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A review of factors affecting the welfare of Atlantic salmon (Salmo salar)

Published online by Cambridge University Press:  01 January 2023

E Santurtun
Affiliation:
Centre for Animal Welfare and Ethics, School of Veterinary Science, University of Queensland, Gatton 4343, Queensland, Australia The Donkey Sanctuary-UNAM Programme, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de México, Mexico
DM Broom
Affiliation:
Centre for Animal Welfare and Anthrozoology, Department of Veterinary Medicine, University of Cambridge, Madingley Road, Cambridge CB3 0ES, UK
CJC Phillips*
Affiliation:
Centre for Animal Welfare and Ethics, School of Veterinary Science, University of Queensland, Gatton 4343, Queensland, Australia
*
Contact for correspondence and requests for reprints: c.phillips@uq.edu.au

Abstract

In the expanding salmon industry, many farmers use production methods that could result in poor welfare of the fish at various points of their lifecycle. We have reviewed methods used for producing salmon for food with the aim of identifying and drawing attention to factors likely to affect farmed Atlantic salmon (Salmo salar) welfare. In addition to water conditions and high stocking density at sea, other issues are important for fish welfare. Handling and transport of salmon between fresh- and seawater phases and before slaughter can have severe negative effects and research should continue to seek improved methods. Stocking densities in fresh- or seawater have substantial effects on the welfare of salmon and a reduction in densities should be considered in order to reduce fin damage in particular. Currently used feeding systems result in starvation for some fish and fin damage for others, hence new systems should be developed. Some on-demand feeding systems improve welfare. All farmed fish should be stunned prior to slaughter, not left to die of asphyxia. Carbon dioxide and electrical stunning methods do not always stun salmon humanely. The widely used methods of percussive stunning, manual or automatic, must be precise to effectively stun large numbers of fish. Welfare outcome indicators, such as fin damage, morbidity and mortality rate, should be used in standards and laws relating to salmon welfare.

Type
Articles
Copyright
© 2018 Universities Federation for Animal Welfare

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References

Aarseth, KAV, Perez, J, Boe, K and Jeksrud, WK 2006 Reliable pneumatic conveying of fish feed. Aquacultural Engineering 35: 1425. https://doi.org/10.1016/j.aquaeng.2005.06.006CrossRefGoogle Scholar
Aas, TS, Oehme, M, Sørensen, M, He, G, Lygren, I and Åsgård, T 2011 Analysis of pellet degradation of extruded high energy fish feeds with different physical qualities in a pneumatic feeding system. Aquacultural Engineering 44: 2534. https://doi.org/10.1016/j.aquaeng.2010.11.002CrossRefGoogle Scholar
Ackerman, PA, Wicks, BJ, Iwama, GK and Randall, DJ 2006 Low levels of environmental ammonia increase susceptibility to disease in Chinook salmon smolts. Physiological and Biochemical Zoology 79: 695707. https://doi.org/10.1086/504615Google ScholarPubMed
Adams, C, Huntingford, F, Turnbull, J, Arnott, S and Bell, A 2000 Size heterogeneity can reduce aggression and promote growth in Atlantic salmon parr. Aquaculture International 8: 543549. https://doi.org/10.1023/A:1009255612529CrossRefGoogle Scholar
Adams, CE, Turnbull, JF, Bell, A, Bron, JE and Huntingford, FA 2007 Multiple determinants of welfare in farmed fish: Stocking density, disturbance, and aggression in Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences 64: 336344. https://doi.org/10.1139/f07-018CrossRefGoogle Scholar
Agetsuma, M, Aizawa, H, Aoki, T, Nakayama, R, Takahoko, M, Goto, M, Sassa, T, Amo, R, Shiraki, T, Kawakami, K, Hosoya, T, Higashijima, S-I and Okamoto, H 2010 The habe-nula is crucial for experience-dependent modification of fear responses in zebrafish. Nature Neuroscience 13: 13541356. https://doi.org/10.1038/nn.2654Google ScholarPubMed
Alfredsen, JA, Holand, B, Solvang-Garten, T and Uglem, I 2007 Feeding activity and opercular pressure transients in Atlantic salmon (Salmo salar L): application to feeding management in fish farming. Hydrobiologia 195: 199207. https://doi.org/10.1007/s10750-006-0554-9Google Scholar
Alver, MO, Alfredsen, JA and Sigholt, T 2004 Dynamic mod-elling of pellet distribution in Atlantic salmon (Salmo salar L) cages. Aquacultural Engineering 31: 5172. https://doi.org/10.1016/j.aquaeng.2004.01.002Google Scholar
Barton, BA 2000 Salmonid fishes differ in their cortisol and glu-cose responses to handling and transport stress. North American Journal of Aquaculture 62: 1218. https://doi.org/10.1577/1548-8454(2000)062<0012:SFDITC>2.0.CO;22.0.CO;2>CrossRefGoogle Scholar
Bjørlykke, GA, Kvamme, BO, Raae, AJ, Roth, B and Slinde, E 2013 Slaughter of Atlantic salmon (Salmo salar L) in the pres-ence of carbon monoxide. Fish Physiology and Biochemistry 39: 871879. https://doi.org/10.1007/s10695-012-9747-5CrossRefGoogle Scholar
Bjørlykke, GA, Roth, B, Sørheim, O, Kvamme, BO and Slinde, E 2011 The effects of carbon monoxide on Atlantic salmon (Salmo salar L). Food Chemistry 127: 17061711. https://doi.org/10.1016/j.foodchem.2011.02.045CrossRefGoogle Scholar
Brackley, R, Bean, C, Lucas, M, Thomas, R and Adams, C 2016 Assessment of scale-loss to Atlantic salmon (Salmo salar L) smolts from passage through an Archimedean screw turbine. In: Webb, JA, Costelloe, JF, Casas Mulet, R and Lyon, JP (eds) 11th International Symposium on Ecohydraulics. 7-12 February 2016, Melbourne School of Engineering, University of Melbourne, AustraliaGoogle Scholar
Braithwaite, V 2010 Do Fish Feel Pain? Oxford University Press: Oxford, UKGoogle Scholar
Broom, DM 1999 Fish welfare and the public perception of farmed fish. Proceedings of Aquavision 98, Second Nutreco Aquaculture Business Conference pp 16. May 1998, Stavanger, NorwayGoogle Scholar
Broom, DM 2007 Cognitive ability and sentience: which aquat-ic animals should be protected? Diseases of Aquatic Organisms 75:99108. https://doi.org/10.3354/dao075099Google ScholarPubMed
Broom, DM 2014 Sentience and Animal Welfare. CABI: Wallingford, UK. https://doi.org/10.1079/9781780644035.0000CrossRefGoogle Scholar
Broom, DM 2016 Fish brains and behaviour indicate capacity for feeling pain. Animal Sentience 2016.010 (5 pages). https://www.neu-roscience.cam.ac.uk/publications/download.php?id=39835Google Scholar
Broom, DM and Fraser, AF 2015 Domestic Animal Behaviour and Welfare, Fifth Edition. CABI: Wallingford, UK. https://doi.org/10.1079/9781780645391.0000Google Scholar
Buckland-Nicks, JA, Gillis, M and Reimchen, TE 2012 Neural network detected in a presumed vestigial trait: ultra-structure of the salmonid adipose fin. Proceedings of the Royal Society B-Biological Sciences 279: 553563. https://doi.org/10.1098/rspb.2011.1009Google Scholar
Burridge, LJ, Weis, S, Cabello, F, Pizarro, J and Bostick, K 2010 Chemical use in salmon aquaculture: A review of current practices and possible environmental effects. Aquaculture 306: 723. https://doi.org/10.1016/j.aquaculture.2010.05.020CrossRefGoogle Scholar
Cañon Jones, HA, Hansen, LA, Noble, C, Damsgård, B, Broom, DM and Pearce, GP 2010 Social network analysis of behavioural interactions influencing fin damage development in Atlantic salmon (Salmo salar) during feed-restriction. Applied Animal Behaviour Science 127: 139151CrossRefGoogle Scholar
Cañon Jones, HA, Noble, C, Damsgård, B and Pearce, GP 2011 Social network analysis of the behavioural interactions that influence the development of fin damage in Atlantic salmon parr (Salmo salar) held at different stocking densities. Applied Animal Behaviour Science 133: 117126CrossRefGoogle Scholar
Cañon Jones, HA, Noble, C, Damsgård, B and Pearce, GP 2012 Investigating the influence of predictable and unpredictable feed delivery schedules upon the behaviour and welfare of Atlantic salmon parr (Salmo salar) using social network analysis and fin damage. Applied Animal Behaviour Science 138: 132140CrossRefGoogle Scholar
Chandroo, KP, Duncan, IJH and Moccia, RD 2004 Can fish suffer? Perspectives on sentience, pain, fear and stress. Applied Animal Behaviour Science 86: 225250. https://doi.org/10.1016/j.applanim.2004.02.004CrossRefGoogle Scholar
Einen, O, Waagan, B and Thomassen, MS 1998 Starvation prior to slaughter in Atlantic salmon (Salmo salar): 1. Effects on weight loss body shape slaughter- and fillet-yield proximate and fatty acid composition. Aquaculture 166: 85104. https://doi.org/10.1016/S0044-8486(98)00279-8Google Scholar
Ellis, T, North, B, Scott, AP, Bromage, NR, Porter, M and Gadd, D 2002 The relationships between stocking density and welfare in farmed rainbow trout. Journal of Fish Biology 61: 493531. https://doi.org/10.1111/j.1095-8649.2002.tb00893.xCrossRefGoogle Scholar
Ellis, T, Oidtmann, B, St-Hilaire, S, Turnbull, J, North, B, MacIntyre, C, Nikolaidis, J, Hoyle, I, Kestin, S and Knowles, T 2008 Fin erosion in farmed fish. In: Branson, E (ed) Fish Welfare pp 121149. John Wiley and Sons: Chichester, UK. https://doi.org/10.1002/9780470697610.ch9Google Scholar
Erikson, U, Hultmann, L and Erik Steen, J 2006 Live chilling of Atlantic salmon (Salmo salar) combined with mild carbon diox-ide anaesthesia: I Establishing a method for large-scale processing of farmed fish. Aquaculture 252: 183198. https://doi.org/10.1016/j.aquaculture.2005.05.013Google Scholar
Erikson, U, Sigholt, T and Seland, A 1997 Handling stress and water quality during live transportation and slaughter of Atlantic salmon (Salmo salar). Aquaculture 149: 243252. https://doi.org/10.1016/S0044-8486(96)01453-6Google Scholar
European Food Safety Authority (EFSA) 2007 Animal wel-fare aspects of husbandry systems for farmed fish in relation to Atlantic salmon. EFSA Journal: 124Google Scholar
European Food Safety Authority (EFSA) 2008 Animal wel-fare aspects of husbandry systems for farmed Atlantic salmon. Scientific Opinion of the Panel on Animal Health and Welfare.(Question No EFSA-Q-2006-033). http://www.efsa.europe.eu/en/efsajournal/pub/736Google Scholar
European Food Safety Authority (EFSA) 2009 Species-spe-cific welfare aspects of the main systems of stunning and killing of farmed Atlantic salmon. http://efsa.onlinelibrary.wiley.com/hub/issue/10.1002/efs2.2009.7.issue-4/Google Scholar
Farm Animal Welfare Council (FAWC) 2014a Opinion on the Welfare of Farmed Fish at the Time of Killing. http://www defra gov uk/fawc/files/Opinion-on-the-welfare-of-farmed-fish-at-the-time-of-killing pdfGoogle Scholar
Finstad, B, Iversen, M and Sandodden, R 2003 Stress-reducing methods for releases of Atlantic salmon (Salmo salar) smolts in Norway. Aquaculture 222: 203214. https://doi.org/10.1016/S0044-8486(03)00112-1CrossRefGoogle Scholar
Food and Agriculture Organisation (FAO) 2014 Food and Agriculture Organization of the United Nations Fisheries and Aquaculture Department Statistics. http://www fao org/fishery/statistics/enGoogle Scholar
Føre, MJ, Alfredsen, A and Gronningsater, A 2011 Development of two telemetry-based systems for monitoring the feeding behaviour of Atlantic salmon (Salmo salar L) in aquaculture sea-cages. Computers and Electronics in Agriculture 76: 240251. https://doi.org/10.1016/j.compag.2011.02.003Google Scholar
Foss, A, Grimsbo, E, Vikingstad, R and Nortvedt, R 2012 Live chilling of Atlantic salmon: physiological response to handling and temperature decrease on welfare. Fish Physiology and Biochemistry 38: 565571. https://doi.org/10.1007/s10695-011-9536-6Google ScholarPubMed
Gatica, MC, Monti, GE, Knowles, TG, Warriss, PD and Gallo, CB 2010 Effects of commercial live transportation and preslaughter handling of Atlantic salmon on blood constituents. Archivos De Medicina Veterinaria 42: 7378. https://doi.org/10.4067/S0301-732X2010000100010Google Scholar
Grimsrud, KM, Nielsen, HM, Navrud, S and Olesen, I 2013 Households’ willingness-to-pay for improved fish welfare in breeding programs for farmed Atlantic salmon. Aquaculture 372:1927. https://doi.org/10.1016/j.aquaculture.2012.10.009CrossRefGoogle Scholar
Hammenstig, D, Sandblom, E, Axelsson, M and Johnsson, JL 2014 Effects of rearing density and dietary fat content on burst-swim performance and oxygen transport capacity in juvenile Atlantic salmon Salmo salar. Journal of Fish Biology 85: 11771191. https://doi.org/10.1111/jfb.12511CrossRefGoogle ScholarPubMed
Handeland, SO, Imsland, AK, Ebbesson, LOE, Nilsen, TO, Hosfeld, CD, Baeverfjord, G, Espmark, A, Rosten, T, Skilbrei, OT, Hansen, T, Gunnarsson, GS, Breck, O and Stefansson, SO 2013 Low light intensity can reduce Atlantic salmon smolt quality. Aquaculture 384: 1924. https://doi.org/10.1016/j.aquaculture.2012.12.016CrossRefGoogle Scholar
Handeland, SO, Imsland, AK and Stefansson, SO 2008 The effect of temperature and fish size on growth, feed intake, food conversion efficiency and stomach evacuation rate of Atlantic salmon post-smolts. Aquaculture 283: 3642. https://doi.org/10.1016/j.aquaculture.2008.06.042Google Scholar
Hosfeld, CD, Hammer, J, Handeland, SO, Fivelstad, S and Stefansson, SO 2009 Effects of fish density on growth and smoltification in intensive production of Atlantic salmon (Salmo salar L). Aquaculture 294: 236241. https://doi.org/10.1016/j.aqua-culture.2009.06.003Google Scholar
Humane Slaughter Association (HSA) 2005 Humane har-vesting of salmon and trout. Guidance notes No 5. HSA: Wheathampstead, Herts, UKGoogle Scholar
Huntingford, FA and Kadri, S 2014 Defining, assessing and pro-moting the welfare of farmed fish. Revue Scientifique et Technique -Office International des Epizooties 33: 233244. https://doi.org/10.20506/rst.33.1.2286Google Scholar
Iversen, M, Finstad, B, McKinley, RS, Eliassen, RA, Carlsen, KT and Evjen, T 2005 Stress responses in Atlantic salmon (Salmo salar L) smolts during commercial well boat transports, and effects on survival after transfer to sea. Aquaculture 243: 373382. https://doi.org/10.1016/j.aquaculture.2004.10.019CrossRefGoogle Scholar
Iversen, M, Finstad, B and Nilssen, KJ 1998 Recovery from loading and transport stress in Atlantic salmon (Salmo salar L) smolts. Aquaculture 168: 387394. https://doi.org/10.1016/S0044-8486(98)00364-0CrossRefGoogle Scholar
Iversen, MH and Eliassen, RA 2009 The effect of AQUI-S-® on primary, secondary and tertiary stress responses during salmon smolt, Salmo salar L, transport and transfer to sea. Journal of the World Aquaculture Society 40: 216225. https://doi.org/10.1111/j.1749-7345.2009.00244.xGoogle Scholar
Jørgensen, EH, Baardvik, BM, Eliassen, R and Jobling, M 1996 Food acquisition and growth of juvenile Atlantic salmon (Salmo salar) in relation to spatial distribution of food. Aquaculture 143: 277289. https://doi.org/10.1016/0044-8486(96)01287-2CrossRefGoogle Scholar
Kadri, S, Huntingford, FA, Metcalfe, NB and Thorpe, JE 1996 Social interactions and the distribution of food among one-sea-winter Atlantic salmon (Salmo salar) in a sea-cage. Aquaculture 139: 110. https://doi.org/10.1016/0044-8486(95)01163-3CrossRefGoogle Scholar
King, HR 2009 Fish transport in the aquaculture sector: An overview of the road transport of Atlantic salmon in Tasmania. Journal of Veterinary Behavior: Clinical Applications and Research 4:163168. https://doi.org/10.1016/j.jveb.2008.09.034CrossRefGoogle Scholar
Kjartansson, H, Fivelstad, S, Thomassen, JM and Smith, MJ 1988 Effects of different stocking densities on physiological-parameters and growth of adult Atlantic salmon (Salmo salar) reared in circular tanks. Aquaculture 73: 261274. https://doi.org/10.1016/0044-8486(88)90060-9Google Scholar
Kleingeld, DW 2013 Aspects of animal welfare protection at stun-ning and slaughter procedures of fish. Fleischwirtschaft 93: 188192Google Scholar
Kolarevic, J, Baeverfjord, G, Takle, H, Ytteborg, E, Reiten, BKM, Nergard, S and Terjesen, BF 2014 Performance and welfare of Atlantic salmon smolt reared in recirculating or flow through aquaculture systems. Aquaculture 432: 1525. https://doi.org/10.1016/j.aquaculture.2014.03.033CrossRefGoogle Scholar
Kristensen, T, Urke, HA, Poppe, TT and Takle, H 2012 Atrial natriuretic peptide levels and heart morphology in migrating Atlantic salmon (Salmo salar) smolts from 4 rivers with different environmental conditions. Aquaculture 362: 172176. https://doi.org/10.1016/j.aquaculture.2011.08.003CrossRefGoogle Scholar
Krogdahl, Å and Bakke-McKellep, MA 2005 Fasting and refeeding cause rapid changes in intestinal tissue mass and digestive enzyme capacities of Atlantic salmon (Salmo salar L). Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 141: 450460. https://doi.org/10.1016/j.cbpb.2005.06.002Google Scholar
Lines, JA and Spence, J 2012 Safeguarding the welfare of farmed fish at harvest. Fish Physiology and Biochemistry 38: 153162. https://doi.org/10.1007/s10695-011-9561-5CrossRefGoogle ScholarPubMed
Lines, JA and Spence, J 2014 Humane harvesting and slaughter of farmed fish. Revue Scientifique et Technique de Office Internationale Epizootie 33: 255264. https://doi.org/10.20506/rst.33.1.2284Google ScholarPubMed
Liu, B, Liu, Y and Wang, X 2015 The effect of stocking density on growth and seven physiological parameters with assessment of their potential as stress response indicators for the Atlantic salmon (Salmo salar). Marine and Freshwater Behaviour and Physiology 48: 177192. https://doi.org/10.1080/10236244.2015.1034956CrossRefGoogle Scholar
Lopez-Olmeda, JF, Noble, C and Sanchez-Vazquez, FJ 2012 Does feeding time affect fish welfare? Fish Physiology and Biochemistry 38: 143152. https://doi.org/10.1007/s10695-011-9523-yCrossRefGoogle ScholarPubMed
Martinez-Espineira, R, Chopin, T, Robinson, S, Noce, A, Knowler, D and Yip, W 2015 Estimating the biomitigation ben-efits of Integrated Multi-Trophic Aquaculture: A contingent behavior analysis. Aquaculture 437: 182194. https://doi.org/10.1016/j.aquaculture.2014.11.034CrossRefGoogle Scholar
Martins, CIM, Eding, EH, Verdegem, MCJ, Heinsbroek, LTN, Schneider, O, Blancheton, JP, Roque d’Orbcastel, E and Verreth, JAJ 2010 New developments in recirculating aqua-culture systems in Europe: A perspective on environmental sus-tainability. Aquacultural Engineering 43: 8393. https://doi.org/10.1016/j.aquaeng.2010.09.002CrossRefGoogle Scholar
Maule, AG and Schreck, CB 1991 Stress and cortisol treatment changed affinity and number of glucocorticoid receptors in leukocytes and gill of coho salmon. General and Comparative Endocrinology 84:8393. https://doi.org/10.1016/0016-6480(91)90067-GCrossRefGoogle ScholarPubMed
Morkore, T, Mazo, PI, Tahirovic, V and Einen, O 2008 Impact of starvation and handling stress on rigor development and quali-ty of Atlantic salmon (Salmon salar L). Aquaculture 277: 231238. https://doi.org/10.1016/j.aquaculture.2008.02.036CrossRefGoogle Scholar
Noble, C, Kadri, S, Mitchell, DF and Huntingford, FA 2007a The impact of environmental variables on the feeding rhythms and daily feed intake of cage-held 1+ Atlantic salmon parr (Salmo salar L). Aquaculture 269: 290298. https://doi.org/10.1016/j.aquaculture.2007.04.079Google Scholar
Noble, C, Kadri, S, Mitchell, DF and Huntingford, FA 2007b Influence of feeding regime on intraspecific competition, fin dam-age and growth in 1+ Atlantic salmon parr (Salmo salar L) held in freshwater production cages. Aquaculture Research 38: 11371143. https://doi.org/10.1111/j.1365-2109.2007.01777.xCrossRefGoogle Scholar
Noble, C, Kankainen, M, Setala, J, Berrill, IK, Ruohonen, K, Damsgaard, B and Toften, H 2012 The bio-economic costs and benefits of improving productivity and fish welfare in aquaculture: utilizing CO2 stripping technology in Norwegian Atlantic salmon smolt production. Aquaculture Economics and Management 16: 297314. https://doi.org/10.1080/13657305.2012.729251Google Scholar
Nomura, M, Sloman, KA, von Keyserlingk, MAG and Farrell, AP 2009 Physiology and behaviour of Atlantic salmon (Salmo salar) smolts during commercial land and sea transport. Physiology and Behavior 96: 233243. https://doi.org/10.1016/j.phys-beh.2008.10.006CrossRefGoogle ScholarPubMed
Nordgreen, J, Horsberg, TE, Ranheim, B and Chen, ACN 2007 Somatosensory evoked potentials in the telencephalon of Atlantic salmon (Salmo salar) following galvanic stimulation of the tail. Journal of Comparative Physiology. A Neuroethology Sensory Neural and Behavioral Physiology 193: 12351242. https://doi.org/10.1007/s00359-007-0283-1Google ScholarPubMed
North, BP, Turnbull, JF, Ellis, T, Porter, MJ, Migaud, H, Bron, J and Bromage, NR 2006 The impact of stocking density on the welfare of rainbow trout (Oncorhynchus mykiss). Aquaculture 255:466479. https://doi.org/10.1016/j.aquaculture.2006.01.004CrossRefGoogle Scholar
Oehme, M, Aas, TS, Sørensen, M, Lygren, I and Åsgård, T 2012 Feed pellet distribution in a sea cage using pneumatic feeding system with rotor spreader. Aquacultural Engineering 51: 4452. https://doi.org/10.1016/j.aquaeng.2012.07.001CrossRefGoogle Scholar
Oldenburg, EW, Colotelo, AH, Brown, RS and Eppard, MB 2011 Holding of juvenile salmonids for surgical implantation of elec-tronic tags: a review and recommendations. Reviews in Fish Biology and Fisheries 36: 776784. https://doi.org/10.1007/s11160-010-9186-2Google Scholar
Persson, L and Alanara, A 2014 The effect of shelter on wel-fare of juvenile Atlantic salmon (Salmo salar) reared under a feed restriction regimen. Journal of Fish Biology 85: 845–656. https://doi.org/10.1111/jfb.12443Google Scholar
Pessot, CA, Atland, A, Liltved, H, Lobos, MG and Kristensen, T 2014 Water treatment with crushed marble or sodium silicate mitigates combined copper and aluminium toxici-ty for the early life stages of Atlantic salmon (Salmo salar L). Aquacultural Engineering 60: 7783. https://doi.org/10.1016/j.aquaeng.2014.04.001Google Scholar
Pettersen, JM, Bracke, MBM and Midtlying, PJ 2014 Salmon welfare index model 2.0: an extended model for overall welfare assessment of caged Atlantic salmon, based on a review of selected welfare indicators and intended for fish health professionals. Reviews in Aquaculture 6: 162169. https://doi.org/10.1111/raq.12039CrossRefGoogle Scholar
Portavella, M, Torres, B and Salas, C 2004 Avoidance response in goldfish: Emotional and temporal involvement of medial and lateral telencephalic pallium. Journal of Neuroscience 24:2342–2335. https://doi.org/10.1523/JNEUROSCI.4930-03.2004CrossRefGoogle ScholarPubMed
Remo, SC, Hevroy, EM, Olsvik, PA, Fontanillas, R, Breck, O and Waagbo, R 2014 Dietary histidine requirement to reduce the risk and severity of cataracts is higher than the requirement for growth in Atlantic salmon smolts, independently of the dietary lipid source. British Journal of Nutrition 111: 17591772. https://doi.org/10.1017/S0007114513004418CrossRefGoogle Scholar
Riley, SC, Tatara, CP, Berejikian, BA and Flagg, TA 2009 Behavior of steelhead fry in a laboratory stream is affected by fish density but not rearing environment, North American Journal of Fisheries Management 29: 18061818. https://doi.org/10.1577/M09-035.1CrossRefGoogle Scholar
Robb, DHF and Kestin, SC 2002 Methods used to kill fish: Field observations and literature reviewed. Animal Welfare 11: 269292Google Scholar
Roth, B, Grimsbo, E, Slinde, E, Foss, A, Stien, LH and Nortvedt, R 2012 Crowding, pumping and stunning of Atlantic salmon, the subsequent effect on pH and rigor mortis. Aquaculture 326: 178180. https://doi.org/10.1016/j.aquaculture.2011.11.005CrossRefGoogle Scholar
Roth, B, Imsland, A, Moeller, D and Slinde, E 2003 Effect of electric field strength and current duration on stunning and injuries in market-sized Atlantic salmon held in seawater. North American Journal of Aquaculture 65: 813. https://doi.org/10.1577/1548-8454(2003)065<0008:EOEF-SA>2.0.CO;2Google Scholar
Roth, B, Slinde, E and Robb, DHF 2007 Percussive stunning of Atlantic salmon (Salmo salar) and the relation between force and stunning. Aquacultural Engineering 36: 192197. https://doi.org/10.1016/j.aquaeng.2006.11.001Google Scholar
Royal Society for the Prevention of Cruelty to Animals (RSPCA) 2012 Welfare standards for farmed Atlantic salmon, October 2012. RSPCA: Horsham, West Sussex, UKGoogle Scholar
RSPCA 2015 RSPCA welfare standards for farmed Atlantic salmon. https://view.pagetiger.com/RSPCAWelfareStandardsforFarmedAtl anticSalmonGoogle Scholar
Salwiczek, LH, Prétôt, L, Demarta, L, Proctor, D, Essler, J, Pinto, AI, Wismer, S, Stoinski, T, Brosnan, SF and Bshary, R 2012 Adult cleaner wrasse outperform capuchin monkeys, chim-panzees and orang-utans in a complex foraging task derived from cleaner – client reef fish cooperation. PLoS ONE 7: e49068. https://doi.org/10.1371/journal.pone.0049068Google Scholar
Shrimpton, JM, Björnsson, BT and McCormick, SD 2000 Can Atlantic salmon smolt twice? Endocrine and biochemical changes during smolting. Canadian Journal of Fisheries and Aquatic Sciences 57: 19691976. https://doi.org/10.1139/f00-143CrossRefGoogle Scholar
Skjervold, PO, Fjæra, SO, Østby, PB and Einen, O 2001 Live-chilling and crowding stress before slaughter of Atlantic salmon (Salmo salar). Aquaculture 192: 265280. https://doi.org/10.1016/S0044-8486(00)00447-6Google Scholar
Sneddon, LU, Braithwaite, VA and Gentle, MJ 2003 Novel object test: examining nociception and fear in the rainbow trout. Journal of Pain 4: 431440. https://doi.org/10.1067/S1526-5900(03)00717-XCrossRefGoogle ScholarPubMed
Soderberg, RW, Meade, JW and Redell, LA 1993 Growth, survival, and food conversion of Atlantic salmon reared at four different densities with common water quality. The Progressive Fish-Culturist 55: 2931. https://doi.org/10.1577/1548-8640(1993)055<0029:GSAFCO>2.3.CO;22.3.CO;2>CrossRefGoogle Scholar
Stien, LH, Bracke, MBM, Folkedal, O, Nilsson, J, Oppedal, F, Torgersen, T, Kittilsen, S, Midtlyng, PJ, Vindas, MA, Overli, O and Kristiansen, TS 2013a Salmon Welfare Index Model (SWIM 1.0): a semantic model for overall welfare assessment of caged Atlantic salmon: review of the selected welfare indicators and model presentation. Reviews in Aquaculture 5: 3357. https://doi.org/10.1111/j.1753-5131.2012.01083.xCrossRefGoogle Scholar
Stien, LH, Fosseidengen, JE, Malm, ME, Sveier, H, Torgensen, T, Wright, DW and Oppedal, F 2013b Low inten-sity light of different colours modifies Atlantic salmon depth use. Aquacultural Engineering 62: 4248. https://doi.org/10.1016/j.aquaeng.2014.05.001CrossRefGoogle Scholar
Stones, DAJ 2003 Dietary carbohydrate utilization by fish. Reviews in Fisheries Science 11: 337369. https://doi.org/10.1080/10641260390260884Google Scholar
Summerfelt, ST, Sharrer, M, Gearheart, M, Gillette, K and Vinci, BJ 2009 Evaluation of partial water reuse systems used for Atlantic salmon smolt production at the White River National Fish Hatchery. Aquacultural Engineering 41: 7884. https://doi.org/10.1016/j.aquaeng.2009.06.003CrossRefGoogle Scholar
Tang, S, Thorarensen, H, Brauner, CJ, Wood, CM and Farrell, AP 2009 Modeling the accumulation of CO2 during high density, re-circulating transport of adult Atlantic salmon, (Salmo salar) from obser-vations aboard a sea-going commercial live-haul vessel. Aquaculture296:102-109. https://doi.org/10.1016/j.aquaculture.2009.07.020Google Scholar
Turnbull, J, Bell, A, Adams, C, Bron, J and Huntingford, F 2005 Stocking density and welfare of cage farmed Atlantic salmon: application of a multivariate analysis. Aquaculture 243: 121132. https://doi.org/10.1016/j.aquaculture.2004.09.022Google Scholar
Turnbull, JF 2006 Current issues in fish welfare. Journal of Fish Biology 68: 332372. https://doi.org/10.1111/j.0022-1112.2006.001046.xGoogle Scholar
Turnbull, JF, North, BP, Ellis, T, Adams, CE, Bron, J, MacIntyre, CM and Huntingford, FA 2008 Stocking density and the welfare of farmed salmonids. In: Branson, EJ (ed) Fish Welfare pp 111120. Blackwell Publishing Ltd: Oxford, UK. https://doi.org/10.1002/9780470697610.ch8CrossRefGoogle Scholar
Turnbull, JF, Richards, RH and Robertson, DA 1996 Gross, histological and scanning electron microscopic appearance of dor-sal fin rot in farmed Atlantic salmon, Salmo salar L parr. Journal of Fish Diseases 19: 415427. https://doi.org/10.1111/j.1365-2761.1996.tb00381.xGoogle Scholar
Waagbø, R, Jørgensen, SM, Timmerhaus, G, Breck, O and Olsvik, PA 2017 Short-term starvation at low temperature prior to harvest does not impact the health and acute stress response of adult Atlantic salmon. PeerJ 5: e3273. https://doi.org/10.7717/peerj.3273Google Scholar
Wedemeyer, GA 1996 Transportation and handling, In: Pennell W and Barton BA (eds) Developments in Aquaculture and Fisheries Science Volume 29 pp 727758. Elsevier: Amsterdam, The Netherlands. https://doi.org/10.1016/S0167-9309(96)80015-9Google Scholar
Wicks, BJ, Joensen, R, Tang, Q and Randall, DJ 2002 Swimming and ammonia toxicity in salmonids: the effect of sub lethal ammonia exposure on the swimming performance of coho salmon and the acute toxicity of ammonia in swimming and resting rainbow trout. Aquatic Toxicology 59: 5569. https://doi.org/10.1016/S0166-445X(01)00236-3CrossRefGoogle ScholarPubMed
W i n f ree, RA, K i nd s c h i, GA and S h a w, HT 1998 E l e v a t e d water temperature, crowding and food deprivation accelerate fin erosion in juvenile steelhead. Progressive Fish-Culturist 60: 192199. https://doi.org/10.1577/1548-8640(1998)060<0192:EWT-CAF>2.0.CO;2Google Scholar