforcing the ARRIVE guidelines on reporting standards for pre-clinical animal studies. PLoS Biology 12, e1001756.
Batzina, A and Karakatsouli, N 2014. Is it the blue gravel substrate or only its blue color that improves growth and reduces aggressive behavior of gilthead seabream Sparus aurata? Aquacultural Engineering 62, 4953.
Bégout Anras, ML and Lagardère, JP 2004. Measuring cultured fish swimming behaviour: first results on rainbow trout using acoustic telemetry in tanks. Aquaculture 240, 175186.
Boerrigter, JGJ, van den Bos, R, van de Vis, H, Spanings, T and Flik, G 2015. Effects of density, PVC-tubes and feeding time on growth, stress and aggression in African catfish (Clarias gariepinus). Aquaculture Research 47, 25532568.
Brown, C and Day, RL 2002. The future of stock enhancements: lessons for hatchery practice from conservation biology. Fish and Fisheries 3, 7994.
Brown, C 2015. Fish intelligence, sentience and ethics. Animal Cognition 18, 117.
Chrousos, GP and Gold, PW 1992. The concepts of stress and stress system disorders: overview of physical and behavioral homeostasis. Journal of the American Medical Association 267, 12441252.
Conte, FS 2004. Stress and the welfare of cultured fish. Applied Animal Behaviour Science 86, 205223.
Council of Europe 2006. Standing Committee of the European Convention for the Protection of Animals kept for farming purposes recommendation concerning farmed fish. Retrieved on 05 December 2017 from
Cressey, D 2016. Surge in support for animal-research guidelines. Nature, Published online by Nature International Weekly Journal of Science 01 February 2016.
Directive 2010/63/EU (2010) European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes. Text with EEA relevance. Retrieved on 05 December 2017 from
European Parliament Report 2013. Report from the Commission to the Council and the European Parliament. Sixth Report on the statistics on the number of animals used for experimental and other scientific purposes in the Member States of the European Union SEC (2010) 1107. Retrieved on 05 December 2017 from
Farm Animal Welfare Council 1992. FAWC updates the five freedoms. Veterinary Record 17, 357.
Giacomini, AC, Abreu, MS, Zanandrea, R, Saibt, N, Friedrich, MT, Koakoski, G, Gusso, D, Piato, AL and Barcellos, LJ 2016. Environmental and pharmacological manipulations blunt the stress response of zebrafish in a similar manner. Scientific Reports 6, 28986.
Hawkins, P, Morton, DB, Burman, O, Dennison, N, Honess, P, Jennings, M, Lane, S, Middleton, V, Roughan, JV, Wells, S and Westwood, K 2011. A guide to defining and implementing protocols for the welfare assessment of laboratory animals: eleventh report of the BVAAWF/FRAME/RSPCA/UFAW Joint Working Group on Refinement. Laboratory Animals 45, 113.
Howe, K, Clark, MD, Torroja, CF, Torrance, J, Berthelot, C, Muffato, M, Collins, JE, Humphray, S, McLaren, K, Matthews, L, McLaren, S, Sealy, I, Caccamo, M, Churcher, C, Scott, C, Barrett, JC, Koch, R, Rauch, GJ, White, S, Chow, W, Kilian, B, Quintais, LT, Guerra-Assunção, JA, Zhou, Y, Gu, Y, Yen, J, Vogel, JH, Eyre, T, Redmond, S, Banerjee, R, Chi, J, Fu, B, Langley, E, Maguire, SF, Laird, GK, Lloyd, D, Kenyon, E, Donaldson, S, Sehra, H, Almeida-King, J, Loveland, J, Trevanion, S, Jones, M, Quail, M, Willey, D, Hunt, A, Burton, J, Sims, S, McLay, K, Plumb, B, Davis, J, Clee, C, Oliver, K, Clark, R, Riddle, C, Elliot, D, Threadgold, G, Harden, G, Ware, D, Begum, S, Mortimore, B, Kerry, G, Heath, P, Phillimore, B, Tracey, A, Corby, N, Dunn, M, Johnson, C, Wood, J, Clark, S, Pelan, S, Griffiths, G, Smith, M, Glithero, R, Howden, P, Barker, N, Lloyd, C, Stevens, C, Harley, J, Holt, K, Panagiotidis, G, Lovell, J, Beasley, H, Henderson, C, Gordon, D, Auger, K, Wright, D, Collins, J, Raisen, C, Dyer, L, Leung, K, Robertson, L, Ambridge, K, Leongamornlert, D, McGuire, S, Gilderthorp, R, Griffiths, C, Manthravadi, D, Nichol, S, Barker, G, Whitehead, S, Kay, M, Brown, J, Murnane, C, Gray, E, Humphries, M, Sycamore, N, Barker, D, Saunders, D, Wallis, J, Babbage, A, Hammond, S, Mashreghi-Mohammadi, M, Barr, L, Martin, S, Wray, P, Ellington, A, Matthews, N, Ellwood, M, Woodmansey, R, Clark, G, Cooper, J, Tromans, A, Grafham, D, Skuce, C, Pandian, R, Andrews, R, Harrison, E, Kimberley, A, Garnett, J, Fosker, N, Hall, R, Garner, P, Kelly, D, Bird, C, Palmer, S, Gehring, I, Berger, A, Dooley, CM, Ersan-Ürün, Z, Eser, C, Geiger, H, Geisler, M, Karotki, L, Kirn, A, Konantz, J, Konantz, M, Oberländer, M, Rudolph-Geiger, S, Teucke, M, Lanz, C, Raddatz, G, Osoegawa, K, Zhu, B, Rapp, A, Widaa, S, Langford, C, Yang, F, Schuster, SC, Carter, NP, Harrow, J, Ning, Z, Herrero, J, Searle, SM, Enright, A, Geisler, R, Plasterk, RH, Lee, C, Westerfield, M, de Jong, PJ, Zon, LI, Postlethwait, JH, Nüsslein-Volhard, C, Hubbard, TJ, Roest Crollius, H, Rogers, J and Stemple, DL 2013. The zebrafish reference genome sequence and its relationship to the human genome. Nature 496, 498503.
Huntingford, FA, Adams, C, Braithwaite, V, Kadri, S, Pottinger, T, Sandøe, P and Turnbull, J 2006. Current issues in fish welfare. Journal of Fish Biology 68, 332372.
Hurley, IA, Mueller, RL, Dunn, KA, Schmidt, EJ, Friedman, M, Ho, RK, Prince, VE, Yang, Z, Thomas, MG and Coates, MI 2007. A new time-scale for ray-finned fish evolution. Proceedings of the Royal Society B: Biological Sciences 274, 489498.
Kikuta, H, Fredman, D, Rinkwitz, S, Lenhard, B and Becker, TS 2007. Retroviral enhancer detection insertions in zebrafish combined with comparative genomics reveal genomic regulatory blocks - a fundamental feature of vertebrate genomes. Genome Biology 8, S4.
Kilkenny, C, Browne, WJ, Cuthill, IC, Emerson, M and Altman, DG 2010. Improving bioscience research reporting: The ARRIVE guidelines for reporting animal research. Journal of Pharmacology and Pharmacotherapeutics 1, 9499.
Kristiansen, TS, Fernö, A, Holm, JC, Privitera, L, Bakke, S and Fosseidengen, JE 2004. Swimming behaviour as an indicator of low growth rate and impaired welfare in Atlantic halibut (Hippoglossus hippoglossus L.) reared at three stocking densities. Aquaculture 230, 137151.
Laursen, DC, Andersson, , Silva, PIM, Petersson, E and Höglund, E 2013. Utilising spatial distribution in two-tank systems to investigate the level of aversiveness to crowding in farmed rainbow trout Oncorhynchus mykiss . Applied Animal Behaviour Science 144, 163170.
Lefevre, F, Cos, I, Pottinger, TG and Bugeon, J 2016. Selection for stress responsiveness and slaughter stress affect flesh quality in pan-size rainbow trout, Oncorhynchus mykiss. Aquaculture 464, 654664.
López-Olmeda, JF, Noble, C and Sánchez-Vázquez, FJ 2012. Does feeding time affect fish welfare? Fish Physiology and Biochemistry 38, 143152.
Malavasi, S, Cipolato, G, Cioni, C, Torricelli, P, Alleva, E, Manciocco, A and Toni, M 2013. Effects of temperature on the antipredator behaviour and on the cholinergic expression in the European sea bass (Dicentrarchus labrax L.) juveniles. Ethology 119, 592604.
Malavasi, S, Georgalas, V and Torricelli, P 2009. Behavioural indicators of ‘wildness’ as useful tools for restocking: the European Sea Bass (Dicentrachus labrax L.) juvenile as study model. In Aquaculture research progress (ed. TK Nakamura), pp. 15. Nova Science Publishers, Hauppauge, NY, USA.
Manciocco, A, Calamandrei, G and Alleva, E 2014. Global warming and environmental contaminants in aquatic organisms: the need of the etho-toxicology approach. Chemosphere 100, 17.
Manciocco, A, Toni, M, Tedesco, A, Malavasi, S, Alleva, E and Cioni, C 2015. The acclimation of European Sea Bass (Dicentrarchus labrax) to temperature: behavioural and neurochemical responses. Ethology 121, 6883.
Mushtaq, MY, Verpoorte, R and Kim, HK 2013. Zebrafish as a model for systems biology. Biotechnology & Genetic Engineering Reviews 29, 187205.
Näslund, J and Johnsson, JI 2016. State-dependent behavior and alternative behavioral strategies in brown trout (Salmo trutta L.) fry. Behavioral Ecology and Sociobiology 70, 21112125.
Nuffield Council on Bioethics 2005. The ethics of research involving animals. Nuffield Council on Bioethics, London, UK. Retrieved on 05 December 2017 from
Poli, B, Parisi, G, Scappini, F and Zampacavallo, G 2005. Fish welfare and quality as affected by pre-slaughter and slaughter management. Aquaculture International 13, 2949.
Pounder, KC, Mitchell, JL, Thomson, JS, Pottinger, TG, Buckley, J and Sneddon, LU 2016. Does environmental enrichment promote recovery from stress in rainbow trout? Applied Animal Behaviour Science 176, 136142.
Reinhardt, V 2004. Common husbandry-related variables in biomedical research with animals. Laboratory Animals 38, 213235.
Rodewald, P, Hyvärinen, P and Hirvonen, H 2011. Wild origin and enriched environment promote foraging rate and learning to forage on natural prey of captive reared Atlantic salmon parr. Ecology of Freshwater Fish 20, 569579.
Russell, WMS and Burch, RL 1959/1992. The principles of humane experimental technique. Universities Federation for Animal Welfare, Wheathampstead, UK.
Salvanes, AG, Moberg, O, Ebbesson, LO, Nilsen, TO, Jensen, KH and Braithwaite, VA 2013. Environmental enrichment promotes neural plasticity and cognitive ability in fish. Proceedings of the Royal Society B: Biological Sciences 280, 20131331.
Schartl, M 2014. Beyond the zebrafish: diverse fish species for modeling human disease. Disease Models & Mechanisms 7, 181192.
Simpson, J and Kelly, JP 2011. The impact of environmental enrichment in laboratory rats-behavioural and neurochemical aspects. Behavioural Brain Research 222, 246264.
Slavík, O, Maciak, M and Horký, P 2012. Shelter use of familiar and unfamiliar groups of juvenile European catfish Silurus glanis . Applied Animal Behaviour Science 142, 116123.
Toms, CN, Echevarria, DJ and Jouandot, DJ 2010. A methodological review of personality-related studies in fish: focus on the shy-bold axis of behavior. International Journal of Comparative Psychology 23, 125.
Toni, M, Angiulli, E, Malavasi, S, Alleva, E and Cioni, C 2017. Variation in environmental parameters in research and aquaculture: effects on behaviour, physiology and cell biology of teleost fish. Journal of Aquaculture & Marine Biology 5, 00137.
Uglem, I, Kjørsvik, E, Gruven, K and Lamberg, A 2009. Behavioural variation in cultivated juvenile Atlantic cod (Gadus morhua L.) in relation to stocking density and size disparity. Applied Animal Behaviour Science 17, 201209.
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