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Parasites as biological tags of marine, freshwater and anadromous fishes in North America from the tropics to the Arctic

Published online by Cambridge University Press:  10 March 2014

DAVID J. MARCOGLIESE*
Affiliation:
Aquatic Biodiversity Section, Watershed Hydrology and Ecology Research Division, Water Science and Technology Directorate, Science and Technology Branch, St Lawrence Centre, Environment Canada, 105 McGill, 7th floor, Montreal, Quebec H2Y 2E7, Canada
KYM C. JACOBSON
Affiliation:
Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, Newport, Oregon 97365, USA
*
* Corresponding author: Aquatic Biodiversity Section, Watershed Hydrology and Ecology Research Division, Water Science and Technology Directorate, Science and Technology Branch, St Lawrence Centre, Environment Canada, 105 McGill, 7th floor, Montreal, Quebec H2Y 2E7, Canada. E-mail: david.marcogliese@ec.gc.ca

Summary

Parasites have been considered as natural biological tags of marine fish populations in North America for almost 75 years. In the Northwest Atlantic, the most studied species include Atlantic cod (Gadus morhua), Atlantic herring (Clupea harengus) and the redfishes (Sebastes spp.). In the North Pacific, research has centred primarily on salmonids (Oncorhynchus spp.). However, parasites have been applied as tags for numerous other pelagic and demersal species on both the Atlantic and Pacific coasts. Relatively few studies have been undertaken in the Arctic, and these were designed to discriminate anadromous and resident salmonids (Salvelinus spp.). Although rarely applied in fresh waters, parasites have been used to delineate certain fish stocks within the Great Lakes-St Lawrence River basin. Anisakid nematodes and the copepod Sphyrion lumpi frequently prove useful indicators in the Northwest Atlantic, while myxozoan parasites prove very effective on the coast and open seas of the Pacific Ocean. Relative differences in the ability of parasites to discriminate between fish stocks on the Pacific and Atlantic coasts may be due to oceanographic and bathymetric differences between regions. Molecular techniques used to differentiate populations and species of parasites show promise in future applications in the field.

Type
Fisheries
Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Arthur, J. R. (1983). A Preliminary Analysis of the Discreteness of Stocks of Walleye Pollock (Theragra chalcogramma) from the Northeastern Pacific Ocean off Canada Based on their Parasites. Canadian Technical Report of Fisheries and Aquatic Sciences, No. 1184, Ottawa, Canada.Google Scholar
Arthur, J. R. (1984). A survey of the parasites of walleye pollock (Theragra chalcogramma) from the northeastern Pacific Ocean off Canada and a zoogeographical analysis of the parasite fauna of this fish throughout its range. Canadian Journal of Zoology 62, 675684. doi: 10.1139/z84-099.Google Scholar
Arthur, J. R. (1997). Recent advances in the use of parasites as biological tags for marine fish. In Diseases in Asian Aquaculture III (ed. Flegel, T. W. and MacRae, I. H.), pp. 141154. Fish Health Section, Asian Fisheries Society, Manila, the Philippines.Google Scholar
Arthur, J. R. and Albert, E. (1993). Use of parasites for separating stocks of Greenland halibut (Reinhardtius hippoglossoides) in the Canadian Northwest Atlantic. Canadian Journal of Fisheries and Aquatic Sciences 50, 21752181. doi: 10.1139/f93-243.Google Scholar
Arthur, J. R. and Albert, E. (1994). A survey of the parasites of Greenland halibut (Reinhardtius hippoglossoides) caught off Atlantic Canada, with notes on their zoogeography in this fish. Canadian Journal of Zoology 72, 765778. doi: 10.1139/z94-103.Google Scholar
Arthur, J. R. and Albert, E. (1996). Parasites as Potential Biological Tags for Capelin (Mallotus villosus) in the St. Lawrence Estuary and Gulf. Canadian Technical Report of Fisheries and Aquatic Sciences, No. 2112, Ottawa, Canada.Google Scholar
Arthur, J. R. and Arai, H. P. (1980). Studies on the parasites of Pacific herring (Clupea harengus pallasi Valenciennes): a preliminary evaluation of parasites as indicators of geographical origin for spawning herring. Canadian Journal of Zoology 58, 521527. doi: 10.1139/z80-072.Google Scholar
Arthur, J. R., Albert, E. and Boily, F. (1995). Parasites of capelin (Mallotus villosus) in the St. Lawrence estuary and gulf. Canadian Journal of Fisheries and Aquatic Sciences 52, 246253.Google Scholar
Bailey, R. E., Margolis, L. and Groot, C. (1988). Estimating stock composition of migrating juvenile Fraser River (British Columbia) sockeye salmon, Oncorhynchus nerka, using parasites as natural tags. Canadian Journal of Fisheries and Aquatic Sciences 45, 586591. doi: 10.1139/f88-071.Google Scholar
Bailey, R. E., Margolis, L. and Workman, G. D. (1989). Survival of certain naturally acquired freshwater parasites of juvenile sockeye salmon, Oncorhynchus nerka (Walbaum), in hosts held in fresh and sea water, and implications for their use as population tags. Canadian Journal of Zoology 67, 17571766. doi: 10.1139/z89-252.CrossRefGoogle Scholar
Bakay, Y. I. (1988). Application of Results from Parasitological Investigations in Redfish (Sebastes mentella Travin) Populational Structure. ICES CM Documents No. G:35.Google Scholar
Baker, T. G., Morand, S., Wenner, C. A., Roumillat, W. A. and de Buron, I. (2007). Stock identification of the sciaenid fish Micropogonias undulatus in the western North Atlantic Ocean using parasites as biological tags. Journal of Helminthology 81, 155167. doi: 10.1017/S0022149X07753920.Google Scholar
Baldwin, R. E., Rew, M. B., Johansson, M. L., Banks, M. A. and Jacobson, K. C. (2011). Population structure of three species of Anisakis nematodes recovered from Pacific sardines (Sardinops sagax) distributed throughout the California Current System. Journal of Parasitology 97, 545554. doi: 10.1645/GE-2690.1.CrossRefGoogle ScholarPubMed
Baldwin, R. E., Banks, M. A. and Jacobson, K. C. (2012). Integrating fish and parasite data as a holistic solution for identifying the elusive stock structure of Pacific sardines (Sardinops sagax). Reviews in Fish Biology and Fisheries 22, 137156. doi: 10.1007/s11160-011-9227-5.Google Scholar
Barse, A. M. and Hocutt, C. M. (1990). White marlin parasites: potential indicators of stock separations, seasonal migrations, and feeding habits. In Proceedings of the Second International Billfish Symposium, Kailua-Kona, Hawaii, August 1–5, 1988. Part 2: Contributed Papers, pp. 4149. National Coalition for Marine Conservation, Inc.Google Scholar
Beacham, T. D., Margolis, L. and Nelson, R. J. (1998). A comparison of methods of stock identification for sockeye salmon (Oncorhynchus nerka) in Barkley Sound, British Columbia. North Pacific Anadromous Fish Commission Bulletin 1, 227239.Google Scholar
Begg, G. A. and Waldman, J. R. (1999). An holistic approach to fish stock identification. Fisheries Research 43, 3544. doi: 10.1016/S0165-7836(99)00065-X.Google Scholar
Bentzen, P., Taggart, C. T., Ruzzante, D. E. and Cook, D. (1996). Microsatellite polymorphism and the population structure of Atlantic cod (Gadus morhua) in the Northwest Atlantic. Canadian Journal of Fisheries and Aquatic Sciences 53, 27062721. doi: 10.1139/f96-238.Google Scholar
Bertrand, M., Marcogliese, D. J. and Magnan, P. (2008). Trophic polymorphism in brook charr revealed by diet, parasites and morphometrics. Journal of Fish Biology 72, 555572. doi: 10.1111/j.1095-8649.2007.01720.x.Google Scholar
Beverley-Burton, M. (1978). Population genetics of Anisakis simplex (Nematoda: Ascaridoidea) in Atlantic salmon (Salmo salar) and their use as biological indicators of host stocks. Environmental Biology of Fishes 3, 369377. doi: 10.1007/BF00000529.Google Scholar
Beverley-Burton, M. and Pippy, J. H. C. (1977). Morphometric variations among larval Anisakis simplex (Nematoda: Ascaridoidea) from fishes of the North Atlantic and their use as biological indicators of host stocks. Environmental Biology of Fishes 2, 309314.CrossRefGoogle Scholar
Beverley-Burton, M. and Pippy, J. H. C. (1978). Distribution, prevalence and mean intensity of larval Anisakis simplex (Nematoda: Ascaridoidea) in Atlantic salmon Salmo salar L. and their use as biological indicators of host stocks. Environmental Biology of Fishes 3, 211222.CrossRefGoogle Scholar
Bishop, C. A., Lear, W. H., Baird, J. W. and Wells, R. (1988). Comparison of Cod Samples from St. Pierre Bank, Burgeo Bank and Rose Blanche Bank from Analysis of Meristic Characters, Average Length at Age, and Prevalence of Parasitic Nematodes. Northwest Atlantic Fisheries Organization SCR Document No. 8/70.Google Scholar
Black, G. A., Montgomery, W. L. and Whoriskey, F. G. (1983). Abundance and distribution of Salmincola edwardsii (Copepoda) on anadromous brook trout, Salvelinus fontinalis (Mitchell), in the Moisie River system, Quebec. Journal of Fish Biology 22, 567575. doi: 10.1111/j.1095-8649.1983.tb04216.x.CrossRefGoogle Scholar
Black, G. W. (1981). Metazoan parasites as indicators of movements of anadromous brook charr (Salvelinus fontinalis) to sea. Canadian Journal of Zoology 59, 18921896. doi: 10.1139/z81-257.Google Scholar
Blanar, C. A., Marcogliese, D. J. and Couillard, C. M. (2011). Natural and anthropogenic factors shape metazoan parasite community structure in mummichog (Fundulus heteroclitus) from two estuaries in New Brunswick, Canada. Folia Parasitologica 58, 240248.CrossRefGoogle ScholarPubMed
Blasco-Costa, I. and Poulin, R. (2013). Host traits explain the genetic structure of parasites: a meta-analysis. Parasitology 140, 13161322. doi: 10.1017/S0031182013000784.CrossRefGoogle ScholarPubMed
Blaylock, R. B., Margolis, L. and Holmes, J. C. (2003). The use of parasites in discriminating stocks of the Pacific halibut (Hippoglossus stenolepis) in the Northeast Pacific. Fishery Bulletin 101, 19.Google Scholar
Boje, J. (1987). Parasites as Natural Tags on Cod in Greenland Waters. ICES Demersal Fish Committee No. C.M. 1987/G:64.Google Scholar
Boje, J., Riget, F. and Koie, M. (1997). Helminth parasites as biological tags in population studies of Greenland halibut (Reinhardtius hippoglossoides (Walbaum)), in the North-west Atlantic. ICES Journal of Marine Science 54, 886895. doi: 10.1006/jmsc.1997.0214.Google Scholar
Bouillon, D. R. and Dempson, J. B. (1989). Metazoan parasite infections in landlocked and anadromous Arctic charr (Salvelinus alpinus Linnaeus), and their use as indicators of movement to sea in young anadromous charr. Canadian Journal of Zoology 67, 24782485. doi: 10.1139/z89-350.Google Scholar
Bourgeois, C. E. and Ni, I.-H. (1984). Metazoan parasites of northwest Atlantic redfishes (Sebastes spp.). Canadian Journal of Zoology 62, 18791885. doi: 10.1139/z84-274.Google Scholar
Bowen, C. A. II and Stedman, R. M. (1990). Host-parasite relationships and geographic distribution of Salmincola corpulentus (Copepoda: Lernaeopodidae) on bloater (Coregonus hoyi) stocks in Lake Huron. Canadian Journal of Zoology 68, 19881994. doi: 10.1139/z90-280.Google Scholar
Bowen, W. D. (1990). General introduction. In Population Biology of Sealworm (Pseudoterranova decipiens) in Relation to its Intermediate and Seal Hosts (ed. Bowen, W. D.), pp. viiviii. Canadian Bulletin of Fisheries and Aquatic Sciences, No. 222, Ottawa, Canada.Google Scholar
Bower, S. M. and Margolis, L. (1991). Potential use of helminth parasites in stock identification of flying squid, Ommastrephes bartrami, in North Pacific waters. Canadian Journal of Zoology 69, 11241126. doi: 10.1139/z91-158.Google Scholar
Boyar, H. C. and Perkins, F. E. (1971). The Occurrence of a Larval Nematode (Anisakis sp.) in Adult Herring from ICNAF Subareas 4 and 5, 1962–1969. International Commission for the Northwest Atlantic Fisheries, Research Bulletin, No. 71/99.Google Scholar
Bradford, R. G. and Iles, T. D. (1992). Unique biological characteristics of spring-spawning herring (Clupea harengus L.) in Minas Basin, Nova Scotia, a tidally dynamic environment. Canadian Journal of Zoology 70, 641648. doi: 10.1139/z92-096.CrossRefGoogle Scholar
Brattey, J. and Bishop, C. A. (1992). Larval Anisakis simplex (Nematoda: Ascaridoidea) infection in the musculature of Atlantic cod, Gadus morhua, from Newfoundland and Labrador. Canadian Journal of Fisheries and Aquatic Sciences 49, 26352647. doi: 10.1139/f92-292.Google Scholar
Brattey, J. and Campbell, A. (1986). A survey of parasites of the American lobster, Homarus americanus (Crustacea: Decapoda), from the Canadian Maritimes. Canadian Journal of Zoology 64, 19982003. doi: 10.1139/z86-301.Google Scholar
Brattey, J., Bishop, C. A. and Myers, R. A. (1990). Geographic distribution and abundance of Pseudoterranova decipiens (Nematoda: Ascaridoidea) in the musculature of Atlantic cod, Gadus morhua, from Newfoundland and Labrador. In Population Biology of the Sealworm (Pseudoterranova decipiens) in Relation to its Intermediate and Seal Hosts (ed. Bowen, W. D.), pp. 6782. Canadian Bulletin of Fisheries and Aquatic Sciences, No. 222.Google Scholar
Burgner, R. L. (1992). Review of high seas salmonid research by the United States. In Proceedings of the International Workshop on Future Salmon Research in the North Pacific Ocean. Special Publication of the National Research Institute of Far Seas Fisheries (ed. Ishida, Y., Nagasawa, K., Welch, D. W., Myers, K. M. and Shershnev, A. P.), pp. 1117. Shimizu, Japan, No. 20.Google Scholar
Burn, P. R. (1980). Pollution effects on fish parasites. Coastal Ocean Pollution Assessment News 1, 34.Google Scholar
Castro-Pampillón, J. A., Soto-Búa, M., Rodríguez-Domínguez, H., Mejuto-García, J., Arias-Fernández, C. and García-Estévez, J. M. (2002). Selecting parasites for use in biological tagging of the Atlantic swordfish (Xiphias gladius). Fisheries Research 59, 259262. doi: http://dx.doi.org/10.1016/S0165-7836(02)00008-5.CrossRefGoogle Scholar
Catalano, S. R., Whittington, I. D., Donnellan, S. C. and Gillanders, B. M. (2013). Parasites as biological tags to assess host population structure: guidelines, 5 recent genetic advances and comments on a holistic approach. International Journal for Parasitology: Parasites and Wildlife (Epub ahead of print). doi: http://dx.doi.org/10.1016/j.ijppaw.2013.11.001.Google Scholar
Chenoweth, J. F., McGladdery, S. E., Sindermann, C. J., Sawyer, T. K. and Bier, J. W. (1986). An investigation into the usefulness of parasites as tags for herring (Clupea harengus) stocks in the western North Atlantic, with emphasis on use of the larval nematode Anisakis simplex . Journal of Northwest Atlantic Fisheries Science 7, 2533.Google Scholar
Criscione, C. D., Cooper, B. and Blouin, M. S. (2006). Parasite genotypes identify source populations of migratory fish more accurately than fish genotypes. Ecology 87, 823828. doi: 10.1890/0012-9658(2006)87[823:PGISPO]2.0.CO;2.Google Scholar
Dalton, T. J. (1991). Variation in prevalence of Nanophyetus salmincola, a parasite tag indicating U.S. Northwest origin, in steelhead trout (Oncorhynchus mykiss) caught in the central North Pacific Ocean. Canadian Journal of Fisheries and Aquatic Sciences 48, 11041108. doi: 10.1139/f91-131.CrossRefGoogle Scholar
Dick, T. A. (1984). Parasites and Arctic charr management – an academic curiosity or practical reality? In Biology of the Arctic charr, Proceedings of the International Symposium on Arctic Charr (ed. Johnson, L. and Burns, B. L.), pp. 371394. University of Manitoba Press, Winnipeg, Canada.Google Scholar
Dick, T. A. and Belosevic, M. (1981). Parasites of Arctic charr Salvelinus alpinus (Linnaeus) and their use in separating sea-run and non-migrating charr. Journal of Fish Biology 18, 339347. doi: 10.1111/j.1095-8649.1981.tb03775.x.Google Scholar
Due, T. T. and Curtis, M. A. (1995). Parasites of freshwater resident and anadromous Arctic charr (Salvelinus alpinus) in Greenland. Journal of Fish Biology 46, 578592. doi: 10.1111/j.1095-8649.1995.tb01098.x.Google Scholar
Eddy, S. B. and Lankester, M. W. (1978). Feeding and migratory habits of Arctic char, Salvelinus alpinus, indicated by the presence of the swimbladder nematode Cystidicola cristovomeri White. Journal of the Fisheries Research Board of Canada 35, 14881491. doi: 10.1139/f78-234.Google Scholar
Fréchet, A., Dodson, J. J. and Powles, H. (1983). The parasites of the American anadromous smelt (Osmerus mordax) of Québec and their usefulness as biological markers. Canadian Journal of Zoology 61, 621626. doi: 10.1139/z83-083.Google Scholar
Frimeth, J. P. (1987). Potential use of certain parasites of brook charr (Salvelinus fontinalis) as biological indicators in the Tabusintac River, New Brunswick, Canada. Canadian Journal of Zoology 65, 19891995. doi: 10.1139/z87-303.Google Scholar
Groot, C., Bailey, R. E., Margolis, L. and Cooke, K. (1989). Migratory patterns of sockeye salmon (Oncorhynchus nerka) smolts in the Strait of Georgia, British Columbia, as determined by analysis of parasite assemblages. Canadian Journal of Zoology 67, 16701678. doi: 10.1139/z89-240.Google Scholar
Hare, G. M. and Burt, M. D. B. (1976). Parasites as potential biological tags of Atlantic salmon (Salmo salar) smolts in the Miramichi River system, New Brunswick. Journal of the Fisheries Research Board of Canada 33, 11391143. doi: 10.1139/f76-142.Google Scholar
Herrington, W. C., Bearse, H. M. and Firth, F. E. (1939). Observations on the life history, occurrence and distribution of the redfish parasite Sphyrion lumpi . US Bureau of Fisheries Special Report 5, 118.Google Scholar
Hoff, M. H., Pronin, N. M. and Baldanova, D. R. (1997). Parasites of lake herring (Coregonus artedi) from Lake Superior, with special reference to the use of parasites as markers of stock structure. Journal of Great Lakes Research 23, 458467.CrossRefGoogle Scholar
Hogans, W. E. and Brattey, J. (1982). Parasites of the Gills and Gastrointestinal Tracts of Swordfish (Xiphias gladius) from the Northwest Atlantic Ocean, with an Assessment of their Use as Biological Tags. Final report. St. Andrews, New Brunswick, Fundy Isles Marine Enterprises, Ltd.Google Scholar
Hogans, W. E., Dadswell, M. J., Uhazy, L. S. and Appy, R. G. (1993). Parasites of American shad, Alosa sapidissima (Osteichthyes: Clupeidae), from rivers of the North American Atlantic coast and the Bay of Fundy, Canada. Canadian Journal of Zoology 71, 941946. doi: 10.1139/z93-123.Google Scholar
Humphreys, R. L., Crossler, M. A. and Rowland, C. M. (1993). Use of a monogenean gill parasite and feasibility of condition indexes for identifying new recruits to a seamount population of armorhead Pseudopentaceros wheeleri (Pentacerotidae). Fishery Bulletin 91, 455463.Google Scholar
Jackson, R. I. and Royce, W. F. (1986). Ocean Forum; An Interpretative History of the International North Pacific Fisheries Commission. Fishing News Books Ltd., Farnham, UK.Google Scholar
Jennings, M. R. and Hendrickson, G. L. (1982). Parasites of Chinook salmon (Oncorhynchus tshawytscha) and coho salmon (O. kisutch) from the Mad River and vicinity, Humboldt County, California. Proceedings of the Helminthological Society of Washington 49, 279284.Google Scholar
Jones, M. E. B. and Taggart, C. T. (1998). Distribution of gill parasite (Lernaeocera branchialis) and parasite-induced host mortality: inferences from tagging data. Canadian Journal of Fisheries and Aquatic Sciences 55, 364375. doi: 10.1139/f97-209.Google Scholar
Kabata, Z. (1963). Parasites as biological tags. International Commission for the Northwest Atlantic Fisheries, Special Publication 4, 3137.Google Scholar
Kabata, Z., McFarlane, G. A. and Whitaker, D. J. (1988). Trematoda of sablefish, Anoplopoma fimbria (Pallas, 1811), as possible biological tags for stock identification. Canadian Journal of Zoology 66, 195200. doi: 10.1139/z88-027.Google Scholar
Khan, R. A. and Thulin, J. (1991). Influence of pollution on parasites of aquatic animals. Advances in Parasitology 30, 201238.Google Scholar
Khan, R. A. and Tuck, C. (1995). Parasites as biological indicators of stocks of Atlantic cod (Gadus morhua) off Newfoundland, Canada. Canadian Journal of Fisheries and Aquatic Sciences 52, 195201. doi: 10.1139/f95-527.Google Scholar
Khan, R. A., Murphy, J. and Taylor, D. (1980). Prevalence of a trypanosome in Atlantic cod (Gadus morhua) especially in relation to stocks in the Newfoundland area. Canadian Journal of Fisheries and Aquatic Sciences 37, 14671475. doi: 10.1139/f80-190.Google Scholar
Khan, R. A., Dawe, M., Bowering, R. and Misra, R. K. (1982). Blood protozoa as an aid for separating stocks of Greenland halibut, Reinhardtius hippoglossoides, in the Northwest Atlantic. Canadian Journal of Fisheries and Aquatic Sciences 39, 13171322. doi: 10.1139/f82-176.Google Scholar
Kilambi, R. V. and DeLacy, A. C. (1967). Heterogeneity of surf smelt, Hypomesus pretiosus (Girard), in the State of Washington, as judged by incidence of larval Anisakis (Nematoda). Journal of the Fisheries Research Board of Canada 24, 629633. doi: 10.1139/f67-054.Google Scholar
Krause, R. J., McLaughlin, J. D. and Marcogliese, D. J. (2010). Parasite fauna of Etheostoma nigrum (Percidae: Etheostomatinae) in localities of varying pollution stress in the St Lawrence River, Quebec, Canada. Parasitology Research 107, 285294. doi: 10.1007/s00436-010-1862-6.Google Scholar
Landsberg, J. H., Blakesley, B. A., Reese, R. O., McRae, G. and Forstchen, P. R. (1998). Parasites of fish as indicators of environmental stress. Environmental Monitoring and Assessment 51, 211232.Google Scholar
Leaman, B. M. and Kabata, Z. (1987). Neobrachiella robusta (Wilson, 1912) (Copepoda: Lernaeopodidae) as a tag for identification of stocks of its host, Sebastes alutus (Gilbert, 1890) (Pisces: Teleostei). Canadian Journal of Zoology 65, 25792582. doi: 10.1139/z87-390.Google Scholar
Lee, E. M. and Khan, R. A. (2000). Length-weight-age relationships, food, and parasites of Atlantic cod (Gadus morhua) off coastal Labrador within NAFO Divisions 2H and 2J-3K. Fisheries Research 45, 6572. doi: 10.1016/S0165-7836(99)00101-0.CrossRefGoogle Scholar
Lubieniecki, B. (1973). Note on the occurrence of larval Anisakis in adult herring and mackerel from Long Island to Chesapeake Bay. International Commission for the Northwest Atlantic Fisheries, Research Bulletin 10, 7981.Google Scholar
Lux, F. E. (1963). Identification of New England yellowtail flounder groups. Fishery Bulletin 63, 110.Google Scholar
MacKenzie, K. (1987). Parasites as indicators of host populations. International Journal for Parasitology 17, 345352. doi: 10.1016/0020-7519(87)90109-3.Google Scholar
MacKenzie, K. (1993). Parasites as biological indicators. Bulletin of the Scandinavian Society of Parasitology 1, 110.Google Scholar
MacKenzie, K. and Abaunza, P. (1998). Parasites as biological tags for stock discrimination of marine fish: a guide to procedures and methods. Fisheries Research 38, 4556. doi: 10.1016/S0165-7836(98)00116-7.Google Scholar
MacKenzie, K., Williams, H. H., Williams, B., McVicar, A. H. and Siddall, R. (1995). Parasites as indicators of water quality and the potential use of helminth transmission in marine pollution studies. Advances in Parasitology 35, 85144.Google Scholar
Marcogliese, D. J. (2004). Parasites: small players with crucial roles in the ecological theatre. EcoHealth 1, 151164. doi: 10.1007/s10393-004-0028-3.Google Scholar
Marcogliese, D. J. (2005). Parasites of the superorganism: are they indicators of ecosystem health? International Journal for Parasitology 35, 705716. doi: 10.1016/j.ijpara.2005.01.015.Google Scholar
Marcogliese, D. J. (2008). Interdisciplinarity in marine parasitology. In Proceedings of the International Workshop on Marine Parasitology: Applied Aspects of Marine Parasitology (ed. Afonso-Dias, I., Menezes, G., MacKenzie, K. and Eiras, J. C.). Arquipélago 6 (Suppl.), 714.Google Scholar
Marcogliese, D. J., Dumont, P., Gendron, A. D., Mailhot, Y., Bergeron, E. and McLaughlin, J. D. (2001). Spatial and temporal variation in abundance of Diplostomum spp. in walleye (Stizostedion vitreum) and white suckers (Catostomus commersoni) from the St. Lawrence River. Canadian Journal of Zoology 79, 355369. doi: 10.1139/cjz-79-3-355.Google Scholar
Marcogliese, D. J., Albert, E., Gagnon, P. and Sévigny, J.-M. (2003). Use of parasites in stock identification of the deepwater redfish (Sebastes mentella) in the Northwest Atlantic. Fishery Bulletin 101, 183188.Google Scholar
Marcogliese, D. J., Gendron, A. D., Plante, C., Fournier, M. and Cyr, D. (2006). Parasites of spottail shiners (Notropis hudsonius) in the St. Lawrence River: effects of municipal effluents and habitat. Canadian Journal of Zoology 84, 14611481. doi: 10.1139/z06-088.Google Scholar
Marcogliese, D. J., Gendron, A. D. and Cone, D. K. (2009). Impact of municipal effluents and hydrological regime on myxozoan parasite communities of fish. International Journal for Parasitology 39, 13451351. doi: 10.1016/j.ijpara.2009.04.007.Google Scholar
Margolis, L. (1963). Parasites as indicators of the geographical origins of sockeye salmon, Oncorhynchus nerka (Walbaum), occurring in the North Pacific Ocean and adjacent seas. Bulletin, International North Pacific Fisheries Commission 11, 101156.Google Scholar
Margolis, L. (1982). Parasitology of Pacific salmon – an overview. In Aspects of Parasitology – a Festschrift Dedicated to the Fiftieth Anniversary of the Institute of Parasitology of McGill University, 1932–1982 (ed. Meerovitch, E.), pp. 135226. McGill University, Montreal, Canada.Google Scholar
Margolis, L. (1984). Preliminary Report on Identification of Continent of Origin of Ocean-Caught Steelhead Trout, Salmo gairdneri, using Naturally Occurring Parasite “Tags”. Department of Fisheries and Oceans, Fisheries Research Branch, Pacific Biological Station, Nanaimo, Canada (Unpublished Report).Google Scholar
Margolis, L. (1985). Continent of origin of steelhead, Salmo gairdneri, taken in the North Pacific Ocean in 1984, as determined by naturally occurring parasite “tags”. In Annual Meeting of the International North Pacific Fisheries Commission, Tokyo, Japan, October 1985.Google Scholar
Margolis, L. (1992). A brief history of Canadian research from 1955 to 1990 related to Pacific salmon (Oncorhynchus species) on the high seas. In Proceedings of the International Workshop on Future Salmon Research in the North Pacific Ocean (ed. Ishida, Y., Nagasawa, K., Welch, D. W., Myers, K. W. and Shershnev, A. P.), pp. 110. National Research Institute of Far Seas Fisheries, Shimizu, Japan.Google Scholar
Margolis, L. (1998). Are naturally-occurring parasite “tags” stable? An appraisal from four case histories involving Pacific salmonids. North Pacific Anadromous Fish Commission Bulletin 1, 205212.Google Scholar
Margolis, L. and Arthur, J. R. (1979). Synopsis of the Parasites of Fishes of Canada. Bulletin of the Fisheries Research Board of Canada, No. 199. Ottawa, Canada.Google Scholar
McClelland, G. and Marcogliese, D. J. (1994). Larval anisakine nematodes as biological indicators of cod (Gadus morhua) populations in the southern Gulf of St. Lawrence and on the Breton Shelf, Canada. Bulletin of the Scandinavian Society for Parasitology 4, 97116.Google Scholar
McClelland, G. and Melendy, J. (2007). Use of endoparasitic helminths as tags in delineating stocks of American plaice (Hippoglossoides platessoides) from the southern Gulf of St. Lawrence and Cape Breton Shelf. Fishery Bulletin 105, 180188.Google Scholar
McClelland, G. and Melendy, J. (2011). Use of parasites as tags in delineating stocks of Atlantic cod (Gadus morhua) from the southern Gulf of St. Lawrence and the Cape Breton Shelf. Fisheries Research 107, 233238. doi: 10.1016/j.fishres.2005.07.006.Google Scholar
McClelland, G., Misra, R. K. and Marcogliese, D. J. (1983). Variations in Abundance of Larval Anisakines, Sealworm (Phocanema decipiens) and Related Species in Cod and Flatfish from the Southern Gulf of St. Lawrence (4T) and the Breton Shelf (4Vn). Canadian Technical Report of Fisheries and Aquatic Sciences, No. 1210.Google Scholar
McClelland, G., Melendy, J., Osborne, J., Reid, D. and Douglas, S. (2005). Use of parasite and genetic markers in delineating populations of winter flounder from the central and south-west Scotian Shelf and north-east Gulf of Maine. Journal of Fish Biology 66, 10821100. doi: 10.1016/j.fishres.2005.07.006.Google Scholar
McDonald, T. E. and Margolis, L. (1995). Synopsis of the Parasites of Fishes of Canada: Supplement (1978–1993). Canadian Special Publication of Fisheries and Aquatic Sciences, No. 122. Ottawa, Canada.Google Scholar
McGladdery, S. E. (1987). Potential for Eimeria sardinae (Apicomplexa: Eimeridae) oocysts for distinguishing between spawning groups and between first- and repeat-spawning Atlantic herring (Clupea harengus harengus). Canadian Journal of Fisheries and Aquatic Sciences 44, 13791385. doi: 10.1139/f87-166.Google Scholar
McGladdery, S. E. and Burt, M. D. B. (1985). Potential of parasites for use as biological indicators of migration, feeding, and spawning behavior of northwestern Atlantic herring (Clupea harengus). Canadian Journal of Fisheries and Aquatic Sciences 42, 19571968. doi: 10.1139/f85-243.Google Scholar
Melendy, J., McClelland, G. and Hurlbut, T. (2005). Use of parasite tags in delineating stocks of white hake (Urophycis tenuis) from the southern Gulf of St. Lawrence and Cape Breton Shelf. Fisheries Research 76, 392400. doi: 10.1016/j.fishres.2005.07.006.Google Scholar
Moles, A. and Jensen, K. (2000). Prevalence of the sockeye salmon brain parasite Myxobolus arcticus in selected Alaska streams. Alaska Fishery Research Bulletin 6, 8593.Google Scholar
Moles, A., Rounds, P. and Kondzela, C. (1990). Use of the brain parasite Myxobolus neurobius in separating mixed stocks of sockeye salmon. American Fisheries Society Symposium 7, 224231.Google Scholar
Moles, A., Heifetz, J. and Love, D. C. (1998). Metazoan parasites as potential markers for selected Gulf of Alaska rockfishes. Fishery Bulletin 96, 912916.Google Scholar
Moran, J. D. W., Arthur, J. R. and Burt, M. D. B. (1996). Parasites of sharp-beaked redfishes (Sebastes fasciatus and Sebastes mentella) collected from the Gulf of St. Lawrence, Canada. Canadian Journal of Fisheries and Aquatic Sciences 53, 18211826. doi: 10.1139/cjfas-53-8-1821.Google Scholar
Moser, M. and Hsieh, J. (1992). Biological tags for stock separation in Pacific herring Clupea harengus pallasi in California. Journal of Parasitology 78, 5460. doi: 10.2307/3283685.Google Scholar
Muzzall, P. M. and Haas, R. C. (1998). Parasites of walleyes, Stizostedion vitreum, from Saginaw Bay, Lake Huron, and the other Great Lakes. Journal of Great Lakes Research 24, 152158.Google Scholar
Muzzall, P. M. and Whelan, G. E. (2011). Parasites of Fish from the Great Lakes: A Synopsis and Review of the Literature, 1871–2010. Great Lakes Fishery Commission, Ann Arbor, MI, USA.Google Scholar
Myers, K. W., Campbell, W. B. and Burgner, R. L. (1991). ParasiteTag Identification of U.S. Pacific Northwest Origin Steelhead Caught in the North Pacific Ocean in 1990. (INPFC Doc.) FRI-UW-9103. Fishersies Research Institute, University of Washington, Seattle, WA, USA.Google Scholar
Myers, K. W., Harris, C. K., Ishida, Y., Margolis, L. and Ogura, M. (1993). Review of the Japanese\Landbased Driftnet Salmon Fishery in the Western North Pacific Ocean and the Continent of Origin of Salmonids in this Area. International North Pacific Fisheries Commission Bulletin, No. 52.Google Scholar
Nagasawa, K., Mori, J. and Okamura, H. (1998). Parasites as biological tags of stocks of neon flying squid (Ommastrephes bartramii) in the North Pacific Ocean. In International Symposium on Large Pelagic Squids (ed. Okutani, T.), pp. 4964. Japan Marine Fishery Resources Research Center, Tokyo, Japan.Google Scholar
Nigrelli, R. F. and Firth, F. E. (1939). On Sphyrion lumpi (Kroyer), a copepod parasite on the redfish, Sebastes marinus (Linnaeus), with special reference to the host-parasite relationships. Zoologica 24, 110.Google Scholar
Nyman, O. L. and Pippy, J. H. C. (1972). Differences in Atlantic Salmon, Salmo salar, from North America and Europe. Journal of the Fisheries Research Board of Canada 29, 179185. doi: 10.1139/f72-029.Google Scholar
Olson, R. E. and Pratt, I. (1973). Parasites as indicators of English sole (Parophrys vetulus) nursery grounds. Transactions of the American Fisheries Society 102, 405411. doi: 10.1577/1548-8659(1973)102<405:PAIOES>2.0.CO;2.Google Scholar
Pálsson, J. (1986). Quantitative Studies on the Helminth Fauna of Capelin (Mallotus villosus (Müller)) in the Northwest Atlantic for the Purpose of Stock Discrimination. Canadian Technical Report of Fisheries and Aquatic Sciences, No. 1499, p. 21, Ottawa, Canada.Google Scholar
Parsons, L. S. and Hodder, V. M. (1971). Variation in the incidence of larval nematodes in herring from Canadian Atlantic waters. International Commission for the Northwest Atlantic Fisheries, Research Bulletin 8, 511.Google Scholar
Pella, J., Masuda, M., Guthrie, C. III, Kondzela, C., Gharrett, A. and Winans, G. (1998). Stock Composition of Some Sockeye Salmon, Oncorhynchus nerka, Catches in Southeast Alaska, Based on Incidence of Allozyme Variants, Freshwater Ages, and a Brain-Tissue Parasite. U.S. Department of Commerce, NOAA Technical Report, NMFS, No. 132.Google Scholar
Perlmutter, A. (1953). Population studies of the rosefish. Transactions of the New York Academy of Sciences 15, 189191.Google Scholar
Pippy, J. H. C. (1969). Preliminary Report on Parasites as Biological Tags in Atlantic Salmon (Salmo salar). 1. Investigations 1966 to 1968. Fisheries Research Board of Canada Technical Report, No. 134. Ottawa, Canada.Google Scholar
Pippy, J. H. C. (1980). The value of parasites as biological tags in Atlantic salmon at West Greenland. Rapports et procès-verbaux des réunions/Conseil permanent international pour l'exploration de la mer 176, 7681.Google Scholar
Quinn, T. P., Wood, C. C., Margolis, L., Riddell, B. E. and Hyatt, K. D. (1987). Homing in wild sockeye salmon (Oncorhynchus nerka) populations as inferred from differences in parasite prevalence and allozyme allele frequencies. Canadian Journal of Fisheries and Aquatic Sciences 44, 19631971. doi: 10.1139/f87-241.Google Scholar
Rulifson, R. A. and Dadswell, M. J. (1995). Life history and population characteristics of striped bass in Atlantic Canada. Transactions of the American Fisheries Society 124, 477507.Google Scholar
Sankurathri, C. S., Kabata, Z. and Whitaker, D. J. (1983). Parasites of the Pacific hake, Merluccius productus (Ayres, 1855) in the Strait of Georgia, in 1974–1975. Syesis 16, 522.Google Scholar
Scott, D. M. and Martin, W. R. (1957). Variation in the incidence of larval nematodes in Atlantic cod fillets along the southern Canadian mainland. Journal of the Fisheries Research Board of Canada 14, 975996. doi: 10.1139/f57-043.Google Scholar
Scott, D. M. and Martin, W. R. (1959). The incidence of nematodes in the fillets of small cod from Lockeport, Nova Scotia, and the southwestern Gulf of St. Lawrence. Journal of the Fisheries Research Board of Canada 16, 213221. doi: 10.1139/f59-017.Google Scholar
Scott, J. S. (1969). Trematode populations in the Atlantic argentine, Argentina silus, and their use as biological indicators. Journal of the Fisheries Research Board of Canada 26, 879891. doi: 10.1139/f69-086.Google Scholar
Scott, J. S. (1975). Geographic variation in incidence of trematode parasites of American plaice (Hippoglossoides platessoides) in the Northwest Atlantic. Journal of the Fisheries Research Board of Canada 32, 547550. doi: 10.1139/f75-068.Google Scholar
Scott, J. S. (1981). Alimentary tract parasites of haddock (Melanogrammus aeglefinus L.) on the Scotian Shelf. Canadian Journal of Zoology 59, 22442252. doi: 10.1139/z81-304.Google Scholar
Scott, J. S. (1982). Digenean parasite communities in flatfishes of the Scotian Shelf and southern Gulf of St. Lawrence. Canadian Journal of Zoology 60, 28042811. doi: 10.1139/z82-359.Google Scholar
Scott, J. S. (1985 a). Occurrence of alimentary tract helminth parasites of pollock (Pollachius virens L.) on the Scotian Shelf. Canadian Journal of Zoology 63, 16951698. doi: 10.1139/z85-252.Google Scholar
Scott, J. S. (1985 b). Digenean (Trematoda) populations in winter flounder (Pseudopleurnectes americanus) from Passamaquoddy Bay, New Brunswick, Canada. Canadian Journal of Zoology 63, 16991705. doi: 10.1139/z85-253.Google Scholar
Scott, J. S. (1987). Helminth parasites of the alimentary tract of the hakes (Merluccius, Urophycis, Phycis: Teleostei) of the Scotian Shelf. Canadian Journal of Zoology 65, 304311. doi: 10.1139/z87-047.Google Scholar
Scott, J. S. (1988). Helminth parasites of redfish (Sebastes fasciatus) from the Scotian Shelf, Bay of Fundy, and eastern Gulf of Maine. Canadian Journal of Zoology 66, 617621. doi: 10.1139/z88-092.Google Scholar
Scott, J. S. and Bray, S. A. (1989). Helminth parasites of the alimentary tract of Atlantic halibut (Hippoglossus hippoglossus L.) and Greenland halibut (Reinhardtius hippoglossoides (Walbaum)) on the Scotian Shelf. Canadian Journal of Zoology 67, 14761481. doi: 10.1139/z89-209.Google Scholar
Sherman, K. and Wise, J. P. (1961). Incidence of the cod parasite Lernaeocera branchialis L. in the New England area, and its possible use as an indicator of cod populations. Limnology and Oceanography 6, 6167.Google Scholar
Siddall, R., Pike, A. W. and McVicar, A. H. (1994). Parasites of flatfish in relation to sewage sludge dumping. Journal of Fish Biology 45, 193209. doi: 10.1111/j.1095-649.1994.tb01300.x.Google Scholar
Sindermann, C. J. (1957). Diseases of the western North Atlantic V. Parasites as indicators of herring movements. Research Bulletin of the Maine Department of Sea and Shore Fisheries 27, 130.Google Scholar
Sindermann, C. J. (1959). Population studies of herring using parasitological and serological methods. In Report to International Joint Commission, Vol. 4 (ed. Boyar, H. C., Dow, R. L., Larsen, C. M., Lozier, L. J., Scattergood, L. W., Sindermann, C. J. and Watson, J. E.), pp. 115. International Passamaquoddy Fisheries Board; Presented to: International Joint Commission, Ottawa, Ontario, Washington, DC, Appendix III, Biology – United States.Google Scholar
Sindermann, C. J. (1961 a). Parasitological tags for redfish of the western North Atlantic. International Commission for the Northwest Atlantic Fisheries, Special Publication 3, 111117.Google Scholar
Sindermann, C. J. (1961 b). Parasite tags for marine fish. Journal of Wildlife Management 25, 4147.Google Scholar
Sindermann, C. J. (1982). Parasites as Natural Tags for Marine Fish: A Review. Northwest Atlantic Fisheries Organization, SCR Doc. No. 82/IX/80.Google Scholar
Sindermann, C. and Rosenfield, A. (1954). Diseases of fishes of the western North Atlantic I. Diseases of the sea herring (Clupea harengus). Department of Sea and Shore Fisheries Research Bulletin 18, 123.Google Scholar
Stanley, R. D., Lee, D. L. and Whitaker, D. J. (1992). Parasites of yellowtail rockfish, Sebastes flavidus (Ayres, 1862) (Pisces: Teleostei), from the Pacific coast of North America as potential biological tags for stock identification. Canadian Journal of Zoology 70, 10861096. doi: 10.1139/z92-152.Google Scholar
Stunkard, H. W. and Lux, F. E. (1965). A microsporidian infection of the digestive tract of the winter flounder, Pseudopleuronectes americanus . Biological Bulletin 129, 371387.Google Scholar
Templeman, W. (1953). Knowledge of divisions of stocks of cod, haddock, redfish and American plaice in Subareas 3 and 2 of the Northwest Atlantic Convention Area. International Commission for the Northwest Atlantic Fisheries, Annual Proceedings 3, 6266.Google Scholar
Templeman, W. and Fleming, A. M. (1963). Distribution of Lernaeocera branchialis (L.) on cod as an indicator of cod movements in the Newfoundland area. International Commission for the Northwest Atlantic Fisheries, Special Publication 4, 318322.Google Scholar
Templeman, W. and Squires, H. J. (1960). Incidence and distribution of infestation by Sphyrion lumpi (Krøyer) on the redfish, Sebastes marinus (L.), of the western North Atlantic. Journal of the Fisheries Research Board of Canada 17, 931. doi: 10.1139/f60-002.CrossRefGoogle Scholar
Templeman, W., Squires, H. J. and Fleming, A. M. (1957). Nematodes in the fillets of cod and other fishes in Newfoundland and neighbouring areas. Journal of the Fisheries Research Board of Canada 14, 831897. doi: 10.1139/f57-037.Google Scholar
Templeman, W., Hodder, V. M. and Fleming, A. M. (1976). Infection of lumpfish (Cyclopterus lumpus) with larvae and of Atlantic cod (Gadus morhua) with adults of the copepod, Lernaeocera branchialis, in and adjacent to the Newfoundland area, and inferences therefore on inshore-offshore migrations of cod. Journal of the Fisheries Research Board of Canada 33, 711731. doi: 10.1139/f76-088.Google Scholar
Thompson, A. B. and Margolis, L. (1987). Determination of population discreteness in two species of shrimp, Pandalus jordani and Pandalopsis dispar, from coastal British Columbia using parasite tags and other population characteristics. Canadian Journal of Fisheries and Aquatic Sciences 44, 982989. doi: 10.1139/f87-116.Google Scholar
Urawa, S. (1989). Parasites as biological indicators contributing to salmonid biology. Scientific Reports of the Hokkaido Salmon Hatchery 43, 5374.Google Scholar
Urawa, S., Nagasawa, K., Margolis, L. and Moles, A. (1998). Stock identification of Chinook salmon (Oncorhynchus tshawytscha) in the north Pacific Ocean and Bering Sea by parasite tags. North Pacific Anadromous Fish Commission Bulletin 1, 199204.Google Scholar
Urawa, S., Harrell, L., Mahnken, C. W. and Myers, K. W. (2006). Geographical distribution and seasonal occurrence of Myxobolus kisutchi (Myxozoa: Myxosporea) in the central nerve tissues of Chinook and coho salmon in the Columbia River and its vicinities. Bulletin of the National Salmon Resources Center (Japan) 8, 17.Google Scholar
Uzmann, J. R. (1970). Use of parasites in identifying lobster stocks. Journal of Parasitology 56, 349.Google Scholar
Walker, W. A. (2001). Geographical variation of the parasite, Phyllobothrium delphini (Cestoda), in Dall's porpoise, Phocoenoides dalli, in the northern North Pacific, Bering Sea, and sea of Okhotsk. Marine Mammal Science 17, 264275. doi: 10.1111/j.1748-7692.2001.tb01270.x.Google Scholar
Whitaker, D. J. and McFarlane, G. A. (1997). Identification of sablefish, Anoplopoma fimbria (Pallas, 1811), stocks from seamounts off the Canadian Pacific coast using parasites as biological tags. In International Symposium on the Biology and Management of Sablefish, Anoplopoma fimbria (ed. Wilkins, M. E. and Saunders, M. W.), pp. 131136. NOAA, NMFS, No. 130. Seattle, WA, USA.Google Scholar
Williams, H. H., MacKenzie, K. and McCarthy, A. M. (1992). Parasites as biological indicators of the population biology, migrations, diet, and phylogenetics of fish. Reviews in Fish Biology and Fisheries 2, 144176.CrossRefGoogle Scholar
Wood, C. C., Rutherford, D. T. and McKinnell, S. (1989). Identification of sockeye salmon (Oncorhynchus nerka) stocks in mixed-stock fisheries in British Columbia and Southeast Alaska using biological markers. Canadian Journal of Fisheries and Aquatic Sciences 46, 21082120. doi: 10.1139/f89-261.Google Scholar
Zubchenko, A. V. (1981). Parasitic fauna of some Macrouridae in the Northwest Atlantic. Journal of Northwest Atlantic Fisheries Science 2, 6772.Google Scholar
Zwanenburg, K. C. T., Bentzen, P. and Wright, J. M. (1992). Mitochondrial DNA differentiation in Western North Atlantic populations of haddock (Melanogrammus aeglefinus). Canadian Journal of Fisheries and Aquatic Sciences 49, 25272537. doi: 10.1139/f92-279.Google Scholar