Hostname: page-component-77f85d65b8-fcw2g Total loading time: 0 Render date: 2026-03-26T07:35:26.366Z Has data issue: false hasContentIssue false
  • English
  • Français

Assessment, causes and consequences of short opercula in laboratory-reared Atlantic salmon (Salmo salar)

Part of: Fish Collection

Published online by Cambridge University Press:  01 January 2023

E Blaker  and
T Ellis
E Blaker*
Affiliation:
Centre for Environment, Fisheries and Aquaculture Science (Cefas), Weymouth Laboratory, Barrack Road, The Nothe, Weymouth, Dorset DT4 8UB, UK
T Ellis
Affiliation:
Centre for Environment, Fisheries and Aquaculture Science (Cefas), Weymouth Laboratory, Barrack Road, The Nothe, Weymouth, Dorset DT4 8UB, UK
*
* Contact for correspondence: ellen.blaker@cefas.co.uk
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the 'Save PDF' action button.

Opercular deformity is a common morphological abnormality of laboratory and other cultured fishes, observed in a wide variety of species but with an unclear aetiology. Following observations of short opercula in stocks of Atlantic salmon (Salmo salar) reared in our laboratory, we developed a photographic key to score individual fish on a scale of 1 to 5. Inter-rater reliability was assessed as ‘almost perfect’. This visual method is quick and simple to use, can be used to score live fish in situ in tanks as well as sampled fish, does not require sophisticated equipment and provides quantitative information to investigate the aetiology of short opercula. Opercular size was scored for a cohort of in-house reared Atlantic salmon, in a time series of random samples of ≥ 30 fish (mean weights ranging from 0.8 to 299 g) over 14 months. Short opercula were first recorded during the parr stage, prevalence and severity increased as the fish grew, and the deformity was asymmetrical, occurring predominantly on the left side. Therefore, among the many potential causal factors, nipping is suggested as the primary cause of short opercula within our culture system, with asymmetry due to the clockwise current. We also present evidence that short opercula are associated with gill damage which supports this deformity being a welfare issue that merits assessment.

Keywords

animal welfareAtlantic salmonfish welfareopercular damagewelfare assessmentwelfare indicator

Information

Type
Research Article
Information
Animal Welfare , Volume 31 , Issue 1 , February 2022 , pp. 79 - 89
Copyright
© 2022 Universities Federation for Animal Welfare

References

Al-Harbi, AH 2001 Skeletal deformities in cultured common carp Cyprinus carpio L. Asian Fisheries Science 14: 247–254. https://doi.org/10.33997/j.afs.2001.14.3.001CrossRefGoogle Scholar
Amoroso, G, Adams, MB, Ventura, T, Carter, CG and Cobcroft, JM 2016 Skeletal anomaly assessment in diploid and triploid juvenile Atlantic salmon (Salmo salar L) and the effect of temperature in freshwater. Journal of Fish Diseases 39: 449–466. https://doi.org/10.1111/jfd.12438CrossRefGoogle ScholarPubMed
Andrews, B 2011 Ornamental Fish Farming: The Small, Medium and Large Scale Breeding and Marketing of Freshwater Tropical Fish and Goldfish. AbeBooks: Victoria, BC, CanadaGoogle Scholar
Baeverfjord, G, Antony Jesu Prabhu, P, Fjelldal, PG, Albrektsen, S, Hatlen, B, Denstadli, V, Ytteborg, E, Takle, H, Lock, EJ, Berntssen, MHG, Lundebye, AK, Åsgård, T and WaagbØ, R 2019 Mineral nutrition and bone health in salmonids. Reviews in Aquaculture: 740-765. https://doi.org/10.1111/raq.12255CrossRefGoogle Scholar
Barkstedt, J, Barkalow, SL, Farrington, MA, Kennedy, JL and Platania, SP 2018 Frequency of opercular deformities in age-0 native catostomids in the San Juan River from 1998 to 2012. Transactions of The American Fisheries Society 147: 1115–1123. https://doi.org/10.1002/tafs.10107CrossRefGoogle Scholar
Beraldo, B and Canavese, B 2011 Recovery of opercular anomalies in gilthead sea bream, Sparus aurata L: morphological and morphometric analysis. Journal of Fish Diseases 34: 21–30. https://doi.org/10.1111/j.1365-2761.2010.01206.xCrossRefGoogle ScholarPubMed
Beraldo, P, Pinosa, M, Tibaldi, E and Canavese, B 2003 Abnormalities of the operculum in gilthead sea bream (Sparus aurata): Morphological description. Aquaculture 220: 89–99. https://doi.org/10.1016/S0044-8486(02)00416-7CrossRefGoogle Scholar
Berillis, P 2015 Factors that can lead to the development of skeletal deformities in fishes: a review. Journal of Fisheries Sciences 9: 17–23Google Scholar
Boglione, C, Gisbert, E, Gavaia, P, Witten, PE, Moren, M, Fontagné, S and Koumoundouros, G 2013 Skeletal anomalies in reared European fish larvae and juveniles. Part 2: Main typolo-gies, occurrences and causative factors. Reviews in Aquaculture 5: 121–167. https://doi.org/10.1111/raq.12016CrossRefGoogle Scholar
Boglione, C, Pulcini, D, Scardi, M, Palamara, E, Russo, T and Cataudella, S 2014 Skeletal anomaly monitoring in rainbow trout (Oncorhynchus mykiss, Walbaum 1792) reared under different conditions. PLoS One 9(5). https://doi.org/10.1371/journal.pone.0096983CrossRefGoogle ScholarPubMed
Branson, EJ and Turnbull, T 2008 Welfare and deformities in fish. In: Branson, EJ (ed) Fish Welfare pp 202–216. Blackwell Publishing Ltd: Oxford, UK. https://doi.org/10.1002/9780470697610.ch13CrossRefGoogle Scholar
Bruno, DW 1990 Miscellaneous external abnormalities of farmed salmonids. Aquaculture Information Series 11: 1–6Google Scholar
Conceicao, L and Tandler, A 2018 Success Factors for Fish Larval Production. Wiley Blackwell: Oxford, UKGoogle Scholar
Darias, MJ, Mazurais, D, Koumoundouros, G, Cahu, CL and Zambonino-Infante, JL 2011 Overview of vitamin D and C require-ments in fish and their influence on the skeletal system. Aquaculture 315: 49–60. https://doi.org/10.1016/j.aquaculture.2010.12.030CrossRefGoogle Scholar
Divanach, P, Boglione, C, Cataudella, S, Menu, B, Koumoundouros, G and Kentouri, M 1996 Abnormalities in finfish mariculture: An overview of the problem, causes and solutions. International Workshop on Sea Bass and Sea Bream Culture: Problems and Prospects pp 45–66. 16–18 October, 1996, Verona, ItalyGoogle Scholar
Drost, MR, Muller, M and Osse, JWM 1988 A quantitative hydrodynamical model of suction feeding in larval fishes: the role of friction forces. Proceedings of the Royal Society of London 234: 263–281. https://doi.org/10.1098/rspa.1952.0029Google 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: 493–531. https://doi.org/10.1006/jfbi.2002.2057CrossRefGoogle 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, EJ (ed) Fish Welfare pp 121–149. Blackwell Publishing Ltd: Oxford, UK. https://doi.org/10.1002/9780470697610.ch9CrossRefGoogle Scholar
Ellis, T, Rimmer, GSE, Parker, SJ, Joiner, C, Sebire, M, Verner-Jeffreys, DW and Lines, J 2019 Intank underwater cameras can refine monitoring of laboratory fish. Animal Welfare 28: 191–203. https://doi.org/10.7120/09627286.28.2.191CrossRefGoogle Scholar
Fraser, MR and De Nys, R 2005 The morphology and occur-rence of jaw and operculum deformities in cultured barramundi (Lates calcarifer) larvae. Aquaculture 250: 496–503. https://doi.org/10.1016/j.aquaculture.2005.04.067CrossRefGoogle Scholar
Fraser, TWK, Hansen, T, Fleming, MS and Fjelldal, PG 2015 The prevalence of vertebral deformities is increased with higher egg incubation temperatures and triploidy in Atlantic salmon Salmo salar L. Journal of Fish Diseases 38: 75–89. https://doi.org/10.1111/jfd.12206CrossRefGoogle ScholarPubMed
Georgakopoulou, E, Katharios, P, Divanach, P and Koumoundouros, G 2010 Effect of temperature on the develop-ment of skeletal deformities in Gilthead seabream (Sparus aurata Linnaeus, 1758). Aquaculture 308: 13–19. https://doi.org/10.1016/j.aquaculture.2010.08.006CrossRefGoogle Scholar
Handwerker, TS and Tave, D 1994 Semioperculum: A non-heri-table deformity in Mozambique Tilapia. Journal of Aquatic Animal Health 6: 85–88. https://doi.org/10.1577/1548-8667(1994)006<0085:SANDIM>2.3.CO;2Google Scholar
Hawkins, P, Dennison, N, Goodman, G, Hetherington, S, Llywelyn-Jones, S, Ryder, K and Smith, AJ 2011 Guidance on the severity classification of scientific procedures involving fish: Report of a Working Group appointed by the Norwegian Consensus-Platform for the Replacement, Reduction and Refinement of animal experiments (Norecopa). Laboratory Animals 45: 219–224. https://doi.org/10.1258/la.2011.010181CrossRefGoogle Scholar
Helsley, CE, Ostrowski, AC, Brock, JH and Leung, P 2001 Hawaii Offshore Aquaculture Research Project. https://www.research-gate.net/publication/267401613Google Scholar
Hoyle, I, Oidtmann, B, Ellis, T, Turnbull, J, North, B, Nikolaidis, J and Knowles, TG 2007 A validated macroscopic key to assess fin damage in farmed rainbow trout (Oncorhynchus mykiss). Aquaculture 270: 142–148. https://doi.org/10.1016/j.aquaculture.2007.03.037CrossRefGoogle Scholar
Jensen, JOT 1988 Combined effects of gas supersaturation and dissolved oxygen levels on steelhead trout (Salmo gairdneri) eggs, larvae, and fry. Aquaculture 68: 131–139. https://doi.org/10.1016/0044-8486(88)90236-0CrossRefGoogle Scholar
Jirkof, P, Jarvis, G and Riederer, B 2020 Collection on score sheets, severity assessment and humane end points: Invitation to submit. Laboratory Animals 54: 149. https://doi.org/10.1177/0023677220906399CrossRefGoogle ScholarPubMed
Jobling, M, Baardvik, BM, Christiansen, JS and Jørgensen, EH 1993 The effects of prolonged exercise training on growth perfor-mance and production parameters in fish. Aquaculture International 1: 95–111. https://doi.org/10.1007/BF00692614CrossRefGoogle Scholar
Jobling, M and Wandsvik, A 1983 Effect of social interactions on growth rates and conversion efficiency of Arctic charr, Salvelinus alpinus L. Journal of Fish Biology 22: 577–584. https://doi.org/10.1111/j.1095-8649.1983.tb04217.xCrossRefGoogle Scholar
Kazlauskienë, N, Leliüna, E and Kesminas, V 2006 Peculiarities of opercular malformations of salmon (Salmo salar L) juveniles reared in the Žeimena salmon hatchery. Acta Zoologica Lituanica 16: 312–316. https://doi.org/10.1080/13921657.2006.10512747CrossRefGoogle Scholar
Knight, J and Goodwin, N 2016 Zebrafish health and welfare glos-sary - Welfare Terms, Head. https://zfin.atlassian.net/wiki/spaces/ZHWG/pages/514228273/Ze brafish+Health+and+Welfare+Glossary+-+Welfare+Terms+HeadGoogle Scholar
Koumoundouros, G, Oran, G, Divanach, P, Stefanakis, S and Kentouri, M 1997 The opercular complex deformity in intensive gilthead sea bream (Sparus aurata L) larviculture. Moment of apparition and description. Aquaculture 156: 165–177. https://doi.org/10.1016/S0044-8486(97)89294-0CrossRefGoogle Scholar
Lalone, CA, Villeneuve, DL, Olmstead, AW, Medlock, EK, Kahl, MD, Jensen, KM, Durhan, EJ, Makynen, EA, Blanksma, CA, Cavallin, JE, Thomas, LM, Seidl, SM, Skolness, SY, Wehmas, LC, Johnson, RD and Ankley, GT 2012 Effects of a glucocorticoid receptor agonist, dexamethasone, on fathead min-now reproduction, growth, and development. Environmental Toxicology and Chemistry 31: 611–622. https://doi.org/10.1002/etc.1729CrossRefGoogle ScholarPubMed
Larsen, MH, Nemitz, A, Steinheuer, M, Lysdal, J, Thomassen, S and Holdensgaard, G 2018 Effects of hatchery feeding practices on fin and operculum condition of juvenile Atlantic salmon Salmo salar. https://www.researchgate.net/publication/325218078_Effects_of_ hatchery_feeding_practices_on_fin_and_operculum_condition_of_juvenile_Atlantic_salmon_Salmo_salarGoogle Scholar
Lindesjoo, E, Thulin, J, Bengtsson, B and Tjarnlund, U 1994 Abnormalities of a gill cover bone, the operculum, in perch Perca fluviatilis from a pulp mill effluent area. Aquatic Toxicology 28: 189–207. https://doi.org/10.1016/S0044-8486(02)00416-7CrossRefGoogle Scholar
Murray, DS, Adams, CE, McDade, K, Solomon, SE and Bain, MM 2016 Effect of broodstock holding environment on egg qual-ity in farmed brown trout (Salmo trutta). Animal Reproduction 13: 743–749. https://doi.org/10.21451/1984-3143-AR787CrossRefGoogle Scholar
Noble, C, Gismervik, K, Iversen, MH, Kolarevic, J, Nilsson, J, Stien, LH and Turnbull, JF 2018 Welfare indicators for farmed Atlantic salmon: tools for assessing fish welfare. Nofima: Tromso, Norway. http://hdl.handle.net/11250/2575780Google Scholar
Noble, C, Jones, HAC, Damsgård, B, Flood, MJ, Midling, KO, Roque, A, Sæther, BS and Cottee, SY 2012 Injuries and defor-mities in fish: Their potential impacts upon aquacultural production and welfare. Fish Physiology and Biochemistry 38: 61–83. https://doi.org/10.1007/s10695-011-9557-1CrossRefGoogle ScholarPubMed
Ortiz-Delgado, JB, Fernández, I, Sarasquete, C and Gisbert, E 2014 Normal and histopathological organization of the opercu-lar bone and vertebrae in gilthead sea bream sparus aurata. Aquatic Biology 21: 67–84. https://doi.org/10.3354/ab00568CrossRefGoogle Scholar
Osburn, R 1911 The effects of exposure on the filaments of fishes. Transactions of the American Fisheries Society 40: 371–376. https://doi.org/10.1577/1548-8659(1910)40[371:TEOEOT]2.0.CO;2CrossRefGoogle Scholar
Peruzzi, S, Puvanendran, V, Riesen, G, Seim, RR, Hagen, ⊘, Martínez-Llorens, S, Falk-Petersen, IB, Fernandes, JMO and Jobling, M 2018 Growth and development of skeletal anomalies in diploid and triploid Atlantic salmon (Salmo salar) fed phospho-rus-rich diets with fish meal and hydrolyzed fish protein. PLoS One 13: 1–16. https://doi.org/10.1371/journal.pone.0194340CrossRefGoogle ScholarPubMed
Petrie, A and Sabin, C 2000 Medical Statistics at a Glance, Second Edition. Blackwell Publishing: Oxford, UKGoogle Scholar
Pettersen, JM, Bracke, MBM, Midtlyng, PJ, Folkedal, O, Stien, LH, Steffenak, H and Kristiansen, TS 2014 Salmon welfare index model 2.0: An extended model for overall welfare assess-ment of caged Atlantic salmon, based on a review of selected wel-fare indicators and intended for fish health professionals. Reviews in Aquaculture 6: 162–179. https://doi.org/10.1111/raq.12039CrossRefGoogle Scholar
Plunkett, S and Snyder-Conn, E 2000 Anomalies of larval and juvenile shortnose and Lost River suckers in Upper Klamath Lake, Oregon pp 1–25. Fish & Wildlife Service, Klamath Falls Office, Oregon, USAGoogle Scholar
R Development Core Team 2013 A Language and Environment for Statistical Computing. R Foundation for Statistical Computing: Vienna, AustriaGoogle Scholar
Ribelin, W and Migaki, G 1975 Pathology of Fishes. In: Ribelin, W and Migaki, G (eds) The Pathology of Fishes pp 305–330. The University of Wisconsin Press: USAGoogle Scholar
RSPCA 2021 RSPCA Welfare Standards for Farmed Atlantic Salmon pp 1–90. https://science.rspca.org.uk/documents/1494935/9042554/RSPCA+wel-fare+standards+for+farmed+Atlantic+salmon+%28PDF%29.pdf/60ae55ee-7e92-78f9-ab71-ffb08c846caa?t=1618493958793Google Scholar
Ruban, GI, Akimova, NV, Goriounova, VB, Mikodina, EV, Nikolskaya, MP, Shagayeva, VG, Shatunovsky, MI and Sokolova, SA 2006 Abnormalities in sturgeon gametogenesis and postembryonal ontogeny. Journal of Applied Ichthyology 22: 213–220. https://doi.org/10.1111/j.1439-0426.2007.00954.xCrossRefGoogle Scholar
Russell, WMS and Burch, RL 1959 The Principles of Humane Experimental Technique. Methuen: London, UK. https://doi.org/10.5694/j.1326-5377.1960.tb73127.xCrossRefGoogle Scholar
Sadler, J, Pankhurst, PM and King, HR 2001 High prevalence of skeletal deformity and reduced gill surface area in triploid Atlantic salmon (Salmo salar L). Aquaculture 198: 369–386. https://doi.org/10.1016/S0044-8486(01)00508-7CrossRefGoogle Scholar
Skipnes, BI 2014 Prevalence of fin erosion, shortened operculum and lesions in farmed Atlantic Salmon ( Salmo salar). Norwegian University of Technology, NorwayGoogle Scholar
Smith, P 1997 The epizootiology of furunculosis: the present state of our ignorance. Furunculosis - multidisciplinary fish disease research pp 25–53. Academic Press: San Diego, USA. https://doi.org/10.1016/B978-012093040-1/50005-1CrossRefGoogle Scholar
Speare, DJ and Ferguson, HW 2006 Gills and pseudobranch. Systemic pathology of fish: a text and atlas of normal tissues in teleosts and their responses in disease pp 24–63. Scotian Press: London, UKGoogle Scholar
Stevenson, P 2007 Closed waters: The welfare of farmed atlantic salmon, rainbow trout, atlantic cod & atlantic halibut. Compassion in World Farming and the World Society for the Protection of Animals: 1-80Google Scholar
Taylor, JF, Leclercq, E, Preston, AC, Guy, D and Migaud, H 2012 Parr-smolt transformation in out-of-season triploid Atlantic salmon (Salmo salar L). Aquaculture 362-363: 255-263. https://doi.org/10.1016/j.aquaculture.2010.12.028CrossRefGoogle Scholar
Timmons, MB, Summerfelt, ST and Vinci, BJ 1998 Review of circular tank technology and management. Aquacultural Engineering 18: 51–69. https://doi.org/10.1016/S0144-8609(98)00023-5CrossRefGoogle Scholar
Turnbull, JF, Adams, CE, Richards, RH and Robertson, DA 1998 Attack site and resultant damage during aggressive encoun-ters in Atlantic salmon (Salmo salar L) parr. Aquaculture 159: 345–353. https://doi.org/10.1016/S0044-8486(97)00233-0CrossRefGoogle Scholar
Vatsos, IN 2017 Standardising the microbiota of fish used in research. Laboratory Animals 51: 353–364. https://doi.org/10.1177/0023677216678825CrossRefGoogle ScholarPubMed