Abstract
Gill disorders present a significant challenge in salmon (Salmo salar and Oncorhynchus sp.) farming regions throughout the world. This review of gill disorders and diseases of marine fish is focused on the non-infectious causes of gill disease in marine stage salmonids and these are grouped into harmful algae, such as Karenia mikimotoi, harmful zooplankton, such as Pelagia noctiluca, other environmental challenges, such as pollutants, as well as nutritional and genetic or congenital causes. The present level of understanding of these gill disorders is reviewed with regard to risk factors, potential impacting factors, methods of best practice to mitigate non-infectious gill disease and disorders, as well as knowledge gaps and avenues for future research.
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References
Ahn Y-H, Shanmugam P, Ryu J-H, Jeong J-C (2006) Satellite detection of harmful algae bloom occurrences in Korean waters. Harmful Algae 5:213–231
Albright LJ, Yang CZ, Johnson S (1993) Sublethal concentrations of the harmful diatoms, Chaetoceros concavicornis and C convolutes, increase mortality rates of penned Pacific salmon. Aquaculture 117:215–225
Anderson DM (2009) Approaches to monitoring, control and management of harmful algae blooms (HABS). Ocean Coast Manag 52:342–347
Anderson DM, Glibert PM, Burkholder JM (2008) Harmful algae blooms and eutrophication: nutrient sources, composition and consequences. Estuaries Coasts 25:704–726
Azanza RV, David LT, Borja RT, Baula IU, Fukuyo Y (2008) An extensive Cochlodinium bloom along the western coast of Palawan, Philippines. Harmful Algae 7:324–330
Baeverfjord G, Lein I, Åsgård T, Rye M (1997) Shortened opercula in Atlantic salmon (Salmo salar L) fry reared at high temperatures. In: Proceedings of the 8th international European association of fish pathologists conference. Edinburgh, Scotland P-015
Båmstedt U, Foss JH, Martinussen MB, Fosshagen A (1998) Mass occurrence of the physonect siphonophore Apolemia uvaria (Lesueur) in Norwegian waters. Sarsia 83:79–85
Barlann EA, Furikawa S, Tabeuchi K (2007) Detection of bacteria associated with harmful algal blooms from coastal and microcosm environments using electronic microassays. Environ Microbiol 9:690–702
Barnes RD (1987) Invertebrate zoology. CBS College Publishing, New York, pp 92–148
Barrows FT, Gaylord TG, Sealey WM, Porter L, Smith CE (2008) The effect of vitamin premix in extruded plant-based and fish meal based diets on growth efficiency and health of rainbow trout, Oncorhynchus mykiss. Aquaculture 283:148–155
Black E, Whyte JNC, Bagshaw JW, Ginther NG (1991) The effect of Heterosigma akashiwo on juvenile Oncorhynchus tshawytscha and its implications for fish culture. J Appl Ichthyo 7:168–175
Bolch JS, de Salas MF (2007) A review of the molecular evidence for ballast water introduction of the toxic dinoflagellates Gymnodinium catenatum and the Alexandrium ‘‘tamerensis complex’’ to Australasia. Harmful Algae 6:465–486
Branson EJ, Turnbull T (2008) Chapter 13: welfare and deformities in fish. In: Branson E (ed) Fish welfare. Blackwell, Oxford, pp 202–216
Bruno DW, Ellis AE (1985) Mortalities in farmed Atlantic salmon associated with the jellyfish Phialella quadrata. Bull Eur Assoc Fish Pathol 5:64–65
Bruno DW, Poppe TT (1996) Environmental factors affecting fish health In: A colour atlas of salmonid diseases. Academic Press Limited, London, pp 119–123
Bruno DW, Dear G, Seaton DD (1989) Mortality associated with phytoplankton blooms among farmed Atlantic salmon, Salmo salar, in Scotland. Aquaculture 78:217–222
Cannizzaro JP, Hu C, English DC, Carder KL, Heil CA, Müller-Karger FE (2009) Detection of Karenia brevis blooms on the west Florida shelf using in situ backscattering and fluorescence data. Harmful Algae 8:898–909
Carrasquero-Verde JR (1999) Role of associated bacteria in Heterosigma carterae toxicity to salmonids. Aquat Toxicol 45:19–34
Cembella AD, Quilliam MA, Lewis NI, Bauder AG, Dell’Aversano C, Thomas K, Jellett J, Cusack RR (2002) The toxigenic marine dinoflagellate Alexandrium tamarense as the probable cause of mortality of caged salmon in Nova Scotia. Harmful Algae 1:313–325
Chang FH, Anderson C, Boustead NC (1990) First record of a Heterosigma (Raphidophyceae) bloom with associated mortality of cage reared salmon in Big Glory Bay, New Zealand. NZ J Mar Freshw Res 24:461–469
Clarke WC (1992) Environmental factors in the production of Pacific salmon smolts. J World Aquacult Soc 23:40–42
Dahl E, Tangen K (1993) 25 years experience with Gyrodinium aureolum in Norwegian waters. In: Smayda TJ, Shimizu Y (eds) Toxic phytoplankton blooms in the sea. Elsevier, Amsterdam, pp 15–21
Dahl E, Lindahl O, Paasche E, Throndsen J (1989) The Chrysochromulina polypelis bloom in Scandinavian waters during spring 1988. In: Cosper EM et al (eds) Novel phytoplankton blooms: causes and effects of recurrent brown tide and other unusual blooms. Springer, New York, pp 383–405
Daranas AH, Norte M, Fernándes JJ (2001) Toxic marine microalgae. Toxicon 39:1101–1132
Davidson K, Miller P, Wilding TA, Shutler J, Bresnan E, Kennington K, Swan S (2009) A large and prolonged bloom of Karenia mikimotoi in Scottish waters in 2006. Harmful Algae 8:349–361
Deeds JR, Terlizzi DE, Adolf JE, Stoecker DK, Place AR (2002) Toxic activity from cultures of Karlodinium micrum (=Gyrodinium galatheanum) (Dinophyceae)—a dinoflagellate associated with fish mortalities in an estuarine aquaculture facility. Harmful Algae 1:169–189
Dempster T, Korsøen Ø, Folfedal O, Juell J-E, Oppedal F (2009) Submergence of Atlantic salmon (Salmo salar L) in commercial scale sea-cages: a potential short-term solution to poor surface conditions. Aquaculture 288:254–263
Doyle TK, De Haas H, Cotton D, Dorschell B, Cummins V, Houghton JDR, Davenport J, Hays GC (2008) Widespread occurrence of the jellyfish Pelagia noctiluca in Irish coastal and shelf waters. J Plankton Res 30:963–968
Edwards M, John AWG, Johns DG, Reid PC (2001) Case history and persistence of the non-indigenous diatom Coscinodiscus wailesii in the north-east Atlantic. J Mar Biol Assoc UK 81:207–211
Ferguson HW (2006) Systemic pathology of fish: a text and atlas of normal tissues reponses in teleosts, and their responses in disease. Scotian Press, London
Ferguson HW, Delannoy CMJ, Hay S, Nicolson J, Sutherland D, Crumlish M (2010) Jellyfish as vectors of bacterial disease for farmed salmon (Salmo salar). J Vet Diag Invest 22:376–382
Fernández-Tejedor M, Ángeles Soubrier-Pedreño M, Dolores Furones M (2004) Acute LD50 of a Gyrodinium corsicum natural population of Sparus aurata and Dicentrarchus labrax. Harmful Algae 3:1–9
Fossa JH, Flood PR, Olsen AB, Jensen F (2003) Sma og usynlige, men plagsomme maneter av arten Muggiaea atlantica. Havets Miljo, pp 99–103
Glibert PM, Landsberg JH, Evans JJ, Al-Sarawi MA, Faraj M, Al-Jarallah MA, Haywood A, Ibrahem S, Klesius P, Powell C, Shoemaker C (2002) A fish kill of massive proportion in Kuwait Bay, Arabian Gulf, 2001: the roles of bacterial disease, harmful algae, and eutrophication. Harmful Algae 1:215–231
Granéli E, Turner JT (2006) Ecology of harmful algae. Springer, Berlin
Gray RH, Saroglia MG, Scarano G (1985) Comparative tolerance to gas supersaturated water of two marine fishes, Dicentrachus labrax and Mugil cephalus. Aquaculture 48:83–89
Gunnarsli KS, Toften H, Mortensen A (2009) Effects of nitrogen gas supersaturation on growth and survival in larval cod (Gadus morhua). Aquaculture 288:344–348
Gustafsson S, Hultberg M, Figueroa RI, Renefors K (2009) On the control of HAB species using low surfactant concentrations. Harmful Algae 8:857–863
Hallegraeff GM (1995) Harmful algal blooms: a global overview. In: Hallegraeff GM, Anderson DM, Cembella AD (eds) 1995 Manual on harmful marine microalgae. IOC Manuals and Guides 33, UNESCO, pp 1–22
Harris JO, Powell MD, Attard M, Green TJ (2004) Efficacy of chloramine-T as a treatment for amoebic gill disease (AGD) in marine Atlantic salmon (Salmo salar L). Aquacult Res 35:1448–1456
Hay S (2006) Marine ecology: gelatinous bells may ring change in marine ecosystems. Curr Biol 16:R679–R682
Hay S, Murray A (2008) Jellyfish problems faced by the aquaculture industry. Fish Farmer, pp 40–41
Heil CA, Glibert PM, Al-Sarawi MA, Faraj M, Behbehani M, Husain M (2001) First record of a fish-killing Gymnodinium sp bloom in Kumait Bay, Arabian Sea: chronology and potential causes. Mar Ecol Prog Ser 214:15–23
Hellberg H, Olsen AB, Jensen F (2003) Clinical signs and histopathology in farmed Atlantic salmon (Salmo salar) associated with large numbers of the jellyfish Muggiaea atlantica, (Siphonophore). Book of Abstracts, 11th EAFP International Conference, September, Malta Poster, 52 pp
Helmholz H, Johnston BD, Ruhnau C, Prange A (2010) Gill cell toxicity of northern boreal scyphomedusae Cyanea capillata and Aurelia aurita measured by an in vitro cell assay. Hydrobiologia 645:223–234
Hoagland P, Scatasta S (2006) The economic effects of harmful algal blooms In: Grannéli E, Turner J (eds) Ecology of harmful algal blooms. Springer, Dordrecht, pp 391–402
ICES (2005) Report of the working group on pathology and diseases of marine organisms ICES. Copenhagen, Denmark
Imai I (2005) Mitigation strategies against harmful red tides by use of algicidal bacteria: application of seedweed beds as huge sources of algicidal bacteria. In: Proceedings of the Ist international workshop on HABs, Northwest Pacific Region, Toyama, Japan, pp 99–105
Jones JB, Rhodes LL (1994) Suffocation of pilchards (Sardinops sagax) by a green microalgal bloom in Wellington Harbour, New Zealand. NZ J Mar Freshw Res 28:379–383
Jones KJ, Ayres P, Bullock AM, Roberts RJ, Tett P (1982) A red tide of Gyrodinium aureolium in sea lochs of the Firth of Clyde and associated mortality of pond-reared salmon. J Mar Biol Assoc UK 63:771–982
Karges RG, Woodward B (1984) Development of lamellar epithelial hyperplasia in gills of pantothenic acid-deficient rainbow trout, Salmo gairdineri Richardson. J Fish Biol 25:57–62
Katsuo D, Kim D, Yamaguchi K, Matsuyama Y, Oda T (2007) A new simple screening method for the detection of cytotoxic substances produced by harmful red tide phytoplankton. Harmful Algae 6:790–798
Kempton JW, Lewitus AJ, Deeds JR, McHugh Law J, Place AR (2002) Toxicity of Karlodinium micrum (Dinophyceae) associated with a fish kill in a South Carolina brackish retention pond. Harmful Algae 1:233–241
Kent ML, Whyte JNC, LaTrace C (1995) Gill lesions and mortality in seawater pen-reared Atlantic salmon Salmo salar associated with a dense bloom of Skeletonema costatum and Thalassiosira species. Dis Aquat Org 22:77–81
Khan S, Arakawa O, Onoue Y (1997) Neurotoxins in a toxic red tide of Heterosigma akashiwo (Raphidophyceae) in Kagoshima Bay, Japan. Aquacult Res 28:9–14
Kiemer MCB, Black KD (1997) The effects of hydrogen peroxide on the gill tissues of Atlantic salmon, Salmo salar L. Aquaculture 153:181–189
Kiemer MCB, Black KD, Lussot D, Bullock AM, Ezzi I (1995) The effects of chronic and acute exposure to hydrogen sulphide on Atlantic salmon (Salmo salar L). Aquaculture 135:311–327
Kim HG (2006) Chapter 25 Mitigation and control of harmful algae. In: Grannéli E, Turner J (eds) Ecology of harmful algal blooms. Springer, Dordrecht, pp 327–338
Kim HG, Lee SG, Lee CK, Kim HG, Jung J (1997) Reactive oxygen species as causative agents in the ichthyotoxicity of the red tide dinoflagellate Cochlodinium polykrikoides. J Plank Res 23:2105–2115
Kroglund F, Finstad B, Stefansson SO, Nilsen TO, Kristensen T, Rossland BO, Tein HC, Salbu B (2007) Exposure to moderate acid water and aluminium reduces Atlantic salmon post-smolt survival. Aquaculture 27:360–373
Lee Y-JL, Choi J-K, Kim E-K, Youn S-H, Yang E-J (2008) Field experiments on mitigation of harmful algal blooms using a sophorolipid-yellow clay mixture and effects on marine plankton. Harmful Algae 7:154–162
Liber K, Weber L, Lévesque C (2005) Sublethal toxicity of two wastewater treatment polymers to lake trout fry (Salvelinus namaycush). Chemosphere 61:1123–1133
Lo W-T, Purcell JE, Hung J-J, Su H-M, Hsu P-K (2008) Enhancement of jellyfish (Aurelia aurita) populations by extensive aquaculture rafts in a coastal lagoon in Taiwan 2008. Int Council Explo Sea Oxford J 65:453–461
Lynam CP, Gibbons MJ, Axelson BE, Sparks CA, Coetzee J, Heywood BG, Brierley A (2006) Jellyfish overtake fish in a heavily fished ecosystem. Curr Biol 16:R492–R493
Mæland A, Waagbø R (1998) Examination of the qualitative ability of some cold water marine teleosts to synthesise ascorbic acid. Comp Biochem Physiol Part A 121:249–255
McGillicuddy DJ, Signell RP, Stock CA, Keafer BA, Keller MD, Hetland RD, Anderson DM (2003) A mechanism for initiation of harmful algal blooms in the coastal Gulf of Maine. J Plank Res 25:1131–1138
McManus MA, Kudela RM, Silver MW, Steward GF, Donaghay PL, Sullivan JM (2008) Cryptic blooms: are thin layers the missing connection? Estuaries Coasts 31:396–401
Mengedoht DM, Schulz J, Hirche H-J (2007) Imaging live zooplankton by lightframe on-sight key species investigation (LOKI). In: 4th international zooplankton production symposium, May 28–June 1, 2007, Hiroshima, Japan
Merceron M, Le Fèvre-Lehoërff G, Bizouarn Y, Kempf M (1995) Des poisons médusés. Equinox (Ifremer) 56:6–8
Mills CE (2001) Jellyfish blooms: are populations increasing globally in response to changing ocean conditions? Hydrobiologia 451:55–68
Mitchell S, Rodger H (2007) Pathology of wild and cultured fish affected by a Karenia mikimotoi bloom in Ireland, 2005. Bull Eur Assoc Fish Pathol 27:39–42
Mortensen DM (1985) Massive fish mortalities in the Faroe Islands caused by a Gonyaulax excavate red tide. In: Anderson MP et al (eds) Toxic dinoflagellates. Elsevier, New York, pp 165–170
National Veterinary Institute (2009) The health situation in Norwegian aquaculture 2009. NVI, Oslo, 34 pp (http://www.vetinst.no)
O’Connor B (2002) Jellyfish and salmon farming: is there a cause for concern? Aquaculture Ireland, Dec–Jan
Onoue Y (1990) Massive fish kills by a Ceratium fusus red tide in Kagoshima Bay, Japan. Red Tide News 3:2
Ørnsrud R, Gil L, Waagbo R (2004) Teratogenicity of elevated egg incubation temperature and egg vitamin A status in Atlantic salmon, Salmo salar L. J Fish Dis 27:213–223
Poston HA, Page JW (1982) Gross and histological signs of dietary deficiencies of biotin and pantothenic acid in lake trout, Salvelinus namaycush. Cornell Vet J 72:242–261
Powell M, Harris J (2004) Influence of oxygen on the toxicity of chloramine-T to Atlantic salmon smolts in freshwater and seawater. J Aquat Anim Health 16:83–92
Powell MD, Haman F, Wright GM, Perry SF (1998) Response of rainbow trout (Oncorhynchus mykiss) to a graded hypoxia following repeated intermittent exposure to chloramine-T. Aquaculture 165:27–39
Purcell JE (2005) Climate effects on formation of jellyfish and ctenophore blooms: a review. J Mar Biol Assoc UK 85:461–476
Purcell JE, Uye S, Lo W (2007) Anthropogenic causes of jellyfish blooms and their direct consequences for humans: a review. Mar Ecol Prog Ser 350:153–174
Qi D, Huang Y, Wang X (1993) Toxic dinoflagellate red tide by a Cochlodinium sp along the coast of Fujian, China. In: Smayda T, Shimizu Y (eds) Toxic phytoplankton blooms in the sea. Elsevier, Amsterdam, pp 235–238
Ratcliff J (2004) Mulroy Bay plankton monitoring, May to September 2004. Marine Harvest Ireland report, Kindrum, Co, Donegal, 12 pp
Renfro WC (1963) Gas bubble mortalities of fishes in Galveston Bay, Texas. Trans Am Fish Soc 92:320–322
Richardson AJ, Bakun A, Hays GC, Gibbons MJ (2009) The jellyfish joyride: causes, consequences and management responses to a more gelatinous future. Trends Ecol Evol 24:312–322
Riemann L, Titelman J, Bamstedt U (2006) Links between jellyfish and microbes in a jellyfish dominated fjord. Mar Ecol Prog Ser 325:29–42
Rigby GR, Stevenson IG, Bolch CJ, Hallegraeff GM (1993) The transfer and treatment of shipping ballast waters to reduce the dispersal of toxic marine dinoflagellates. In: Proceedings of the second international conference on marine Bioinvasions, New Orleans, La, April 9–11, 2001, pp 143–144
Riley CM, Holt SA, Holt GJ, Buskey EJ, Arnold CR (1989) Mortality of larval red drum (Sciaenops ocellatus) associated with a Ptychodiscus breis red tide. Contrib Mar Sci 31:137–146
Roberts RJ (2001) Chapter 11: miscellaneous non-infectious diseases. In: Roberts RJ (ed) Fish pathology. Saunders Publishing, London, pp 367–379
Roberts RJ, Rodger HD (2001) Chapter 3: the pathophysiology and systematic pathology of teleosts. In: Roberts RJ (ed) Fish pathology. Saunders Publishing, London, pp 55–133
Roberts RJ, Bullock AM, Turner M, Jones K, Tett P (1983) Mortalities of Salmo gairdinieri exposed to cultures of Gyrodinium aureolum. J Mar Biol Assoc UK 63:741–743
Rodger HD (2007) Gill disorders: an emerging problem for farmed Atlantic salmon (Salmo salar) in the marine environment? Fish Vet J 9:38–48
Rucker RR, Taylor W, Toney R (1963) Formalin in the hatchery. Prog Fish Cult 25:203–207
Rutter T (2010) Managing risk and uncertainty. Sunderland Marine Mutual Insurance, Advancing the Aquaculture agenda: policies to ensure a sustainable aquaculture sector, OECD, Paris, 15–16th April 2010 (www.oecd.org/dataoecd/11/3/45400772.pdf)
Sadler J, Pankhurst PM, King HR (2001) High prevalence of skeletal deformity and reduced gill surface area in triploid Atlantic salmon (Salmo salar L). Aquaculture 198:369–386
Sanchez JG, Speare DJ, Johnson GJ (1997) Morphometric and histochemical assessment of the branchial tissue response of rainbow trout, Oncorhynchus mykiss (Walbaum), associated with chloramine-T treatment. J Fish Dis 20:375–381
Sanchez JG, Speare DJ, Sims DE, Johnson GJ (1998) Morphometric assessment of epidermal and mucus-biofilm changes caused by exposure of trout to chloramine-T or formalin treatment. J Comp Path 118:81–87
Satake M, Shoji M, Oshima Y, Naoki H, Fujita T, Yasumoto T (2002) Gymnocin-A, a cytotoxic polyether from the notorious red tide dinoflagellate, Gymnodinium mikimotoi. Tetrahedron Lett 43:5829–5832
Satake M, Tanaka Y, Ishikura Y, Oshima Y, Naoki H, Yasumoto T (2005) Gymnocin-B with the largest contiguous polyether rings from the red tide dinoflagellate, Karenia (formerly Gymnodinium) mikimotoi. Tetrahedron Lett 46:3537–3540
Scholin C, Doucette G, Jensen S, Roman B, Pargett D, Preston C, Jones W, Feldman J, Everlove C, Harris A, Avarado N, Massion E, Birch J, Greenfield D, Wheeler K, Vrijenhoek R, Mikulski C, Jones K (2009) Remote detection of marine microbes, small invertebrates, harmful algae and biotoxins using the environmental sampling processor (ESP). Oceanography 22:158–167
Seo KS, Lee CK, Park YT, Lee Y (2008) Effect of yellow clay on respiration and phytoplankton uptake of bivalves. Fish Sci 74:120–127
Silke J, O’Brien F, Cronin M (2005) Karenia mikimotoi: an exceptional dinoflagellate bloom in western Irish waters, summer 2005. Marine Environment & Health Series. Number 21 Marine Institute, Oranmore
Smayda TJ (1997) Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol Oceanog 42:1137–1153
Sournia A (1995) Red tide and toxic marine phytoplankton of the world ocean: an inquiry into biodiversity. In: Lassus P et al (eds) Harmful marine algal blooms. Lavoisier, Intercept Ltd, Paris, pp 103–112
Speare DJ (1998) Chapter 8: disorders associated with exposure to excess gases In: Leatherhead JF, Woo PTK (eds) Fish dis eases and disorders, vol 2. CABI Publishing, Oxon
Speare DJ, Brackett J, Ferguson HW (1989) Sequential pathology of the gills of coho salmon with a combined diatom and microsporidian gill infection. Can Vet J 30:571–575
Speare DJ, Arsenault G, MacNair N, Powell MD (1997) Branchial lesions associated with intermittent formalin bath treatment of Atlantic salmon, Salmo salar L, and rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 20:27–33
Speare DJ, Carvajal V, Horney BS (1999) Growth suppression and branchitis in trout exposed to hydrogen peroxide. J Comp Path 120:391–402
Taveekijakarn P, Miyazaki T, Matsumoto M, Arai S (1996) Studies on vitamin K deficiency in amago salmon, Oncorhynchus rhodurus (Jordan & McGregor). J Fish Dis 19:209–214
Taylor FJR (1993) Current problems with harmful phytoplankton blooms in British Columbia In: Smayda TJ, Shimizu Y (eds) Toxic phytoplankton blooms in the sea. Elsevier, New York, pp 699–703
Treasurer JW, Hannah F, Cox D (2003) Impact of a phytoplankton bloom on mortalities and feeding response of farmed Atlantic salmon, Salmo salar, in west Scotland. Aquaculture 218:103–113
Vanhouette-Brunier A, Fernand L, Ménesguen A, Lyons S, Gohin F, Cugier P (2008) Modelling the Karenia mikimotoi bloom that occurred in the western English Channel during summer 2003. Ecol Modell 210:351–376
Waagbø R (2008) Chapter 15 reducing production related diseases in farmed fish In: Lie Ø (ed) Improving farmed fish quality and safety. Woodhead Publishing Limited, Cambridge
Wang J, Wu J (2009) Occurrence and potential risks of harmful algal blooms in the East China Sea. Sci Total Environ 407:4012–4021
Wood EM, Yasutake WT (1957) Histopathology of fish-V Gill diseases. Prog Fish-Cult 19:7–13
Woodward B (1994) Dietary vitamin requirements of cultured young fish, with emphasis on quantitative estimates for salmonids. Aquaculture 124:133–168
Yang CZ, Albright LJ (1992) Effects of the harmful diatom Chaetoceros concavicornis on respiration of rainbow trout Oncorhynchus mykiss. Dis Aquat Org 14:105–114
Yang CZ, Albright LJ (1994) Anti-phytoplankton therapy of finfish: the mucolytic agent L-cysteine ethyl ester protects coho salmon Oncorhynchus kisutch against the harmful phytoplankter Chaetoceros concavicornis. Dis Aquat Org 20:197–202
Yuki K, Yoshimatsu S (1989) Two fish-killing species of Cochlodinium from Harima Nada, Seto Inland Sea, Japan. In: Okaichi T et al (eds) Red tides: biology, environmental science and toxicology. Elsevier, New York
Zhang F, Su R, Wang X, Wang L, He J, Cai M, Luo W, Zheng Z (2009a) A fluorometric method for the discrimination of harmful algal bloom species developed by wavelet analysis. J Exp Mar Biol Ecol 368:37–43
Zhang F, Ma L, Xu Z, Zheng J, Shi Y, Lu Y, Miao Y (2009b) Sensitive and rapid detection of Karenia mikimotoi (Dinophyceae) by loop-mediated isothermal amplification. Harmful Algae 122:47–50
Zhou Q, Li K, Jun X, Bo L (2009) Role and functions of beneficial microorganisms in sustainable aquaculture. Bioresour Technol 100:3780–3786
Zingone R, Enevoldsen HO (2000) The diversity of harmful algal blooms: a challenge for science and management. Ocean Coast Manag 43:725–748
Acknowledgments
Dr. Tom Doyle and Ms. Emily Baxter of University College Cork are thanked for their valuable assistance and background information on gelatinous zooplankton. The veterinarians, fish health professionals and pathology colleagues who voluntarily gave of their time, experiences and advice for this document are sincerely thanked by the authors. Financial support was through the GILPAT project (project reference PBA/AF/08/002 (01)) as part of the National Development Programme, Ireland.
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Rodger, H.D., Henry, L. & Mitchell, S.O. Non-infectious gill disorders of marine salmonid fish. Rev Fish Biol Fisheries 21, 423–440 (2011). https://doi.org/10.1007/s11160-010-9182-6
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DOI: https://doi.org/10.1007/s11160-010-9182-6