Hostname: page-component-745bb68f8f-f46jp Total loading time: 0 Render date: 2025-01-11T01:06:50.524Z Has data issue: false hasContentIssue false
  • English
  • Français

Marine parasites as pollution indicators: an update

Published online by Cambridge University Press:  10 November 2003

H. H. WILLIAMS  and
K. MACKENZIE
H. H. WILLIAMS
Affiliation:
Department of Ecology & Evolutionary Biology, University of Connecticut, 75 N. Eagleville Road, Storrs, USA 06269-3043 and School of Biosciences, Cardiff University, PO Box 915, Cardiff, CF10 3TL
K. MACKENZIE
Affiliation:
Department of Zoology, The University of Aberdeen, Tillydrone Avenue, Aberdeen, AB24 2TZ, UK
Get access Rights & Permissions [Opens in a new window]

Abstract

Eight major reviews are cited to indicate a recent knowledge explosion on the use of marine parasites as potential indicators of pollution. A literature update is given for the period 1995–2001. An analysis of the publications cited is used to provide 10 refined criteria for selecting parasites as indicator/monitor species. Previously unpublished data on Diclidophora merlangi and Dictyocotyle coeliaca confirm their value as potential indicators of hydrocarbon pollution in the North Sea. An extensive knowledge of D. merlangi is summarised to emphasize its potential value as an indicator species and also to encourage studies on the health status and immune responses of its host when subjected to pollutant stressors and infection with this monogenean. A discussion focuses on publications which have reported significant recent advances in this area of research and also on accompanying issues, problems and controversies. These selected publications are used to suggest species, stages in the development of species and assemblages of species worthy of further more detailed investigations into their value as indicators/monitors of pollution. It is predicted that further good progress will be made when contaminants can be accurately identified, their precise effects on both host and parasite can be measured by histochemical and biological methods and the roles of contaminants and parasites in causing disease can be assessed separately. About 100 references are cited.

Keywords

Parasitesindicatorsmarine pollution
Type
Research Article
Information
Parasitology , Volume 126 , Issue 7 , March 2003 , pp. S27 - S41
Copyright
© 2003 Cambridge University Press

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

ARME, C. & HALTON, D. W. (1972). Observations on the occurrence of Diclidophora merlangi (Trematoda: Monogenea) on the gills of whiting, Gadus merlangus. Journal of Fish Biology 4, 27–32.CrossRefGoogle Scholar
ARME, C. & WALKEY, M. (1970). The physiology of fish parasites. In Aspects of Fish Parasitology. Symposia of the British Society for Parasitology (ed. Taylor, A. E. R.) 8, pp. 79–101. Oxford & Edinburgh, Blackwell Scientific Publications.
ATTRILL, M. & POWER, M. (2002). Climatic influence on a marine fish assemblage. Nature, London 417, 275–278.CrossRefGoogle Scholar
BARKER, D. E., KHAN, R. A. & HOOPER, R. (1994). Bioindicators of stress in winter flounder, Pleuronectes americanus, captured adjacent to a pulp and paper mill in St. George's Bay, Newfoundland. Canadian Journal of Fisheries and Aquatic Sciences 51, 2203–2209.CrossRefGoogle Scholar
BERGEY, L., WEIS, J. S. & WEIS, P. (2002). Mercury uptake by the estuarine species Palaemonetes pugio and Fundulus heteroclitus compared with their parasites, Probopyrus pandalicola and Eustrongylides sp. Marine Pollution Bulletin 44, 1046–1050.CrossRefGoogle Scholar
BROEG, K., ZANDER, S., DIAMANT, A., KÖRTING, W., KRÜNER, G., PAPERNA, I. & WESTERNHAGEN, H. V. (1999). The use of fish metabolic, pathological and parasitological indices in pollution monitoring 1. North Sea. Helgoland Marine Research 53, 171–194.CrossRefGoogle Scholar
BROWNLEE, D. J. A., THORNDYKE, M. C., FAIRWEATHER, I. & JOHNSTON, C. F. (1995). Immunocytochemical demonstration of SALMFamide (S1)-like immunoreactivity in the nervous system of two marine platyhelminth parasites, Diclidophora merlangi and Grillotia erinaceus. Acta Biologica Hungarica 46, 205–209.Google Scholar
BUSH, A. O., LAFFERTY, K. D., LOTZ, J. M. & SHOSTAK, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 375–583.CrossRefGoogle Scholar
CHU, F. L. E. & HALE, R. C. (1994). Relationship between pollution and susceptibility to infectious disease in the Eastern oyster, Crassostrea virginica. Marine Environmental Research 38, 243–256.CrossRefGoogle Scholar
CHUBB, J. C. (1997). Fish parasites as indicators of environmental quality: a second perspective. Parassitologia 39, 255.Google Scholar
COLE, H. A. (1979). The assessment of sub-lethal effects of pollutants in the sea. Philosophical Transactions of the Royal Society of London (B) 286, 399–424.Google Scholar
CROSS, M. A., IRWIN, S. W. B. & FITZPATRICK, S. M. (2001). Effects of heavy metal pollution on swimming and longevity in cercariae of Cryptocotyle lingua (Digenea: Heterophyidae). Parasitology 123, 499–507.CrossRefGoogle Scholar
DAWES, B. (1947). The Trematoda of British Fishes. London, UK, Royal Society of London.CrossRef
DIAMANT, A., BANET, A., PAPERNA, I., WESTERNHAGEN, H. V., BROEG, K., KRUENER, G., KOERTING, W. & ZANDER, S. (1999). The use of fish metabolic, pathological and parasitological indices in pollution monitoring II. The Red Sea and Mediterranean. Helgoland Marine Research 53, 195–208.CrossRefGoogle Scholar
ELSTON, R. A., DRUM, A. S., PEARSON, W. H. & PARKER, K. (1997). Health and condition of Pacific herring Clupea pallasi from Prince William Sound, Alaska, 1994. Diseases of Aquatic Organisms 31, 109–126.CrossRefGoogle Scholar
GEORGE-NASCIMENTO, M., KHAN, R. A., GARCIAS, F., LOBOS, V., MUNOZ, G. & VALDEBENITO, V. (2000). Impaired health in Flounder, Paralichthys spp., inhabiting coastal Chile. Bulletin of Environmental Contamination and Toxicology 64, 184–190.CrossRefGoogle Scholar
GESAMP (1990). The State of the Marine Environment. UNEP Regional Reports and Studies No. 115. Nairobi.
HALTON, D. W. (1974). Hemoglobin absorption in the gut of a monogenetic trematode, Diclidophora merlangi. Journal of Parasitology 60, 59–66.CrossRefGoogle Scholar
HALTON, D. W. (1975). Intracellular digestion and cellular defecation in a monogenean, Diclidophora merlangi. Parasitology 70, 331–340.CrossRefGoogle Scholar
HALTON, D. W. (1976). Diclidophora merlangi. Sloughing and renewal of hematin cells. Experimental Parasitology 40, 41–47.Google Scholar
HALTON, D. W. (1979). The surface topography of a monogenean, Diclidophora merlangi, revealed by scanning electron microscopy. Zeitschrift für Parasitenkunde 61, 1–12.CrossRefGoogle Scholar
HALTON, D. W., BRENNAN, G. P., MAULE, A. G., SHAW, C., JOHNSTON, C. F. & FAIRWEATHER, I. (1991). The ultrastructure and immunogold labelling of pancreatic polypeptide-immunoreactive cells associated with the egg-forming apparatus of a monogenean parasite Diclidophora merlangi. Parasitology 102, 429–436.CrossRefGoogle Scholar
HALTON, D. W., DERMOTT, E. & MORRIS, G. P. (1968). Electron microscope studies of Diclidophora merlangi (Monogenea: Polyopisthocotylea). I. Ultrastructure of the cecal epithelium. Journal of Parasitology 54, 909–916.Google Scholar
HALTON, D. W. & HARDCASTLE, A. (1976). Spermatogenesis in a monogenean, Diclidophora merlangi. International Journal for Parasitology 6, 43–54.CrossRefGoogle Scholar
HALTON, D. W. & JENNINGS, J. B. (1965). Observations on the nutrition of monogenetic trematodes. Biological Bulletin 129, 257–272.CrossRefGoogle Scholar
HALTON, D. W., MAULE, A. G., MAIR, G. R. & SHAW, C. (1998). Monogenean neuromusculature: Some structural and functional correlates. International Journal for Parasitology 28, 1609–1623.CrossRefGoogle Scholar
HALTON, D. W. & MORRIS, G. P. (1975). Ultrastructure of the anterior alimentary tract of a monogenean, Diclidophora merlangi. International Journal for Parasitology 5, 407–420.CrossRefGoogle Scholar
HALTON, D. W., MORRIS, G. P. & HARDCASTLE, A. (1974). Gland cells associated with the alimentary tract of a monogenean, Diclidophora merlangi. International Journal for Parasitology 4, 589–599.CrossRefGoogle Scholar
HEMMINGSEN, W. & MACKENZIE, K. (2001). The parasite fauna of the Atlantic cod, Gadus morhua L. Advances in Marine Biology 40, 1–80.CrossRefGoogle Scholar
HOOLE, D. (1997). The effects of pollutants on the immune response of fish: implications for helminth parasites. Parassitologia 39, 219–225.Google Scholar
JOHNSTON, R. N., SHAW, C., BRENNAN, G. P., MAULE, A. G. & HALTON, D. W. (1995). Localisation, quantitation, and characterisation of neuropeptide F- and FMRF amide-immunoreactive peptides in turbellarians and a monogenean: A comparative study. Journal of Comparative Neurology 357, 76–84.CrossRefGoogle Scholar
KENNEDY, C. R. (1997). Freshwater fish parasites and environmental quality: an overview and caution. Parassitologia 39, 249–254.Google Scholar
KESTING, V. & ZANDER, C. D. (2000). Alteration of the metazoan parasite faunas in the brackish Schlei Fjord (Northern Germany, Baltic Sea). International Revue of Hydrobiology 85, 325–340.3.0.CO;2-9>CrossRefGoogle Scholar
KHAN, R. A. (1998 a). Parasites of fish as indicators of environmental stress. Proceedings of the IX International Congress of Parasitology, Makuhari Messe, Chiba, Japan, 24–28 August, 1998, pp. 313–318. Monduzzi Editore, International Proceedings Division, Bologna, Italy.
KHAN, R. A. (1998 b). Influence of petroleum at a refinery terminal on feral winter flounder, Pleuronectes americanus. Bulletin of Environmental Contamination and Toxicology 61, 770–777.Google Scholar
KHAN, R. A. (1999). Length-weight relationship, histopathology and parasitism as bioindicators of stress in winter flounder (Pleuronectes americanus) living near a PCB contaminated naval facility in Newfoundland. Canadian Journal of Zoology 77, 381–388.CrossRefGoogle Scholar
KHAN, R. A., BARKER, D. E., WILLIAMS-RYAN, K. & HOOPER, R. G. (1994). Influence of crude oil and pulp and paper mill effluent on mixed infections of Trichodina cottidarium and T. saintjohnsi (Ciliophora) parasitizing Myoxocephalus octodecemspinosus and M. scorpius. Canadian Journal of Zoology 72, 247–251.Google Scholar
KHAN, R. A. & PAYNE, J. F. (1997). A multidisciplinary approach using several biomarkers, including a parasite, as indicators of pollution: a case history from a paper mill in Newfoundland. Parassitologia 39, 183–188.Google Scholar
KHAN, R. A. & THULIN, J. (1991). Influence of pollution on parasites of aquatic animals. Advances in Parasitology 30, 201–238.CrossRefGoogle Scholar
KVACH, Yu. V. (2001). Ligula invasion of monkey goby (Neogobius fluviatilis) in some estuaries of north western Black Sea region. Vestnik Zoologii 35, 85–88.Google Scholar
LAFFERTY, K. D. (1997). Environmental parasitology: What can parasites tell us about human impacts on the environment? Parasitology Today 13, 251–255.Google Scholar
LAFFERTY, K. D. & KURIS, A. M. (1999). How environmental stress affects the impacts of parasites. Limnology and Oceanography 44, 925–931.CrossRefGoogle Scholar
LANDSBERG, J. H., BLAKESLEY, B. A., REESE, R. O., McRAE, G. & FORSTCHEN, P. R. (1998). Parasites of fish as indicators of environmental stress. Environmental Monitoring and Assessment 51, 211–232.CrossRefGoogle Scholar
LANG, T. (1990). Infestation of North Sea whiting (Merlangius merlangus L.) with externally visible parasites. ICES C.M.1990/E:31 Ref. G, 1–23.
LENIHAN, H. S., MICHELI, F., SHELTON, S. W. & PETERSON, C. H. (1999). The influence of multiple environmental stressors on susceptibility to parasites: An experimental determination with oysters. Limnology and Oceanography 44, 910–924.CrossRefGoogle Scholar
LLEWELLYN, J. (1954). Observations on the food and the gut pigment of the Polyopisthocotylea (Trematoda: Monogenea). Parasitology 44, 428–437.CrossRefGoogle Scholar
LLEWELLYN, J. (1956). The host-specificity, micro-ecology, adhesive attitudes, and comparative morphology of some trematode gill parasites. Journal of the Marine Biological Association of the United Kingdom 35, 113–127.CrossRefGoogle Scholar
LLEWELLYN, J. (1958). The adhesive mechanisms of monogenetic trematodes: the attachment of species of the Diclidophoridae to the gills of gadoid fishes. Journal of the Marine Biological Association of the United Kingdom 37, 67–79.CrossRefGoogle Scholar
LLEWELLYN, J. (1972). Behaviour of monogeneans. In Behavioural Aspects of Parasite Transmission (ed. Canning, E. U. & Wright, C. A.). Zoological Journal of the Linnean Society 51, 19–30.
LLEWELLYN, J., GREEN, J. E. & KEARN, G. C. (1984). A check-list of monogenean (Platyhelminth) parasites of Plymouth hosts. Journal of the Marine Biological Association of the United Kingdom 64, 881–887.CrossRefGoogle Scholar
LLEWELLYN, J. & TULLY, C. M. (1969). A comparison of speciation in diclidophorinean monogenean gill parasites and in their fish hosts. Journal of the Fisheries Research Board of Canada 26, 1063–1074.CrossRefGoogle Scholar
MACDONALD, S. (1975). Hatching rhythms in three species of Diclidophora (Monogenea) with observations on host behaviour. Parasitology 71, 211–228.CrossRefGoogle Scholar
MACDONALD, S. & CALEY, J. (1975). Sexual reproduction in the monogenean Diclidophora merlangi: Tissue penetration by sperms. Zeitschrift für Parasitenkunde 45, 323–334.CrossRefGoogle Scholar
MACHKEVSKY, V. K. & GAEVSKAYA, A. V. (1997). Response of some parasite systems from the Black Sea coastal zone to aquatic pollution. Ekologiya Morya 46, 51–57.Google Scholar
MACKENZIE, K. (1999). Parasites as pollution indicators in marine ecosystems: a proposed early warning system. Marine Pollution Bulletin 38, 955–959.CrossRefGoogle Scholar
MACKENZIE, K., WILLIAMS, H. H., WILLIAMS, B., McVICAR, A. H. & SIDDALL, R. (1995). Parasites as indicators of water quality and the potential use of helminth transmission in marine pollution studies. Advances in Parasitology 35, 85–144.CrossRefGoogle Scholar
MAIR, G. R., MAULE, A. G., HALTON, D. W., ORR, D., JOHNSTON, R. N. & JOHNSTON, C. F. (1997). Comparative analysis of the distribution of bradykinin-, GYIRamide- and neuropeptide F-like immunoreactivities in the monogenean, Diclidophora merlangi. Parasitology 114, 467–473.CrossRefGoogle Scholar
MAIR, G. R., MAULE, A. G., SHAW, C. & HALTON, D. W. (1998). Muscling in on parasitic flatworms. Parasitology Today 14, 73–76.CrossRefGoogle Scholar
MARCOGLIESE, D. J. (2001). Implications of climate change for parasitism of animals in the aquatic environment. Canadian Journal of Zoology 79, 1331–1352.CrossRefGoogle Scholar
MARCOGLIESE, D. J. & CONE, D. K. (1997). Parasite communities as indicators of ecosystem stress. Parassitologia 39, 227–232.Google Scholar
MARCOGLIESE, D. J., NAGLER, J. J. & CYR, D. G. (1998). Effects of exposure to contaminated sediments on the parasite fauna of American plaice (Hippoglossoides platessoides). Bulletin of Environmental Contamination and Toxicology 61, 88–95.CrossRefGoogle Scholar
MAULE, A. G., SHAW, C., HALTON, D. W., JOHNSTON, C. F. & FAIRWEATHER, I. (1989 a). Localization, quantification, and characterization of pancreatic polypeptide immunoreactivity in the parasitic flatworm Diclidophora merlangi and its fish host (Merlangius merlangus). General and Comparative Endocrinology 74, 50–56.Google Scholar
MAULE, A. G., SHAW, C., HALTON, D. W., JOHNSTON, C. F. & FAIRWEATHER, I. (1989 b). Tachykinin immunoreactivity in the parasitic flatworm Diclidophora merlangi and its fish host the whiting (Merlangius merlangus): radioimmunoassay and chromatographic characterisation using region-specific substance P and neurokinin A antisera. Comparative Biochemistry and Phsiology. C, Comparative Pharmacology and Toxicology 94, 533–541.Google Scholar
MAULE, A. G., HALTON, D. W., JOHNSTON, C. F., SHAW, C. & FAIRWEATHER, I. (1990 a). The serotoninergic, cholinergic and peptidergic components of the nervous system in the monogenean parasite, Diclidophora merlangi: a cytochemical study. Parasitology 100, 255–273.Google Scholar
MAULE, A. G., HALTON, D. W., JOHNSTON, C. F., SHAW, C. & FAIRWEATHER, I. (1990 b). A cytochemical study of the serotoninergic, cholinergic and peptidergic components of the reproductive system in the monogenean parasite, Diclidophora merlangi. Parasitology Research 76, 409–419.Google Scholar
MAULE, A. G., BRENNAN, G. P., HALTON, D. W., SHAW, C., JOHNSTON, C. F. & MOORE, S. (1992). Neuropeptidase F-immunoreactivity in the monogenean parasite Diclidophora merlangi. Parasitology Research 78, 655–660.CrossRefGoogle Scholar
McINTYRE, A. D. (1995 a). Environmental monitoring of the oceans. Marine Policy 19, 497–502.Google Scholar
McINTYRE, A. D. (1995 b). Human impact on the oceans: the 1990s and beyond. Marine Pollution Bulletin 31, 147–151.Google Scholar
McVICAR, A. H. (1997). The development of marine environmental monitoring using fish diseases. Parassitologia 39, 177–181.Google Scholar
MOLES, A. & WADE, T. L. (2001). Parasitism and phagocytic function among sand lance Ammodytes hexapterus Pallas exposed to crude oil-laden sediments. Bulletin of Environmental Contamination and Toxicology 66, 528–535.CrossRefGoogle Scholar
MØLLER, H. (1987). Pollution and parasitism in the aquatic environment. International Journal for Parasitology 17, 353–362.CrossRefGoogle Scholar
MONEYPENNY, C. G., MAULE, A. G., SHAW, C., DAY, T. A., PAX, R. A. & HALTON, D. W. (1997). Physiological effects of platyhelminth FMRFamide-related peptides (FaRPs) on the motility of the monogenean Diclidophora merlangi. Parasitology 115, 281–288.CrossRefGoogle Scholar
MORRIS, G. P. & HALTON, D. W. (1971). Electron microscope studies of Diclidophora merlangi (Monogenea: Polyopisthocotylea). II. Ultrastructure of the tegument. Journal of Parasitology 57, 49–61.Google Scholar
NORTH SEA TASK FORCE (1993). North Sea Quality Status Report 1993. Oslo and Paris Commissions, London.
OVERSTREET, R. M. (1997). Parasitological data as monitors of environmental health. Parassitologia 39, 169–175.Google Scholar
OVERSTREET, R. M. (1999). Fish protozoans as indicators of pollution. 5th International Symposium on Fish Parasites, České Budějovice, Czech Republic, 9–13 August, 1999. Book of Abstracts, 102.Google Scholar
PALM, H. & DOBBERSTEIN, R. C. (1999). Occurrence of trichodinid ciliates (Peritricha: Urceolariidae) in the Kiel Fjord, Baltic Sea, and its possible use as a biological indicator. Parasitology Research 85, 726–732.CrossRefGoogle Scholar
PILCHER, M. W., WHITFIELD, P. J. & RILEY, J. D. (1989). Seasonal and regional infestation characteristics of three ectoparasites of whiting, Merlangius merlangus L., in the North Sea. Journal of Fish Biology 35, 97–110.Google Scholar
POWELL, E. N., BARBER, R. D., KENNICUTT, M. C. & FORD, S. E. (1999). Influence of parasitism in controlling the health, reproduction and PAH body burden of petroleum seep mussels. Deep Sea Research Part I–Oceanographic Research Papers 46, 2053–2078.CrossRefGoogle Scholar
REIMER, L. W. (1995). Parasites especially of piscean hosts as indicators of the eutrophication in the Baltic Sea. Applied Parasitology 36, 124–135.Google Scholar
RUBEC, L. A. & DRONEN, N. O. (1994). Revision of the genus Diclidophora Krøyer (Monogenea: Diclidophoridae), with the proposal of Macrouridophora. Systematic Parasitology 28, 159–185.CrossRefGoogle Scholar
RUIVO, M., SAHRHAGE, D., ANDREN, L., ANGELESCU, L. V. & TOMCZAK, G. (eds.) (1972). Marine Pollution and Sea Life. Fishing News Book Ltd. West Byfleet, Surrey, by arrangement with FAO.
SALOMONS, W., BAYNE, B. L., DUURSMA, E. K. & FÖRSTNER, U. (1988). Pollution of the North Sea. An Assessment. Berlin, Springer-Verlag.CrossRef
SHOTTER, R. A. (1972). Notes on helminth parasites of the whiting, Odontogadus merlangus (L.) from the northern Irish Sea. Journal of Fish Biology 4, 117–130.Google Scholar
SHOTTER, R. A. (1973 a). A comparison of the parasite fauna of young whiting, Odontogadus merlangus (L.) (Gadidae) from an inshore and an offshore location off the Isle of Man. Journal of Fish Biology 5, 185–195.Google Scholar
SHOTTER, R. A. (1973 b). Changes in the parasite fauna of whiting, Odontogadus merlangus (L.), with age and sex of host, season, and from different areas in the vicinity of the Isle of Man. Journal of Fish Biology 5, 559–573.Google Scholar
SIDDALL, R., PIKE, A. W. & McVICAR, A. H. (1994). Parasites of flatfish in relation to sewage sludge dumping. Journal of Fish Biology 45, 193–209.CrossRefGoogle Scholar
SMART, D., JOHNSTON, C. F., MAULE, A. G., HALTON, D. W., HRCKOVA, G., SHAW, C. & BUCHANAN, K. D. (1995). Localization of Diploptera punctata allatostatin-like immunoreactivity in helminths: An immunocytochemical study. Parasitology 110, 87–96.CrossRefGoogle Scholar
SMITH, J. W. (1969). The distribution of one monogenean and two copepod parasites of whiting, Merlangius merlangus (L.) caught in British waters. Nytt Magasin for Zoologi 17, 58–63.Google Scholar
SMYTH, J. D. & HALTON, D. W. (1983). The Physiology of Trematodes. Cambridge, Cambridge University Press.
SURES, B., SIDDALL, R. & TARASCHEWSKI, H. (1999). Parasites as accumulation indicators of heavy metal pollution. Parasitology Today 15, 16–21.CrossRefGoogle Scholar
TKACHUK, L. P & MORDVINOVA, T. N. (1999). On parasitic infection of the shrimp, Palaemon elegans, from two coastal regions of the Black Sea. Ekologiya Morya 49, 21–23.Google Scholar
VETHAAK, A. D. & RHEINALLT, T. AP. (1992). Fish disease as a monitor for marine pollution: the case of the North Sea. Reviews in Fish Biology and Fisheries 2, 1–32.CrossRefGoogle Scholar
WHITE, H. H. (ed.) (1984). Concepts in Marine Pollution Measurements. A Maryland Sea Grant Publication, University of Maryland, U.S.A.
WILLIAMS, H. H. (1961). Observations on Echeneibothrium maculatum (Cestoda: Tetraphyllidea). Journal of the Marine Biological Association UK 41, 631–652.CrossRefGoogle Scholar
WILLIAMS, H. H. (1965). Observations on the occurrence of Dictyocotyle coeliaca and Calicotyle kroyeri (Trematoda: Monogenea). Parasitology 55, 201–207.CrossRefGoogle Scholar
WILLIAMS, H. H. & JONES, A. (1994). Parasitic Worms of Fish. London, Taylor & Francis.CrossRef
WILLIAMS, H. H. & MACKENZIE, K. (1995). Is Diclidophora merlangi (Platyhelminthes: Monogenea) a good sentinel of water quality in the North Sea? In Program and Abstracts of the IVth International Symposium of Fish Parasitology, Munich, October 3–7 1995 ( ed. R. W. Hoffmann), p. 14.
YEOMANS, W. E., CHUBB, J. C. & SWEETING, R. A. (1997). Use of protozoan communities for pollution monitoring. Parassitologia 39, 201–212.Google Scholar
YEOMANS, W. E., CHUBB, J. C., SWEETING, R. A., SOMMERVILLE, C., HARRIS, C. & OKAMURA, B. (1999). Trichodinids as indicators of organic pollution: the last word. 5th International Symposium on Fish Parasites, České Budějovice, Czech Republic, 9–13 August, 1999. Book of Abstracts, 166.Google Scholar
ZANDER, C. D. & KESTING, V. (1996). The indicator properties of parasite communities of gobies (Teleostei, Gobiidae) from Kiel and Lübeck Bight, SW Baltic Sea. Applied Parasitology 37, 186–204.Google Scholar