Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-22T19:45:10.803Z Has data issue: false hasContentIssue false

Aquatic pollution: effects on the health of fish and shellfish

Published online by Cambridge University Press:  23 August 2011

D. Bucke
Affiliation:
Ministry of Agriculture, Fisheries and Food, Directorate of Fisheries Research, Fish Diseases Laboratory, Weymouth, Dorset DT4 9TH

Summary

As there is little evidence of pollution affecting the health of fish and shellfish on a global scale, this paper attempts to put into perspective the pollution/fish disease relationship by reviewing examples of studies and reports in the historic and current literature. Although there is no dispute that pollution can affect the health of aquatic organisms under laboratory conditions and may be responsible for the decline of populations of such animals in some inland waters and some estuaries, most of the evidence for pollution causing or increasing disease in fish in open waters is circumstantial. Historical data proves that almost all fish and shellfish diseases known today have been described since the end of the last century. However, it is also known that water pollution, especially in inland waters, has for the past 400-500 years been the result of urbanization and industrialization. This has resulted in some major rivers becoming devoid of or deficient in fish stocks. The concern that pollution may influence the health status of fish and shellfish stocks has increased over the past 20 years. Initial attention was paid to epidermal diseases, including fin-rot in demersal fish, and protozoan diseases in molluscs in the heavily polluted bays and estuaries in North America. As the interest in this subject spread, it became political, and often controversial, especially amongst the North Sea countries. The disagreements have largely been settled amongst scientists because international bodies, such as the International Council for Exploration of the Sea (ICES), established workshops to investigate sampling methods and disease-reporting techniques. Recommendations from those workshops have contributed to some form of standardization for field work and the subject, although largely subjective, has some objective approaches which are described. As there are variable, interacting biological and physical influences in the aquatic environment, it is difficult to establish the background prevalences of diseases in populations offish and shellfish. Examples of the influences of climatic changes are presented, and these show that short-term catastrophes can be directly related. However, a more long-term problem is water acidification resulting largely from anthropogenic activities. In parts of Scandinavia this has, and is, leading to decimation offish stocks in inland waters. In general, diseases in fish and shellfish are very localized, but there is concern amongst scientists that certain cancers, especially liver tumours, occurring in demersal fish inhabiting polluted estuarine and coastal waters, are related to the release of chemicals, e.g. hydrocarbons, pesticides and heavy metals. This subject is discussed in detail, with examples of the author's own studies in North Sea fish. It is concluded that cancers in fish are of extremely low prevalence, and only present in a very few species, and then only in the oldest animals. Though changes in disease pattern may well be an indication of adverse environmental effects, further research is necessary for conclusive evidence.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1993

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alabaster, J. S., Garland, J. H. N., Hart, I. C. & Solbe, J. F. de L. G. (1972). An approach to the problem of pollution and fisheries. Symposium of the Zoological Society of London 29, 87114.Google Scholar
Anders, K. & Moller, H. (1985). Spawning papillomatosis of smelt, Osmerus eperlanus L., from the Elbe Estuary. Journal of Fish Diseases 8, 233–5.CrossRefGoogle Scholar
Andrews, M. J. & Rickard, D. G. (1980). Rehabilitation of the inner Thames Estuary. Marine Pollution Bulletin 11, 327–32.CrossRefGoogle Scholar
Black, J. J., Holmes, M., Dymerski, P. P. & Zapisek, W. F. (1980). Fish tumor pathology and aromatic hydrocarbon pollution in a Great Lakes estuary. In Hydrocarbons in the Aquatic Environment (ed. Gan, B. K. A. & McKay, D), pp. 559–65.CrossRefGoogle Scholar
Brown, J. R., Gowen, R. & Luskky, D. S. (1987). The effect of salmon farming on the benthos of a Scottish Sea Loch. Journal of Marine Biology and Ecology 109, 3951.CrossRefGoogle Scholar
Bucke, D. (1976). Neoplasia in roach (Rutilus rutilus L.) from a polluted environment. Progress in Experimental Tumour Research 20, 205–11.CrossRefGoogle ScholarPubMed
Bucke, D. (1991). Current approaches to the study of pollution-related diseases in fish. Bulletin of the European Association of Fish Pathologists 11, 4653.Google Scholar
Bucke, D. & Feist, S. W., (in press). Histopathological changes in the livers of dab, Limanda limanda L. Journal of Fish Diseases.Google Scholar
Bucke, D. & Nicholson, M. D. (1987). Fish disease investigations in the Irish Sea. ICES CM/E: 19, 7 pp. Mimeo.Google Scholar
Bucke, D. & Stokes, K. (1988). Fish disease monitoring on the 1987 North Sea Ground-fish Survey. ICES CM/E 7, 10 pp. Mimeo.Google Scholar
Bucke, D. & Watermann, B. (1988). Effects of pollutants on fish. In Pollution of the North Sea: an assessment (ed. Salomons, W., Bayne, B. L., Duursma, E. K. & Forstner, U.), pp. 612–23. Berlin: Springer-Verlag.Google Scholar
Bucke, D., Norton, M. G. & Rolfe, M. S. (1983). The field assessment of effects of dumping wastes at sea. II. Epidermal lesions and abnormalities of fish in the outer Thames Estuary. MAFF Fishers Research Technical Report No. 72, 16 pp.Google Scholar
Bucke, D., Watermann, B. & Feist, S. W. (1984). Histological variations of hepato-splenic organs from the North Sea dab, Limanda limanda (L.). Journal of Fish Diseases 7, 255268.CrossRefGoogle Scholar
Buckland, F. (1883). Natural History of British Fishes. Salmonidae: The Salmon, pp. 288314. London: Gresham Press.Google Scholar
Bullock, A. M. & Coults, R. R. (1985). Fish can suffer from sunburn. Fish Farming International 12, 5.Google Scholar
Chubb, J. C. (1976). Seasonal occurrence of helminths in freshwater fishes. Part II. Trematoda. Advances in Parasitology 17, 111–31.Google Scholar
Clifton-HADLEY, R. S., Richards, R. H. & Bucke, D. (1986). Proliferative kidney disease (PKD) in rainbow trout Salmo gairdneri: further observations on the effects of water temperature. Aquaculture 55, 165–71.CrossRefGoogle Scholar
Clifton-HADLEY, R. S, Bucke, D. & Richards, R. H. (1987). A study of the sequential clinical and pathological changes during proliferative kidney disease (PKD) in rainbow trout Salmo gairdneri Richardson. Journal of Fish Biology 10, 335–52.Google Scholar
Couch, J. A. & Harshbarger, J. C. (1985). Effects of carcinogenic agents on aquatic animals: an environmental and experimental overview. Environmental Carcinogenesis Reviews 3, 63105.Google Scholar
Crisp, D. J., Woodhead, P. M. J., Coleman, J. S. & Waugh, G. D. (1964). The death of fish and sub-littoral fauna in the North Sea and the English Channel during the winter of 1962-63. Journal of Animal Ecology 33, 169–74.Google Scholar
Dawe, C. J. (1981). Polyoma tumors in mice and X-cell tumors in fish, viewed through telescope and microscope. In Phyletic Approaches to Cancer (ed. Dawe, C. J., Harshbarger, J. C., Kondo, S., Sugimura, T. & Takayama, S.), pp. 1949. Tokyo: Japanese Scientific Society Press.Google Scholar
Dawe, C. J. & Harshbarger, J. C. (1975). Neoplasms in feral fishes: their significance to cancer research. In The Pathology of Fishes (ed. Ribelin, W. E. & Migaki, G), pp. 871–94. Madison, Wisconsin, USA: University of Wisconsin Press.Google Scholar
Dethlefsen, V. (1980). Observations on fish diseases in the German Bight and their possible relation to pollution. Rapports et Procès- Verbaux des Réunions - Conseil Permanent International pour l'Exploration de la Mer 179, 110–17.Google Scholar
Dethlefsen, V. (1988). Status report on aquatic pollution problems in Europe. Aquatic Toxicology 11, 259–86.CrossRefGoogle Scholar
Dethlefsen, V. (1989). Fish in the polluted North Sea. Dana 8, 109–29.Google Scholar
Dethlefsen, V. & Tiews, K. (1985). Review on the effects of pollution on marine fish life and fisheries in the North Sea. Zeitschrift für angewandte Ichthyologie 3, 97118.CrossRefGoogle Scholar
Dethlefsen, V., Watermann, B. & Hoppenheit, M. (1984). Sources of variance in data from fish disease surveys. Archiv für Fischerwissenschaft 34, 155–73.Google Scholar
Farley, C. A. (1969). Probable neoplastic disease of the hematopoietic system in oysters, Crassostrea virginica and Crassostrea gigas. National Cancer Institute Monograph 31, 341–55.Google Scholar
Farley, C. A. & Sparks, A. K. (1970). Proliferative diseases of hemocytes, endothelial cells and connective tissue in mollusks. Bibliography of Haematology 36, 610–17.Google Scholar
Fijan, N. N. (1972). Infectious dropsy in carp - a disease complex. Symposium of the Zoological Society of London 30, 3951.Google Scholar
Fisher, W. S., Chintala, M. M. & Moline, M. A. (1989). Aquatic pollution and fish health Annual variation of estuarine and oceanic oyster Crassostrea virginica Gmelin hemocyte capacity. Journal of Experimental Marine Biology and Ecology 127, 105–20.CrossRefGoogle Scholar
Frith, C. H. & Ward, J. M. (1980). A morphologic classification of proliferative and neoplastic hepatic lesions in mice. Journal of Environmental Pathology, Toxicology and Oncology 3, 329–51.Google Scholar
Gardner, G. R., Yevich, P. P., Malcolm, A. R., Rogerson, P. F., Mills, L. J., Senecal, A. G., Lee, T. C., Harshbarger, J. C. & Cameron, T. P. (1988). Tumor development in American oysters and winter flounder exposed to a contaminated marine sediment under laboratory and field conditions. In Aquatic Toxicology 11 (ed. Malins, D. C. & Jensen, A), pp. 403–4. Amsterdam: Elsevier Science Publishers, B.V.Google Scholar
GESAMP. (1991). Review of potentially harmful substances: carcinogens. Report of the studies of the joint group of experts on the scientific aspects of marine pollution. No. 46, 56 pp.Google Scholar
Haensley, W. E., Neff, J. M., Sharp, J. R., Morris, A. C., Bedgood, M. F. & Boem, P. D. (1982). Histopathology of Pleuronectes platessa L. from Aber Wrac ‘H and Aber Benoit, Brittany, France: long-term effects of the AMOCO Cadiz crude oil spill. Journal of Fish Diseases 5, 365–91.CrossRefGoogle Scholar
Halliday, M. M. (1976). The biology of Myxosoma cerebralis, the causative organism of whirling disease of salmonids. Journal of Fish Biology 9, 339–57.CrossRefGoogle Scholar
Harada, T., Maronpot, R. R., Morris, R. W., Stitzel, K. A. & Boorman, G. A. (1989). Morphology and stereological characterization of hepatic foci of cellular alteration in control Fischer 344 rats. Toxicologic Pathology 17, 579–93.CrossRefGoogle ScholarPubMed
Harshbarger, J. C., Charles, A. M. & Spero, P. M. (1981). Collection and analysis of neoplasms in subhomothermic animals from a phyletic point of view. In Phyletic Approaches to Cancer (ed. Dawe, C. J., Harshbarger, J. C., Kondo, S., Sugimura, T. & Takayama, S.), pp. 357–84. Tokyo: Japanese Scientific Society Press.Google Scholar
Hendricks, J. D. (1982). Chemical carcinogenesis in fish. In Aquatic Toxicology, Vol. 1 (ed. Waher, L), pp. 149211. New York: Raven Press.Google Scholar
Heron, F., Bucke, D., Chubb, J. C. & Wallace, I. D. (1988). Re-appraisals of the James Johnstone collection of examples of diseased fish materials. ICES CM 1988/E 9, 9 pp. Mimeo.Google Scholar
Hoffman, G. L. (1976). Fish diseases and parasites in relation to the environment. Fish Pathology 10, 123–8.CrossRefGoogle Scholar
Hoglund, J. & Thulin, J. (1990). The epidemiology of the metacercariae of Diplostomum baeri and D. spathaceum in perch (Perca fluviatilis) from the warm water effluent of a nuclear power station. Journal of Helminthology 64, 139–50.CrossRefGoogle Scholar
ICES. (1989). Methodology of fish disease surveys. Report of an ICES Sea-going Workshop held on U/F ARGOS, 16-23 April 1988. ICES Co-operative Research Report No. 166, 33 pp.Google Scholar
ICES. (1991). New cod and climate study interests ICES scientists. ICES Information, Copenhagen No. 18, 12.Google Scholar
Johnstone, J. (1905). Internal parasites and diseased conditions of fishes. Transactions of the Liverpool Biological Society 19, 278300.Google Scholar
Johnstone, J. (1906). Internal parasites and diseased conditions of fishes. Transactions of the Liverpool Biological Society 20, 295329.Google Scholar
Johnstone, J. (1922). Diseases and parasites of fishes. Transactions of the Liverpool Biological Society 36, 286301.Google Scholar
Johnstone, J. (1923). On some malignant tumours in fishes. Transactions of the Liverpool Biological Society 37, 145–7.Google Scholar
Karlsson-NORRGREN, L., Dickson, W., Ljungberg, O. & Runn, P. (1986). Acid water and aluminium exposure: gill lesions and aluminium accumulation in farmed brown trout, Salmo trutta L. Journal of Fish Diseases 9, 19.CrossRefGoogle Scholar
Khudoley, V. V. & Syrenko, O. A. (1978). Tumor induction by N-nitroso compounds in bivalve molluscs Unio pictorum. Cancer Letters 4, 349–54.CrossRefGoogle ScholarPubMed
Köhler, A. & Holzel, F. (1980). Investigation on health conditions of flounder and smelt in the Elbe estuary. Helgoländer Meeresuntersuchungen 33, 401–44.CrossRefGoogle Scholar
Kranz, H. & Dethlefsen, V. (1990). Liver anomalies in dab Limanda limanda, from the southern North Sea, with special consideration given to neoplastic lesions. Diseases of Aquatic Organisms 9, 171–85.CrossRefGoogle Scholar
Kranz, H. & Peters, N. (1985). Pathological conditions in the liver of ruffe, Gymnocephalus cernua (L.), from the Elbe estuary. Journal of Fish Diseases 8, 1324.CrossRefGoogle Scholar
Kurelec, B., Protic, M., Britvic, S., Kezic, N., Rijavec, M. & Zahn, R. K. (1981). Toxic effects in fish and the mutagenic capacity of water from the Sava River in Yugoslavia. Bulletin of Environmental Contamination and Toxicology 26, 179–87.CrossRefGoogle Scholar
Lappalainen, A., Rask, M. & Vuorinen, P. J. (1988). Acidification affects the perch, Perca fluviatilis, population in small lakes of southern Finland. Environmental Biology of Fishes 21, 232–9.CrossRefGoogle Scholar
Lauckner, G. (1983). Diseases of Mollusca: Bivalva. In Diseases of Marine Animals (ed. Kinne, O.), 13, pp. 477977. Helgoland, FRG: Biologische Anstalt.Google Scholar
Lindesjöö, E. & Thulin, J. (1990). Fin erosion of perch (Perca fluviatilis) and ruffe (Gymnocephalus cernua) in a pulp mill effluent. Diseases of Aquatic Organisms 8, 119–26.CrossRefGoogle Scholar
Lowe, J. (1874). Flora and fauna of Norfolk. IV. Fishes. Transactions of the Norfolk and Norwich Naturalists’ Society 1, 2156.Google Scholar
Mahoney, J. B., Midlidge, F. H. & Deuel, D. G. (1973). A fin rot disease of marine and euryhaline fishes in the New York Bight. Transactions of the American Fisheries Society 102, 596605.2.0.CO;2>CrossRefGoogle Scholar
Malins, D. C. & Jensen, A. (1988). Aquatic toxicology toxic chemicals and aquatic life: research and management. Aquatic Toxicology 11, 444 pp.Google Scholar
Malins, D. C., Mccain, B. B., Landahl, J. T., Myers, M. S., Krahn, M. M., Brown, D. W., Chan, S.-L. & Robal, W. T. (1988). Neoplastic and other diseases in fish in relation to toxic chemicals: an overview. Aquatic Toxicology, 11, 4367.CrossRefGoogle Scholar
Malins, D. C., Mccain, B. B., Myers, M. S., Brown, D. W., Krahn, M. M., Ronbal, W. T., Schweiewe, M. H., Landahl, J. J. & Chan, S.-L. (1987). Field and laboratory studies of the ecology of liver neoplasms in marine fish from Puget Sound. Environmental Health Prospects 71, 516.CrossRefGoogle Scholar
Mawdesley-THOMAS, L. E. (1975). Neoplasia in fish. In The Pathology of Fishes (ed. Ribelin, W. E. & Migaki, G.), pp. 805–70. Madison, USA: University of Wisconsin Press.Google Scholar
Mawdesley-THOMAS, L. E. & Bucke, D. (1967). Fish pox in the roach (Rutilus rutilus L.). Veterinary Record 81, 56.CrossRefGoogle ScholarPubMed
Meyers, T. R. & Hendricks, J. D. (1982). A summary of tissue lesions in aquatic animals induced by controlled exposure to environmental contaminants, chemotherapeutic agents and potential carcinogens. Marine Fisheries Review 44, 117.Google Scholar
Mix, M. C. (1986). Cancerous diseases in aquatic animals and their association with environmental pollutants: critical literature review. Marine Environmental Research 20, 1141.CrossRefGoogle Scholar
MÖller, H. (1981). Fish diseases in German and Danish waters in summer 1980. Meeresforschung 29, 116.Google Scholar
Myers, M. S., Rhodes, L. D. & Mccain, B. B. (1987). Pathologic anatomy and patterns of occurrence of hepatic neoplasms, putative preneoplastic lesions, and other idiopathic conditions in English sole (Parophrys vetulus) from Puget Sound, Washington. Journal of the National Cancer Institute 78, 333–63.Google Scholar
NSTF (1990). North Sea Task Force Monitoring Plan 1990-91. North Sea Environment Report (3), 37 pp. London: Department of the Environment.Google Scholar
Orton, J. H. (1924). An account of investigations into the cause or causes of the unusual mortality among oysters in English oyster beds during 1920 and 1921. Part 1. Report, MAFF, Fish Investigations 11 VI (3). 198 pp. London: HMSO.Google Scholar
Pauley, G. B. (1969). A critical review of neoplasia and tumor-like lesions in molluscs. National Cancer Institute Monograph 31, 509–29.Google Scholar
Pearce, J. B. & Depres-PATANGO, L. (1988). A review of monitoring strategies and assessments of estuarine pollution. Aquatic Toxicology 11, 323–43.CrossRefGoogle Scholar
Pentalow, F. T. K. (1955). Pollution and fisheries. Proceedings of the International Association of Theoretical and Applied Limnology XII, 768–71.Google Scholar
Perkins, E. J., Gilchrist, J. R. S. & Abbott, O. J. (1972). Incidence of epidermal lesions in fish of the north-east Irish Sea area 1971. Nature, London, 238, 101–3.CrossRefGoogle Scholar
Peters, N., Köhler, A. & Kranz, H. (1987). Liver pathology in fishes from the Lower Elbe as a consequence of pollution. Diseases of Aquatic Organisms 2, 8797.CrossRefGoogle Scholar
Poels, C. L. M., Van De Gaag, M. A. & Van De Kerkhoff, J. F. L. (1980). An investigation into the long-term effects of Rhine water on rainbow trout. Water Research 14, 1029–35.CrossRefGoogle Scholar
Reiger, H. A. & Meisner, J. D. (1990). Anticipated effects of climate change on freshwater fishes and their habitat. Fisheries 15, 1015.2.0.CO;2>CrossRefGoogle Scholar
Roberts, R. J. (1972). Ulcerative dermal necrosis (UDN) of salmon (Salmo salar L.). Symposium of the Zoological Society, London 30, 5381.Google Scholar
Roberts, R. J. (1975). The effects of temperature on diseases and their histopathological manifestations in fish. In The Pathology of Fishes (ed. Ribelin, W. E. & Migaki, G.), pp. 477–96. Madison, Wisconsin, USA: University of Wisconsin Press.Google Scholar
Roberts, R. J. & Bullock, A. M. (1976). The dermatology of marine teleost fish. II. Dermatopathology of the integument. Oceanography and Marine Biology 14, 227–46.Google Scholar
Ryan, P. M. & Harvey, H. H. (1980). Growth responses of yellow perch, Perca flavescens (Mitchill), to lake acidification in the La Cloche mountain lakes of Ontario. Environmental Biology and Fisheries 5, 97108.CrossRefGoogle Scholar
Schlumberger, H. G. & Lucre, B. (1948). Tumors of fishes, amphibians and reptiles. Cancer Research 8, 657754.Google ScholarPubMed
Selye, H. (1950). Stress and the general adaptation syndrome. British Medical Journal 1, 1383–92.CrossRefGoogle ScholarPubMed
Shelton, R. G. J. & Wilson, K. W. (1973). On the occurrence of lymphocystis, with notes on other pathological conditions, in the flatfish stocks of the north-east Irish Sea. Aquaculture 2, 395410.CrossRefGoogle Scholar
Sherwood, M. J. & Mearns, A. J. (1977). Environmental significance of fin erosion in southern Californian demersal fishes. Annals of the New York Academy of Sciences 298, 177–89.CrossRefGoogle Scholar
Sindermann, C. J. (1980). The use of pathological effects of pollutants in marine environmental monitoring programmes. In Biological Effects of Marine Pollution and the Problems of Monitoring (ed. Mclntyre, A. D. & Pearce, J), 179, pp. 129–34. Rapports et Procès Verbaux des Réunions - Conseil Permanent International pour i'Exploration de la Mer.Google Scholar
Sindermann, C. J. (1983). An examination of some relationships between pollution and disease. Rapport et Procès- Verbaux des Réunions. Commission Internationale pour l'exploration scientifique de la Mer Mediterraneé 182, 3743.Google Scholar
Sindermann, C. J. (1984). Fish and environmental impacts. Archiv für Fischereiwissenschaft 35, 125–60.Google Scholar
Sindermann, C. J. (1990). Pollution associated diseases of marine fish. In Principle Diseases of Marine Fish and Shellfish, 2nd edn, Vol. 1 (ed. Sindermann, C. J.), pp. 399450. San Diego and New York: Academic Press.Google Scholar
Slooff, W. (1983). A study on the usefulness of feral fish as indicators for the presence of chemical carcinogens in Dutch surface waters. Aquatic Toxicology 3, 127–39.CrossRefGoogle Scholar
Slooff, W. & Van Kreijl, C. F. (1982). Monitoring the rivers Rhine and Meuse in The Netherlands for mutagenic activity using the Ames test in combination with rat or fish liver homogenates. Aquatic Toxicology 2, 8998.CrossRefGoogle Scholar
Snieszko, S. F. (1974). The effects of environmental stress on outbreaks of infectious diseases of fish. Journal of Fish Biology 6, 197208.CrossRefGoogle Scholar
Solbé, J. F. (1973). The relation between water quality and the status of fish populations in Willow Brook. Water Treatment Examination, 22, 4161.Google Scholar
Squire, R. A. & Levitt, M. H. (1975). Report on a workshop on classification of specific hepatocellular lesions in rats. Cancer Research 35, 3214–23.Google ScholarPubMed
Sutcliffe, D. W. (1983). Acid precipitation and its effects on aquatic systems in the English Lake District (Cumbria). Report of the Freshwater Biological Association 51, 3062.Google Scholar
Tetlow, J. A. (1972). Pollution of the water. Medicine, Science and the Law 12, 94103.CrossRefGoogle ScholarPubMed
Vethaak, A. D. & Ap Rheinallt, T. (1992). Fish disease as a monitor for marine pollution: the case of the North Sea. Review of Fish Biology and Fisheries 2, 132.CrossRefGoogle Scholar
Waldock, M. J. & Thain, J. E. (1983). Shell thickening in Crassostrea gigas: organotin antifouling or sediment induced? Marine Pollution Bulletin 24, 789–90.Google Scholar
Wedemeyer, G. A. & Goodyear, C. P. (1984). Diseases caused by environmental stressors. In Diseases of Marine Animals, Vol. iv, Part 1, Introduction: Pisces (ed. Kinne, O.), pp. 424–34. Helgoland, Germany: Biologische Anstalt.Google Scholar
Wellings, S. R., Alpers, C. E., Mccain, B. B. & Miller, B. S. (1976). Fin erosion disease of starry flounder (Platichthys stellatus) and English sole (Parophrys vetulus) in the estuary of the Duwamish River, Seattle, Washington. Journal of the Fisheries Research Board of Canada 33, 2577–86.CrossRefGoogle Scholar
Winstead, J. T. & Couch, J. A. (1988). Enhancement of protozoan pathogen (Perkinsus marinus) infections in American oysters, Crassostrea virainica, exposed to the chemical carcinogen N-nitroso-diethylamine (DENA). Diseases of Aquatic Organisms 5, 205–13.CrossRefGoogle Scholar
Wootten, R., McVicar, A. H. & Smith, J. W. (1981). Some disease conditions of fish in Scottish waters. ICES CM/E 46, 4. Mimeo.Google Scholar