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Parasites as biological tags of marine, freshwater and anadromous fishes in North America from the tropics to the Arctic DAVID J. MARCOGLIESE 1 * and KYM C. JACOBSON 2 1

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 2 Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, Newport, Oregon 97365, USA (Received 9 December 2013; revised 8 January 2014; accepted 9 January 2014; first published online 10 March 2014) 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. Key words: biological tags, marine, freshwater, anadromous, fish, Atlantic, Pacific.

INTRODUCTION

The use of parasites as natural biological tags to delineate fish stocks in North American waters dates back to 1939, when the copepod Sphyrion lumpi was first used to distinguish populations of the golden redfish, Sebastes marinus, off the coast of northeastern North America (Herrington et al. 1939; Nigrelli and Firth, 1939). On the Pacific side of the continent, the first published study was on sockeye salmon (Oncorhynchus nerka) in 1963 (Margolis, 1963). There have been approximately 90 publications on the topic, most dedicated to Atlantic and Pacific fisheries, including anadromous fishes, with some studies in the Arctic as well as in fresh waters (Table 1). The earliest studies in North American waters focused on parasites of commercial cosmetic concern in the North Atlantic (Herrington et al. 1939; Nigrelli and Firth, 1939), for large, highly visible roundworms in fillets and huge crustaceans hanging * 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: [email protected] Parasitology (2015), 142, 68–89. © Cambridge University Press 2014 doi:10.1017/S0031182014000110

off fish are not aesthetically appealing to consumers and processors alike. Moreover, they can result in damaged, unmarketable seafood products, requiring costly processing. Furthermore, food inspectors may reject a heavily infected batch resulting in additional economic losses (Sindermann and Rosenfield, 1954). The goal of early studies was thus to avoid harvesting fish populations in which these parasites were abundant and costly to process. Parasites involved included the above-mentioned S. lumpi on redfish and the notorious codworm or sealworm (Pseudoterranova decipiens) in Atlantic cod (Gadus morhua) (Templeman et al. 1957). Removal of sealworm from Atlantic cod fillets cost the industry over $29 million (Cdn) in 1982, and $30 million for all species in 1984 in Atlantic Canada (Bowen, 1990). However, it was quickly realized that the parasites could be equally useful to delineate stocks for fisheries management. In contrast to the Atlantic, studies in the North Pacific were not a result of unsightly parasites, but an outcome of increased fishing efforts post-World War II and subsequent international competition for marine resources in the high seas of the North Pacific among Japan, Russia, the USA and Canada. A specific concern for Pacific salmonid stocks mixing

Host species ATLANTIC Nephropidae American lobster (Homarus americanus)

Clupeidae Atlantic herring (Clupea harengus)

Parasite(s)

Results

Reference

Various parasites

Discriminated coastal and offshore lobsters

Uzmann (1970)

Polymorphus botulus (Acanthocephala)

Some mixing of inshore and offshore lobsters

Brattey and Campbell (1986)

Various parasites

Differentiation between fish from the Gulf of St Lawrence and Gulf of Maine and between eastern and western Gulf of Maine for 1 + fish, and movement of 2 + eastern fish to the western Gulf of Maine Discriminated fish from Nova Scotia, the Gulf of Maine and Georges Bank

Sindermann (1961b)

Anisakis sp. (Nematoda) Anisakis sp. Anisakis sp. Anisakis sp. Various parasites

Rainbow smelt (Osmerus mordax)

Boyar and Perkins (1971) Parsons and Hodder (1971) Lubieniecki (1973) Beverley-Burton and Pippy (1977) McGladdery and Burt (1985) Chenoweth et al. (1986) McGladdery (1987) Bradford and Iles (1992)

Eimeria sardinae (Apicomplexa) A. simplex

Migration in and out of the Bay of Fundy, offshore from Newfoundland, and in and out of the Gulf of St Lawrence, spawning behaviour Discriminated spawning fish from Southwest Nova Scotia and those from Jeffreys Ledge, Gulf of Maine Distinguished spawning groups of fish on east coast of Canada Migration in and out of Bay of Fundy

Various digeneans

No discrimination of fish from the Scotian Shelf and St Pierre Bank

Scott (1969)

Lecithaster gibbosus (Digenea), Contracaecum sp., Hysterothylacium aduncum (Nematoda) Microsporidium sp. (Microsporidia), A. simplex, Contracaecinea gen. sp. Glugea hertwigi (Microsporidia), Diphyllobothrium sebago (Cestoda), Echinorhynchus salmonis (Acanthocephala)

Discriminated fish from the Gulf of St Lawrence from those off northern and eastern Newfoundland

Pálsson (1986)

No evidence of distinct stocks in the estuary and Gulf of St Lawrence

Arthur and Albert (1996) Fréchet et al. (1983)

Anisakis simplex

Argentinidae Atlantic argentine (Argentina silus) Osmeridae Capelin (Mallotus villosus)

Similarity of fish from the Magdalen Islands, northern Gulf of St Lawrence and SW Newfoundland; separation from those from NE Nova Scotia and the Scotian Shelf; inshore-offshore migration off Nova Scotia Lack of discrimination of fish from Long Island to Chesapeake Bay Attempted to use morphometrics to delineate fish stocks off eastern Canada

Distinguished populations from the Saguenay fjord, the south shore of the St Lawrence estuary, Chaleur Bay, and the north shore of the St Lawrence estuary

Biological tags of North American fishes

Table 1. List of parasites used as biological tags, their hosts, basic results of the study and reference, organized by region, for North American fishes. Studies from Greenland are included only if they pertain to North American marine fishes or local anadromous fishes. Studies from the Pacific open seas are included only if they pertain to North American anadromous species. Scientific names have been updated to reflect changes in host and parasite taxonomy

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Host species

Parasite(s)

Results

Reference

Salmonidae Atlantic salmon (Salmo salar)

Various freshwater and marine parasites

Potentially discriminate Canadian stocks off west Greenland, fish which have migrated to Greenland, and certain rivers of origin in Quebec and New Brunswick Differentiated North American and European fish at sea

Pippy (1969)

Eubothrium crassum (Cestoda), A. simplex Anisakis sp. A. simplex A. simplex

Macrouridae Rock grenadier (Coryphaenoides rupestris) Roughhead grenadier (Macrourus berglax) Marlin-spike (Nezumia bairdi) Merluccciidae Silver hake (Merluccius bilinearis) Silver hake Phycidae White hake (Urophycis tenuis) Hakes (Urophysis chuss, U. tenuis, Phycis chesteri) Gadidae Atlantic cod (Gadus morhua)

Attempted to use morphometrics to delineate fish stocks off eastern Canada Confirmed mixing of North American and European fish off west Greenland, but unable to differentiate them; differentiated fish from different areas off eastern Canada Attempted to infer migrations off east coast of Canada using population genetics; could not discriminate between European and North American fish

Nyman and Pippy (1972) Beverley-Burton and Pippy (1977) Beverley-Burton and Pippy (1978) Beverly-Burton (1978)

Various parasites

Discriminated fish from the Davis Strait, northern Grand Bank, and off Labrador Discriminated fish from the Flemish Cap and off southern Labrador

Zubchenko (1981)

Various parasites

Discriminated fish from the Flemish Cap and off southern Labrador

Zubchenko (1981)

Clestobothrium crassiceps (Cestoda) Various parasites

Discriminated fish from the Scotian Shelf and Gulf of Maine No differentiation of fish on the Scotian Shelf from the Bay of Fundy or the Gulf of Maine

Scott (1987) Scott (1987)

Various parasites

Discriminated fish from deep and shallow waters in the southern Gulf of St Lawrence, and the Cape Breton Shelf No differentiation of fish on the Scotian Shelf from the Bay of Fundy or the Gulf of Maine

Melendy et al. (2005)

Various parasites

Various parasites

Pseudoterranova decipiens (Nematoda) Pseudoterranova decipiens (Nematoda) Lernaeocera branchialis (Copepoda) L. branchialis

Discriminated fish from 4 fisheries (western Nova Scotia, offshore banks, Cape Breton area, southwestern Gulf of St Lawrence); inshore-offshore; seasonal migrations Discriminated fish between inshore and offshore Lockport, Nova Scotia, and between SE and SW Gulf of St Lawrence; migration in and out of Gulf of St Lawrence Discriminated 4 groups of fish (Gulf of Maine, southern Gulf of Maine, Georges Bank, New England) Distinguished inshore fish from Newfoundland from those offshore and on the Grand Banks and Flemish Cap

David J. Marcogliese and Kym C. Jacobson

Table 1. (Cont.)

Zubchenko (1981)

Scott (1987)

Scott and Martin (1957) Scott and Martin (1959) Sherman and Wise (1961) Templeman and Fleming (1963) 70

Hemiuris levinseni (Digenea), H. aduncum Nematodes in fillets P. decipiens A. simplex in muscle P. decipiens, A. simplex, Contracaecum osculatum Various parasites Various parasites Various parasites Haddock (Melanogrammus aeglefinus) Pollock (Pollachius virens) Scorpaenidae Redfish (Sebastes spp.)

Various parasites

Acadian redfish (Sebastes fasciatus) Acadian redfish, deepwater redfish (Sebastes mentella) Deepwater redfish

Anisakid nematodes, parasite species richness Sphyrion lumpi, (Copepoda) Chondracanthus nodosus (Copepoda) S. lumpi

Deepwater redfish

S. lumpi A. simplex, H. aduncum, S. lumpi

Golden redfish (Sebastes marinus)

Myxidium bergense (Myxosporea), Lepidapedon rachion (Digenea) Various parasites

S. lumpi

Discriminated fish from Labrador and eastern Newfoundland, western and southern Newfoundland, Gulf of St Lawrence, northern Grand Banks, southern Grand Banks, and Flemish Cap Discriminated between fish from East and West Greenland, and inshore and offshore Greenland Differences in infection levels among fish from St Pierre Bank, Burgeo Bank and Rose Blanche Bank (off southern Newfoundland) Discriminated among fish from various areas surrounding Newfoundland, influx of migrants Discriminated southern Newfoundland from Labrador, eastern Newfoundland and Grand Banks Distinguished among fish from the SW Gulf of St Lawrence, SE Gulf and the Breton Shelf, determined migrant and resident fish Discriminated among fish from various areas surrounding Newfoundland Unable to differentiate fish from southern and northern Labrador Discriminated distinct spawning groups from the SE and SW Gulf of St Lawrence Potential differentiation of fish from the Bay of Fundy, Browns Bank and Emerald-Banquereau banks Discriminated fish from the central and SW Scotian Shelf

Khan et al. (1980) Boje (1987) Bishop et al. (1988) Brattey et al. (1990) Brattey and Bishop (1992) McClelland and Marcogliese (1994) Khan and Tuck (1995) Lee and Khan (2000) McClelland and Melendy (2011) Scott (1981)

Biological tags of North American fishes

Trypanosoma murmanensis (Mastigophora)

Scott (1985a)

Discriminated among fish from Labrador and eastern Newfoundland, southern Newfoundland, and Flemish Cap Discriminated Gulf of Maine from the Scotian Shelf and Bay of Fundy

Bourgeois and Ni (1984) Scott (1988)

Potentially discriminated among redfish species

Moran et al. (1996)

Discriminated between fish from Hamilton Inlet Bank, eastern Grand Banks, and SE Gulf of St Lawrence from NE Grand Banks, Flemish Cap and Scotian Shelf; possibility of slow migration Discriminated fish from Flemish Cap and Irminger Sea Discriminated among fish from the Labrador Sea, Gulf of St Lawrence, Cabot Strait-Laurentian Channel and Flemish Cap Discriminated fish from Maine and Cape Cod from those from Brown’s Bank

Templeman and Squires (1960) Bakay (1988) Marcogliese et al. (2003) Nigrelli and Firth (1939) Perlmutter (1953) Sindermann (1961a)

Various parasites

Discriminated Gulf of Maine fish from those on Nova Scotian banks Discriminated fish from major fishing grounds off Nova Scotia and the Gulf of Maine, the Gulf of St Lawrence and the Grand Banks

Cyclopteridae Lumpfish (Cyclopterus lumpus)

L. branchialis

Discriminated between fish from inshore and offshore Newfoundland

Templeman et al. (1976)

Moronidae Striped bass (Morone saxatilis)

Various parasites

Mixing of fish from the SW Gulf of St Lawrence and the Bay of Fundy with those from coastal mid-Atlantic waters

Rulifson and Dadswell (1995) 71

Host species

Parasite(s)

Results

Reference

Sciaenidae Atlantic croaker (Micropogonias undulatus) Scombridae Atlantic mackerel (Scomber scombrus) Istiophoridae White marlin (Tetrapturus albidus) Xiphiidae Swordfish (Xiphias gladius)

Various parasites

Discriminated fish between the Mid Atlantic Bight and the South Atlantic Bight

Baker et al. (2007)

Anisakis sp.

Lack of discrimination of fish from Long Island to Chesapeake Bay

Lubieniecki (1973)

Various parasites

Inconclusive (Atlantic and Caribbean)

Barse and Hocutt (1990)

Tristoma coccineum, Tristoma integrum (Monogenea) Various parasites

Discriminated fish from the Scotian Shelf and Grand Banks from those on Georges Bank and Cape Hatteras Discriminated fish from the Gulf of Guinea and the NW Atlantic Ocean

Hogans and Brattey (1982) Castro-Pampillón et al. (2002)

Various parasites

Discriminated fish in the Gulf of St Lawrence from the Scotian Shelf

Scott (1982)

Various digeneans

Discriminated distinct stock in Gulf of St Lawrence, and potential differentiation between Western Bank and Banquereau and Browns Banks Discriminated fish in the Gulf of St Lawrence from the Scotian Shelf Discriminated fish from the SW and SE Gulf of St Lawrence

Scott (1975)

Pleuronectidae Witch flounder (Glyptocephalus cynoglossus) American plaice (Hippoglossoides platessoides)

Various parasites Anisakis sp., Contracaecum sp.

Atlantic halibut (Hippoglossus hippoglossus) Yellowtail flounder (Limanda ferruginea) Winter flounder (Pleuronectes americanus)

Echinorhychus gadi, Corynosoma strumosum (Acanthocephala) Various parasites

Discriminated fish from the SE and SW Gulf of St Lawrence

Cryptocotyle lingua (Digenea)

Discriminated fish from Cape Cod from southern New England and Georges Bank Discriminated fish in the Gulf of St Lawrence from the Scotian Shelf Discriminated inshore fish from Woods Hole and offshore fish from Georges Bank Discriminated fish in the Gulf of St Lawrence from the Scotian Shelf Potential differentiation of fish in the Gulf of St Lawrence, off Sable Island, and Fisher Island Sound (MA) from Passamaquoddy Bay (NB) Discriminated fish from the Scotian Shelf and Gulf of Maine

Various parasites Glugea stephani (Microsporidia) Various parasites Various digeneans Various digeneans and nematodes

Smooth flounder (Liopsetta putnami) Greenland halibut (Reinhardtius hippoglossoides)

Various parasites T. murmanensis, Haemohormidium terraenovae (Apicomplexa) Various parasites Various parasites

No evidence of stock differentiation on banks of the Scotian Shelf

Scott (1982) McClelland et al. (1983) McClelland and Melendy (2007) Scott and Bray (1989) Lux (1963) Scott (1982) Stunkard and Lux (1965) Scott (1982) Scott (1985b) McClelland et al. (2005) Burn (1980) Khan et al. (1982) Scott and Bray (1989) Arthur and Albert (1993)

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Discriminated between fish from the lower and upper Green Bay estuary (NH) Discriminated among fish from the Davis Strait, off Labrador and Newfoundland, and the Gulf of St Lawrence No evidence of stock differentiation on banks of the Scotian Shelf Discriminated among fish from the Gulf of St Lawrence, the Saguenay Fjord and off Labrador

David J. Marcogliese and Kym C. Jacobson

Table 1. (Cont.)

Pandalidae Smooth pink shrimp (Pandalus jordani) Sidestriped shrimp (Pandalopsis dispar) Clupeidae Pacific herring (Clupea pallasii)

Pacific sardine (Sardinops sagax)

Osmeridae Surf smelt (Hypomesus pretiousus) Salmonidae Steelhead salmon (Oncorhynchus mykiss)

Sockeye salmon (Oncorhynchus nerka)

Discriminated fish from SW Greenland fjords, the Denmark Strait and those from West Greenland-Davis Strait-Newfoundland

Boje et al. (1997)

Various parasites

Potential usefulness to delineate stocks on spawning grounds

Various parasites

Separated different spawning groups into smaller geographic regions

Bower and Margolis (1991) Nagasawa et al. (1998)

Neolebouria tinkerbellae (metacercariae), unidentified metacercaria (Digenea) Neolebouria tinkerbellae (metacercariae) (Digenea), unidentified metacercaria

Provided evidence for discrete populations among channels and an offshore area of Barkley Sound, British Columbia (BC) Provided evidence for discrete populations among channels and an offshore area of Barkley Sound, BC

Thompson and Margolis (1987) Thompson and Margolis (1987)

H. aduncum, A. simplex, bucephalid metacercariae (Digenea) Various parasites

Arthur and Arai (1980) Moser and Hsieh (1992) Baldwin et al. (2011)

Myosaccium ecaude, Lecithaster gibbosus (Digenea)

Potential to discriminate Washington spawning stock from stocks in coastal waters of BC and Alaska Potential to discriminate spawning stocks of San Francisco and Tomales Bays, California Panmictic distribution of haplotypes of 3 Anisakis species does not confirm or deny subdivision in California Current system Review of techniques on studies of stock structure, mentions digenean distribution and sardine migration patterns

Anisakis sp.

Provided evidence for 3 distinct spawning populations in state of Washington

Kilambi and DeLacy (1967)

Plagioporus shawi, Nanophyetus salmincola (metacercariae, Digenea) N. salmincola metacercariae N. salmincola metacercariae P. shawi Triaenophorus crassus (plerocercoid, Cestoda), Truttaedacnitis truttae (Nematoda) (Myxobolus arcticus, Henneguya salmincola (Myxosporea) Various parasites

Established a Pacific NW US origin of infected fish on high seas, estimation of proportion in high-seas samples increased beyond tag recoveries Estimated percentage of US steelhead in Japanese high seas fishery Identified US vs Japanese origin fish in high seas fishery Genetics of digeneans show more structure than genetics of fish Delineated fish from North American and Asian origin in high seas fishery

Margolis (1984, 1985)

Anisakis spp.

Various parasites M. arcticus (published as M. neurobius) M. arcticus (published as M. neurobius) M. arcticus, H. salmincola

Used with allozyme allele frequencies to estimate homing precision of wild sockeye in BC Determined that parasite assemblages of Fraser River juveniles could resolve stock composition of smolts migrating through Strait of Georgia, BC Migratory patterns through Strait of Georgia of Fraser River (BC) and Lake Washington (WA) sockeye smolts Identified 15 groups among 51 stocks in fishery using parasite and genetic (electrophoretic) markers Established detailed distribution of parasite in southeast Alaska Compared four techniques for delineating stocks in Barkley Sound, BC; recent change in prevalence reduced usefulness of parasites

Biological tags of North American fishes

PACIFIC Ommastrephidae Neon flying squid (Ommastrephes bartramii)

Various digeneans and nematodes

Baldwin et al. (2012)

Dalton (1991) Myers et al. (1991) Criscione et al. (2006) Margolis (1963) Quinn et al. (1987) Bailey et al. (1988) Groot et al. (1989) Wood et al. (1989) Moles et al. (1990) Beacham et al. (1998) 73

Host species

Parasite(s)

Results

Reference

M. arcticus

In combination with other fish allozyme variants determined stock composition in fisheries of southern SE Alaska and northern BC Distinguished between western Alaska fish and eastern Gulf of Alaska stocks Identified as a potential biological tag in California

Pella et al. (1998)

M. arcticus Coho salmon (O. kisutch), Chinook salmon (O. tshawytscha) Chinook salmon Merlucciidae Pacific hake (Merluccius productus) Gadidae Walleye pollock (Theragra chalcogramma) Scorpaenidae Rougheye rockfish (Sebastes aleutianus) Pacific Ocean perch (Sebastes alutus) Shortraker rockfish (Sebastes borealis) Yellowtail rockfish (Sebastes flavidus) Anoplopomatidae Sablefish (Anoplopoma fimbria)

Pentacerotidae North Pacific armorhead (Pseudopentaceros wheeleri) Pleuronectidae Pacific halibut (Hippoglossus stenolepsis) English sole (Parophrys vetulus) Phocoenidae

Diplostomum spathaceum (Digenea) metacercariae

Moles and Jensen (2000) Jennings and Hendrickson (1982)

M. arcticus, Myxobolus kisutchi (Myxosporea)

Estimated continental origins in the North Pacific Ocean and Bering Sea

Urawa et al. (1998)

Ascarophis sp. (Nematoda), unidentified helminth eggs

Suggests lack of extensive contact between two hake populations in the Strait of Georgia, BC

Sankurathri et al. (1983)

Various parasites

Survey of parasite fauna identified differences among localities in coastal BC

Arthur (1983, 1984)

Various parasites

Potential for stock discrimination in the Gulf of Alaska

Moles et al. (1998)

Neobrachiella robusta (Copepoda)

Potential for stock discrimination off the coast of BC

Various parasites

Potential for stock discrimination in the Gulf of Alaska

Leaman and Kabata (1987) Moles et al. (1998)

Microcotyle sebastis (Monogenea)

Potential for stock identification along Pacific coast of North America

Stanley et al. (1992)

Various adult digeneans

Kabata et al. (1988)

Various adult digeneans, Ceratomyxa anoplopoma (Myxosporea)

Potential to discriminate fish between seamounts and continental slope off the west coast of Canada Fish stocks at seamounts are discrete from each other and from continental slope stocks

Microcotyle macropharynx (Monogenea)

Identified new recruits to seamount population

Humphreys et al. (1993)

Various parasites

Discriminated three groups of adult fish from northern Bering Sea to central California Provided evidence for exclusive use of estuary as nursery grounds in Oregon

Blaylock et al. (2003)

Various parasites

David J. Marcogliese and Kym C. Jacobson

Table 1. (Cont.)

Whitaker and McFarlane (1997)

Olson and Pratt (1973)

74

ARCTIC Salmonidae Arctic charr (Salvelinus alpinus)

Atlantic salmon (Salmo salar) FRESH WATER Clupeidae American shad (Alosa sapidissima) Catostomidae White sucker (Catostomus commersonii) Salmonidae Lake herring (Coregonus artedi) Bloater (Coregonus hoyi) Atlantic salmon

Brook charr (Salvelinus fontinalis)

Phyllobothrium delphini (Cestoda)

Provided evidence for limited movement between Bering Sea region south of western Aleutian Islands

Walker (2001)

Cystidicola cristivomeri (Nematoda)

Distinguished resident fish from anadromous fish in Somerset Island

Various parasites

Discriminated anadromous and resident fish on Baffin Island

Various parasites

Discriminated anadromous and resident fish in Labrador

Various parasites Various parasites

Discriminated resident and anadromous fish in Greenland Unable to differentiate North American and European stocks in West Greenland

Eddy and Lankester (1978) Dick and Belosevic (1981) Bouillon and Dempson (1989) Due and Curtis (1995) Pippy (1980)

Helminths, crustaceans

Bay of Fundy population consists of fish from different areas and rivers along the Atlantic coast

Hogans et al. (1993)

Diplostomum spp.

Discriminated fish from Lake St Louis and Lake St Pierre within the St Lawrence River

Marcogliese et al. (2001)

Various parasites Salmincola corpulentus (Copepoda)

Discriminated fish from Minnesota and Wisconsin waters in Lake Superior Discriminated fish from various locations in Lake Huron

Discocotyle sagittata (Monogenea), Diplostomum spathaceum), Neoechinorhynchus rutili (Acanthocephala) Brachyphallus crenatus (Digenea)

Determined tributaries of origin in the Miramichi River system and estuary (NB)

Hoff et al. (1997) Bowen and Stedman (1990) Hare and Burt (1976)

Various parasites

Estimated minimum proportion of fish in tributary of the Moisie River, Quebec, which had been to sea Estimated maximum proportion of fish which overwintered in tributary of the Moisie River Discriminated fish from different areas of the Tabusintac River (NB), movement of fish into estuary, evidence of anadromous fish in river Discriminated littoral and limnetic fish

Various parasites

Unable to discriminate fish from inner and outer Saginaw Bay, Lake Huron

Diplostomum spp.

Discriminated fish from Lake St Louis and Lake St Pierre within the St Lawrence River, seasonal presence of different stocks near Quebec City

Salmincola edwardsii (Copepoda) Various parasites

Percidae Walleye (Sander vitreus)

Biological tags of North American fishes

Dall’s porpoise (Phocoenoides dalli)

Black (1981) Black et al. (1983) Frimeth (1987) Bertrand et al. (2008) Muzzall and Haas (1998) Marcogliese et al. (2001)

75

David J. Marcogliese and Kym C. Jacobson

76

Fig. 1. Map of the Northwest Atlantic showing the main geographic and bathymetric features, and fish stocks studies in each major area. Common names of fishes are presented in the legend. Scientific names can be found in Table 1.

in a high seas fishery resulted in extensive collaborative research programmes initiated in 1955 that included the use of parasites as biological tags. As other fisheries in the North Pacific grew, so did the need to examine origins of fish in mixed-stock fisheries and the exploration of parasites as potential biological tags. The criteria for successful candidate parasites to be used as natural biological tags have been reviewed and discussed elsewhere (Kabata, 1963; Sindermann, 1982; MacKenzie, 1987, 1993; Williams et al. 1992; MacKenzie and Abaunza, 1998). Advantages and disadvantages of the use of parasites have also been summarized previously (Sindermann, 1982; Dick, 1984; Arthur, 1997; MacKenzie and Abaunza, 1998). Thus, it is not our intention to reiterate these herein. Rather, we intend to summarize the records of the use of parasites as biological tags of marine fishes in North American waters of the Atlantic, Pacific and Arctic Oceans. Furthermore, we examine their use for anadromous fishes in freshwater, estuarine and marine ecosystems, as well as freshwater fishes in large lakes and rivers. We concentrate on primary publications and only include government reports if the data have not been published elsewhere. The majority of studies (> 50) feature Atlantic fishes, with

a sizeable number (approximately two dozen) investigating Pacific fishes, and relatively few on fish from Arctic and freshwater ecosystems (Table 1). There is a distinct lack of studies from the Caribbean and Mexican tropical waters. A T L A N T I C WA T E R S

The majority of studies of parasites as biological tags in North America have been completed in Atlantic waters. Most studies pertain to fisheries in the northwestern Atlantic (Fig. 1), with relatively few off the eastern seaboard of the USA. Investigations cover a total of 30 species of fish belonging to 14 families, and one crustacean. The fishes include seven gadids and flatfishes each, as well as species of clupeids, salmonids, osmerids, redfishes, scombrids, among others (Table 1). The fish species attracting the most attention are Atlantic cod, Atlantic herring (Clupea harengus) and the redfishes (Sebastes spp.). Below, we focus on these species as they constitute long-term case studies with the most extensive historical records for Atlantic waters. Over half the studies include more than one species of parasite. Overall, parasites deemed useful as tags in Atlantic waters include examples from

Biological tags of North American fishes

77

Fig. 2. Sealworm (Pseudoterranova decipiens) in the fillet of an Atlantic cod (Gadus morhua). Photograph by David J. Marcogliese.

Fig. 3. The copepod parasite Sphyrion lumpi, embedded laterally on a redfish (Sebastes sp.). Photograph courtesy of Jonathan D. W. Moran.

numerous taxa, including trypanosomes, microsporidians, myxozoans, nematodes, digeneans, cestodes, acanthocephalans, monogeneans and crustaceans. The most commonly utilized parasites in Atlantic waters have been the anisakid nematodes, used exclusively in 15 studies or in conjunction with other parasite species in 13 of those undertaken in the Northwest Atlantic region (Table 1). This is not surprising, given their previous recognition by MacKenzie (1987) and Williams et al. (1992) as potentially important indicators. Their usefulness derives from the fact that they are extremely abundant in marine fishes and relatively easily observed due to their large size. Investigations on the use of parasites as biological tags in Atlantic cod date back to the works of Scott and Martin (1957, 1959), span the Northwest Atlantic from Greeenland and Labrador to New England, and include both inshore waters and offshore banks (Table 1; Fig. 1). Anisakid nematodes, in particular P. decipiens (Fig. 2), are most often employed as biological tags. Most studies focus on two areas, around Newfoundland and Labrador, or alternatively the southern Gulf of St Lawrence and Scotian Shelf off Nova Scotia (Table 1; Fig. 1). Studies generally support the existence of multiple stocks off Newfoundland, encompassing Labrador and northern Newfoundland, the northern Gulf of St Lawrence, various banks off southern Newfoundland, as well as the Grand Banks and Flemish Cap (Fig. 3; Templeman and Fleming, 1963; Khan et al. 1980; Bishop et al. 1988; Brattey et al. 1990; Brattey and Bishop, 1992; Khan and Tuck, 1995). Most of these studies restricted themselves to the use of a single parasite species or taxon, including the copepod Lernaeocera branchialis (Templeman and Fleming, 1963), the blood protozoan Trypanosoma murmanensis (Khan et al. 1980), the anisakid larval nematode Anisakis simplex, also known as the herringworm or whaleworm (Brattey and Bishop, 1992) and, of course, the sealworm

P. decipiens (Bishop et al. 1988; Brattey et al. 1990). However, the most recent studies of cod in these waters expand the scope of study, making use of four to five different groups of parasites (Khan and Tuck, 1995). Further south, but still in Canadian waters, the most commonly used biological tag in Atlantic cod is the sealworm, sometimes utilized in conjunction with other anisakid nematodes. These were used to differentiate Atlantic cod from southwestern Nova Scotia, the offshore banks on the Scotian Shelf, and southeastern and southwestern Gulf of St Lawrence (Fig. 1). Studies also indicate fish migration in and out of the Gulf in addition to resident fish (Scott and Martin, 1957, 1959; McClelland and Marcogliese, 1994). Again, the most recent study expands previous work to include other parasites as tags, such as the adult anisakid nematode Hysterothylacium aduncum, and the acanthocephalans Echinorhynchus gadi and Corynosoma strumosum, further supporting the differentiation of southwestern and southeastern stocks in the Gulf of St Lawrence (McClelland and Melendy, 2011). Research into stock discrimination of the redfishes is also principally divided among two geographic areas, the northern banks off Newfoundland and the region surrounding the Gulf of Maine (Fig. 1). Initially, most studies focused on the copepod S. lumpi (Fig. 3) as a biological tag (Nigrelli and Firth, 1939; Perlmutter, 1953; Templeman and Squires, 1960; Bakay, 1988). However, as with studies on Atlantic cod, many scientists subsequently incorporated other taxa such as the anisakid nematodes (Sindermann, 1961b; Bourgeois and Ni, 1984; Scott, 1988; Marcogliese et al. 2003). Studies using parasites as biological tags show that redfish from the Gulf of Maine are distinct from all those caught further north in the Bay of Fundy, Brown’s Bank and the Scotian Shelf (Nigrelli and Firth, 1939; Scott, 1988). Still further north, deepwater redfish (Sebastes mentella) were differentiated from the eastern and

David J. Marcogliese and Kym C. Jacobson

western waters off Newfoundland using S. lumpi infection levels (Templeman and Squires, 1960). In a multispecies study where A. simplex, H. aduncum and S. lumpi are shown to have discriminatory power, deepwater redfish stocks are differentiated off Labrador, in the Gulf of St Lawrence, in the Cabot Strait-Laurentian Channel dividing the northern and southern Gulf of St Lawrence, and the Flemish Cap (Fig. 3; Marcogliese et al. 2003). A potential confounding factor affecting studies on redfish is the difficulty in separating the three redfish species (S. marinus, S. mentella and Sebastes fasciatus) in the Northwest Atlantic. In many studies, separation is based on depth of capture and geographic distribution (Templeman and Squires, 1960), but it may prove that early parasite records are erroneous (Bourgeois and Ni, 1984). Differential infections by the copepods S. lumpi and Chondracanthus nodosus on S. mentella and S. fasciatus led Moran et al. (1996) to suggest that these parasites could be used to aid in the identification of these two redfish species. Atlantic herring is the pelagic species with the longest history of tagging studies, dating back to the 1950s and 1960s (Sindermann, 1957, 1959, 1961b). Original studies centre on the distinction between Gulf of Maine populations and other stocks (Fig. 1). Using an assortment of parasites, including Ichthyosporidium hoferi, Kudoa clupeidae and anisakid nematodes, Sindermann (1961b) discriminates herring in the Gulf of Maine from those in the Gulf of St Lawrence, and those off Nova Scotia from those on Georges Bank. He further separates herring from the eastern and western sections of the Gulf of Maine. Anisakis sp. was used to delineate fish from the Gulf of Maine, Nova Scotia and Georges Bank (Fig. 3; Boyar and Perkins, 1971). In contrast, Lubieniecki (1973) could not discriminate herring collected from localities between Long Island and Chesapeake Bay off the east coast of the USA. More recently, herring were separated between the Gulf of Maine and Southwest Nova Scotia using the anisakid A. simplex as a biological tag (Chenoweth et al. 1986). In a novel approach, morphometric variation in the parasite A. simplex also was considered a potential tool to discriminate populations of Atlantic herring (BeverleyBurton and Pippy, 1977). Parasites also have been used as indicators of migration in herring. Inshore-offshore migrations are demonstrated using Anisakis sp. (Parsons and Hodder, 1971), while McGladdery and Burt (1985) use various parasites, including two nematodes, three digeneans, one cestode and one protozoan to indicate migration and spawning behaviour. McGladdery (1987) further distinguishes between first and repeat spawners using Eimeria sardinae in the testes. An examination of parasites as biological indicators in different fish species in the Northwest Atlantic repeatedly demonstrates the recurrence of certain

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geographical patterns. Separation of stocks among the Gulf of St Lawrence, the Breton Shelf and the Scotian Shelf is shown for Atlantic cod, Atlantic herring, American plaice (Hippoglossoides platessoides), yellowtail flounder (Limanda ferruginea), witch flounder (Glyptocephalus cynoglossus), winter flounder (Pleuronectes americanus) and redfishes (Scott and Martin, 1957; Parsons and Hodder, 1971; Scott, 1975, 1982; McClelland and Marcogliese, 1994; McClelland et al. 2005). More precise stock delineations between the southeastern and southwestern southern Gulf of St Lawrence are observed for Atlantic cod and American plaice (Scott and Martin, 1959; McClelland et al. 1983; McClelland and Marcogliese, 1994; McClelland and Melendy, 2007, 2011). Distinct stocks of silver hake (Merluccias bilinearis), Atlantic herring, and redfish are observed in the Scotian Shelf, southwestern Nova Scotia and the Gulf of Maine (Perlmutter, 1953; Templeman and Squires, 1960; Boyar and Perkins, 1971; Chenoweth et al. 1986; Scott, 1987, 1988; Marcogliese et al. 2003). Further distinctions are noted for haddock (Melanogrammus aeglefinus) and winter flounder between the Bay of Fundy and the Scotian Shelf (Scott, 1981, 1985a). Redfish, Greenland halibut (Reinhardtius hippoglossoides) and capelin (Mallotus villosus) are shown to have distinct stocks in the Gulf of St Lawrence, Newfoundland and Labrador (Khan et al. 1982; Bourgeois and Ni, 1984; Pálsson, 1986; Arthur and Albert, 1993; Marcogliese et al. 2003). Distinct stocks of Atlantic cod, redfish and grenadiers are observed on the Flemish Cap and the Grand Banks (Templeman and Fleming, 1963; Zubchenko, 1981; Bourgeois and Ni, 1984; Brattey and Bishop, 1992; Marcogliese et al. 2003). These shared differences suggest that stock structure of these fishes is influenced and defined by oceanographic features, such as deep channels and the physical arrangement of banks on the continental shelf in the Northwest Atlantic Ocean. N O R T H PAC I F I C WAT E R S

Turning westwards, tagging studies in this vast open region cover all spatial scales following the importance for mixed fisheries in open seas, geopolitical zones between neighbouring countries and neighbouring states within the USA. Documented in Table 1 and highlighted below are studies on 21 species of fish, marine mammals or invertebrates in North American waters of the Pacific Ocean that have been examined for the use of parasites as natural tags. The majority of studies have been conducted on the anadromous Pacific salmonids leading to the use of freshwater parasites for many studies. Other commercially important demersal and pelagic fishes studied include species of gadids, clupeids, scorpaenids, pleuronectids, an anoplopomatid and a pentacerotid as well three invertebrate species (Table 1).

Biological tags of North American fishes

As mentioned above, in contrast to the origin of the use of parasites as tags in Atlantic waters, the examination of parasites as tags in North Pacific waters originated with the need for stock identification in mixed stock fisheries after WWII. With Japan’s subsequent increasing need for dietary protein, concerns of the USA and Canada regarding Japan’s offshore catches of commercially important species such as Pacific salmon (Oncorhynchus spp.), Pacific halibut (Hippoglossus stenolepis), and Pacific herring (Clupea pallasii) in international waters (high seas), led to the International Convention for the High Seas Fisheries of the North Pacific Ocean and the formation of the International North Pacific Fisheries Commission (INPFC) in 1952 (Jackson and Royce, 1986). With its member nations (USA, Canada and Japan) the INPFC established a collaborative research programme with a key objective of determining the geographical line or lines that best separate Pacific salmon originating from North America and Asia (Burgner, 1992). This programme recognized parasites as biological tags on the high seas as a potential method for stock identification or determination of continent of origin. For this reason Pacific salmonids appear to be the first fish species in the North Pacific to be studied for the potential use of parasites as biological tags. The North American efforts in this research were pioneered by a Canadian federal fisheries scientist, Dr Leo Margolis (Fig. 4). An initial international collaborative effort between 1955 to 1959 yielded a sample size of close to 13 000 specimens of different life stages of sockeye salmon (O. nerka) from North American rivers, British Columbia coastal systems, Kamchatka (Russian Far East) and the high seas (Margolis, 1963). Juvenile (plerocercoid) stages of the tapeworm Triaenophorus crassus in muscle and the intestinal nematode Truttatedacnitis (Dacnitis) truttae, which seemed to persist throughout the life of the salmon, were considered good candidates to identify the ocean distribution of western Alaskan and Kamchatkan sockeye (Margolis, 1963). The presence of T. crassus indicated Western Alaskan (Bristol Bay) origin due to the occurrence of its definitive host, northern pike (Esox lucius) in lakes cohabited by pike and sockeye salmon. In this extensive and pioneering study, Margolis concludes that maturing Bristol Bay sockeye comprised a large proportion of the fish taken immediately south of the Aleutians in late May and early June and from those taken in the northwestern part of the Gulf of Alaska in early June (Fig. 5 upper image). Immature sockeye caught later in the summer occupy areas similar to mature salmon (Fig. 5 lower image). These results, later corroborated by artificial tagging studies, indicate a large overlap in the distribution of Kamchatka and Bristol Bay sockeye salmon in the Northeast Pacific high seas (Margolis, 1992). On a smaller spatial scale, freshwater myxosporeans, Henneguya salmincola and Myxobolus arcticus

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Fig. 4. Dr Leo Margolis (1927–1997) of the Canadian Department of Fisheries and Oceans proudly displaying the Order of Canada, awarded in 1990 (courtesy of the Nanaimo Museum, Nanaimo, British Columbia).

(previously identified as Myxobolus neurobius; Urawa, 1989) were used to distinguish returning sockeye salmon among lakes in British Columbia (Margolis, 1982) and to estimate straying rates among five British Columbian populations (Quinn et al. 1987). The occurrence of this Myxobolus species was an effective tag for separating Alaskan from Canadian stocks of sockeye salmon, but unreliable for estimates of individual stocks (Wood et al. 1989). Moles and Jensen (2000) examined over 10 000 spawning sockeye salmon from 86 lakes and streams throughout Alaska to identify the potential of M. arcticus as a biological tag for mixed stock fisheries of Alaska. They found that the high prevalence of this myxosporean among eastern Gulf of Alaska stocks (primarily of lake origin) compared with an absence of the parasite from many western stocks (primarily from river systems), along with interannual stability of infection, provide opportunities for even smallscale stock separation. In stream-type Chinook salmon (Oncorhynchus tshawytscha), which typically spend up to a year in fresh water before emigrating to the ocean, the myxosporean brain parasites M. arcticus and Myxobolus kisutchi were identified as potential biological tags for adult Chinook salmon caught in the North Pacific

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Fig. 5. High-seas locations of catch of Triaenophorus-infected and Dacnitis-infected sockeye salmon (Oncorhynchus nerka) from 1955 to 1959. Sampling locations where neither Triaenophorus nor Dacnitis were found are not shown. Upper chart = maturing sockeye; lower chart = immature sockeye. Reproduced from Margolis (1963) with permission from the North Pacific Anadromous Fish Commission.

Ocean and Bering Sea. Freshwater baseline studies demonstrated an overall prevalence of 67·7% of M. arcticus in Chinook salmon originating from Asian rivers compared to 2·3% from North American rivers (reviewed in Myers et al. 1993; Urawa et al. 1998). In addition, M. kisutchi is recovered only from stocks from the Columbia River Basin of Oregon and Washington and vicinities (reviewed in Urawa et al. 1998, 2006). Urawa et al. (1998) used these parasites in Chinook salmon captured in the high seas in 1989–1990 to demonstrate that Asian Chinook salmon that harbour M. arcticus are widely distributed in the North Pacific Ocean, but prove rare in the Bering Sea. In the 1970s the INPFC expanded its interest to anadromous rainbow trout, also known as steelhead (Oncorhynchus mykiss), which range from northern California to the north side of the Alaska Peninsula, mix in the high seas of the North Pacific Ocean and are difficult to distinguish from steelhead originating in Asia (western Kamchatka). Two freshwater digeneans, Plagioporus shawi (adults) and Nanophyetus

salmincola (metacercariae), with distributions restricted by the distribution of their snail intermediate hosts, were examined for their potential to identify the ocean range of steelhead trout originating from the northwestern USA (Margolis, 1984, 1985). Studies conducted on steelhead caught in the central North Pacific in 1986 and 1987 provide evidence that steelhead from the northwestern USA make up a substantial proportion of the Japanese by-catch (summarized in Dalton, 1991). Identification of metacercariae of N. salmincola in additional steelhead samples from Japanese research vessels expands the known western range limit of North American steelhead (Myers et al. 1991). The last year of Japan’s operation of a landbased salmon driftnet fishery on the high seas was 1991 (Myers et al. 1993). This reduced the need for monitoring the stocks of salmon in the high seas and the emphasis of salmon studies became more regional and the scale for detecting differences much smaller. As an example of this, Criscione et al. (2006) show that the genotypes of P. shawi, collected from five

Biological tags of North American fishes

freshwater locations in Oregon and Washington states, are four times more accurate than the genotypes of steelhead (using the baseline available at that time) in assigning fish to their river of origin. This derives from the fact that the digenean possesses a restricted freshwater life cycle (aquatic snail to fish) that subsequently limits dispersal among freshwater drainages. However, Criscione et al. (2006) point out temporal limitations of the technique, in addition to infection restrictions, as P. shawi may not survive long enough in marine waters to provide information on adult steelhead. Despite these limitations, combining genetic assessment of host and parasite seems worthy of future efforts in steelhead stock analyses. Furthermore, a baseline of genotypes for the Myxobolus species mentioned above might prove to again add information on stock structure of salmonids given their parasites’ longevity in the host. In addition to the Pacific salmon, the North Pacific Ocean supports other mixed stock fisheries including Pacific herring, Pacific halibut and other groundfish species, that remain important to those countries sending fishing fleets to the North Pacific Ocean. These studies and others are summarized in Table 1. In general, stock delineation studies have been conducted over large geographic areas for widely distributed marine species such as Pacific halibut (Blaylock et al. 2003) and the neon flying squid (Ommastrephes bartrami) (Nagasawa et al. 1998). In contrast, studies have been conducted on smaller scales for Pacific herring, a few of the approximate 100 rockfish species (Sebastes spp.) and other species with demersal life stages. The use of natural tags in rockfishes that experience barotrauma and do not survive mark– recapture studies may be especially important. On very fine scales, studies on parasites were able to separate stocks of sablefish (Anoplopoma fimbria) at different seamounts off the Canadian coast (Kabata et al. 1988; Whitaker and McFarlane 1997) and identify new recruits to Hawaiian Ridge seamounts for North Pacific armorhead (Pseudopentaceros wheeleri) (Humphreys et al. 1993). To summarize findings in the Pacific, freshwater myxosporeans are shown to be the most useful of the parasites of salmonids. In marine hosts, gill monogeneans and parasitic copepods prove among the most reliable tags. In many cases parasite communities instead of individual parasites can differentiate regional differences. Most recently, and described further below, there has been promise of using genetic structure of parasite populations to more accurately identify stock structure or migration patterns of marine hosts. A R C T I C WAT E R S

While few in number, almost all studies using parasites as biological tags confined exclusively to the Arctic have the goal of distinguishing between

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resident freshwater and anadromous Arctic charr (Salvelinus alpinus). Areas of study include Somerset Island, Baffin Island, Labrador and Greenland (Table 1). Of the studies conducted in the Northwest Atlantic, the only ones which include samples extending into Arctic waters are those on Greenland halibut and Atlantic cod (Templeman et al. 1976; Zubchenko, 1981; Khan et al. 1982) and cod from Greenland (Boje, 1987). Few parasites stand out as potential indicator species in the Arctic. Dick (1984) suggests that Bothrimonus sp. and Brachyphallus sp., among others, are good indicators of sea-run Arctic charr on Victoria Island. He further proposes that the freshwater origin of sea-run charr in estuarine or marine samples may be elucidated by the presence of Cystidicola sp., Eubothrium sp. and Crepidostomum sp. Numbers of these freshwater parasites are reduced but not eliminated in estuarine conditions. However, Dick (1984) cautions that results are system-specific and that each fish population must be evaluated separately. F R E S H WAT E R S

Aside from anadromous fishes, very few studies use parasites as biological tags to discriminate stocks of freshwater fish and all of these are confined to the Great Lakes-St Lawrence Basin (Table 1). However, parasites are used frequently to determine river of origin for anadromous salmonids on both the Pacific and Atlantic coasts (Table 1). Furthermore, they are used to distinguish anadromous from resident fishes in freshwater ecosystems, as in Arctic charr (Eddy and Lankester, 1978; Dick and Belosevic, 1981; Bouillon and Dempson, 1989; Due and Curtis, 1995; Table 1, and see above). Hare and Burt (1976) used parasites to determine tributary of origin for Atlantic salmon (Salmo salar) within the Miramichi River system in New Brunswick. In the nearby Tabusintac River, freshwater parasites indicate foci of infection in freshwater brook charr (Salvelinus fontinalis), whereas a decrease in prevalence of various marine parasites reflect approximate arrival time of anadromous fish from this river (Frimeth, 1987). The distribution of other freshwater parasites suggests that brook charr move between estuaries (Frimeth, 1987). Examination of the parasite fauna of American shad, Alosa sapidissima, led Hogans et al. (1993) to infer that arrival and departure times in the Cumberland Basin of the Bay of Fundy vary among different local riverine populations. In Quebec lakes, parasites also discriminate between littoral and limnetic forms of brook charr more effectively than dietary differences or morphometrics (Bertrand et al. 2008). Clearly there is good potential here to apply these techniques to freshwater fisheries, especially in large lakes such as the Great Lakes, Lake Winnipeg and

David J. Marcogliese and Kym C. Jacobson

Lake Manitoba, and major fluvial systems such as the St Lawrence, Mississippi and Columbia Rivers, where commercial fisheries are well established. This is especially so given that the parasite fauna of commercial freshwater fish in North America is fairly well known (e.g. Margolis and Arthur, 1979; McDonald and Margolis, 1995; Muzzall and Whelan, 2011) and good baseline information already exists. A PROGRESSION OF APPROACHES AND METHODS

Initially only single parasites were considered in tagging studies, but by 1961 Sindermann developed a multi-species approach hoping to prove more powerful and provide more discriminatory information (Sindermann, 1961a). His approach consisted of an analysis of frequency of occurrence of four different parasites from various areas off northeastern North America, to estimate the maximum degree of mixing between any two areas (Sindermann, 1961a). With the development of more advanced statistical methods and better computational capacity, analytical methods and multi-species approaches grew hand in hand, permitting more enhanced discriminatory ability using natural assemblages of parasites as tags. Among the most popular techniques used is stepwise parametric or non-parametric discriminate function analysis (DFA), which measures how accurately a given individual fish fits into one sample vs another (e.g. Arthur and Albert, 1993, 1996; Boje et al. 1997; Blaylock et al. 2003; McClelland et al. 2005; Melendy et al. 2005; McClelland and Melendy, 2007, 2011). The coherence of different samples of fish from across a region can then be assessed using only parasites that significantly contribute to assigning fish to specific samples or areas. With the increasing use of DFA to discriminate stocks, the choice of parasite indicators is based more now on statistical evidence rather than choices made a priori, which were often based on observational data and ease of measurement. An examination of recent studies using DFA, however, does not reveal any consistent commonalities among the various North American studies except that anisakid nematodes, indeed, are often effective at aiding in stock discrimination in the Northwest Atlantic. In addition, although this is a multi-species technique, usually only a small subset of parasites tested proves informative. For example, Blaylock et al. (2003) ultimately used eight parasite taxa of 59 to discriminate Pacific halibut stocks. On the Atlantic side (Fig. 2), for Greenland halibut Arthur and Albert (1993) found only five of 46 parasite taxa (see Arthur and Albert, 1994) to be discriminatory, while Boje et al. (1997) selected three of 21 taxa. For capelin, Arthur and Albert (1996) selected three of 21 taxa (see Arthur et al. 1995). McClelland and Melendy (2007, 2011) found two of 11 and four of nine parasites

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enumerated to be useful in delineating stocks of American plaice and Atlantic cod, respectively, in the Gulf of St Lawrence. Four of 17 parasite taxa proved discriminatory in a DFA of parasites of white hake (Urophycis tenuis) in the Gulf of St Lawrence (Melendy et al. 2005). Lastly, seven of 20 parasite taxa were informative regarding delineation of winter flounder stocks off Nova Scotia (McClelland et al. 2005). While variation in the physiology, morphology and genetics of the target fish species is used extensively to discriminate among fish stocks, few studies consider such variation within those particular parasite species that infect them. In an early study, BeverleyBurton and Pippy (1977) suggest that morphometric variation in length among the whaleworm A. simplex can be used to distinguish stocks of Atlantic herring and Atlantic salmon (S. salar) off eastern Canada. Beverley-Burton (1978) further suggests that allele frequencies could be used to determine migration patterns of Atlantic salmon. More recently, an evaluation of genotype variation using microsatellites demonstrates that the populations of the digenetic trematode P. shawi varies more than those of its host, steelhead trout from five different rivers in Oregon (Criscione et al. 2006). In contrast, Baldwin et al. (2011) could not identify migration patterns or stock structure of Pacific sardine (Sardinops sagax) based upon the population structure (assessed with the cytochrome c oxidase 2 mitochondrial DNA gene) of three species of larval Anisakis, but found a panmictic distribution of haplotypes from southern California to British Columbia. Beverley-Burton (1978) was unable to distinguish North American and British Atlantic salmon among fish collected from Greenland using enzyme allele frequencies. However, use of molecular markers shows that Diplostomum spp. differ for the most part between North American and Eurasian freshwater fishes (Locke et al. unpublished). Hence, use of molecular barcodes can provide a further tool to discriminate between salmonids from North America and those from Europe or Asia in both the Atlantic and Pacific oceans. Indeed, a meta-analysis of molecular markers in digenetic trematodes shows that those with fully aquatic life cycles exhibit more genetic structuring than those infecting birds and mammals as final hosts (BlascoCosta and Poulin, 2013). These authors suggest that genetic differences among parasite populations reflect the mobility of their hosts. Thus, hosts with limited interchange among stocks can be infected with genetically distinct populations of a given parasite species. Of course, information from biological tags should not be used in isolation (Begg and Waldman, 1999; Marcogliese, 2008; Catalano et al. 2013), but rather should be considered in conjunction with the various other standard techniques currently used in fisheries management, including meristics, physical tagging,

Biological tags of North American fishes

population genetics, growth data and otolith structure, to name a few. This is nothing new, and early North American studies that used parasites together with other methods include Templeman (1953) and Sindermann (1957, 1959, 1961b). However, while few published studies actually incorporate multiple techniques, Sindermann (1959) combined the use of parasites as biological tags with serological measurements to differentiate stocks of Atlantic herring from the Gulf of St Lawrence to the New Jersey coast. Templeman (1953) incorporated parasitological data with vertebral counts, growth and maturation rates, and/or mark-recapture techniques in his review of stock structure of Atlantic cod and redfish in the Northwest Atlantic. Nyman and Pippy (1972) examined growth, allele frequencies and two species of parasite to distinguish North American and European Atlantic salmon at sea. Bishop et al. (1988) included studies of meristic characteristics, growth and nematodes in fillets to differentiate Atlantic cod from different banks off southern Newfoundland. Off the coast of New England, Lux (1963) incorporated information from mark-recapture studies, fin ray counts and occurrence of blackspot metacercariae (Cryptocotyle lingua) to differentiate stocks of winter flounder (P. americanus). On the same host species, another excellent recent study combined parasites as biological tags with host population genetic studies using microsatellites to differentiate among four populations off eastern Canada (McClelland et al. 2005). Quinn et al. (1987) also found electrophoretic differences at 23 loci among five wild British Columbian sockeye salmon populations, corroborating parasitological results. The occurrence of the myxosporean M. arcticus was also used in the mid1980s in combination with allozyme variants and freshwater age at migration to help determine stock composition of sockeye salmon caught in fisheries of the northern boundary area of southern Southeast Alaska and northern British Columbia (Pella et al. 1998). This parasite (previously identified as M. neurobius) was also used in combination with five biochemical genetic markers and scale patterns to estimate the contributions of approximately 15 different groups of 51 stocks of sockeye salmon in a British Columbia and Southeast Alaska coast-wide mixedstock fishery (Wood et al. 1989). The fishery of the Pacific sardine may be a prime example of a recent effort that can benefit from such an integrated assessment. This commercially and ecologically important coastal pelagic fishery crashed in the mid 1900s and experienced a recent resurgence in the late 1990s, as far north as Vancouver Island. Believed to be the northern limits of a migration from a southern California spawning stock, the recent fisheries have been managed as one stock. Thus, Baldwin et al. (2012) focused on this fish in a review of the approaches used to assess stock identity of

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marine fishes. This review includes a discussion of fish morphometrics, artificial tags, fish genetics, parasite community analyses and parasite genetics. Whereas fish genetics has not been able to provide information on stock structure, a study of the parasite communities sampled from southern California to Vancouver Island suggests, based on differences in the recovery of the digeneans Lecithaster gibbosus and Myosaccium ecaude, that the coast-wide migration described in the 1940s using artificial tags may not be the current migration pattern (see review by Baldwin et al. 2012). IMPORTANT LESSONS LEARNED ( OR WHAT DID NOT WORK AND WHY)

Although we stated we would not address the criteria outlined in many other studies for what constitutes a ‘good’ tag for a parasite, we discuss some examples of studies that test some of the assumptions behind the various criteria. For example, using a long-term database (1962–1989) of infections of the copepod ectoparasite L. branchialis on artificially tagged Atlantic cod collected and recaptured off Newfoundland and Labrador, Jones and Taggart (1998) tested whether some of the criteria for good biological tags were applicable to this host-parasite system. They found that there was latitudinal variation in infection rates, that infected fish had reduced survival compared with uninfected fish, and that prevalence varied with fish length. Thus, these authors conclude that using L. branchialis as a natural tag of cod populations can be problematic. They do acknowledge that the copepod may be useful to differentiate cod populations that overwinter (see also Templeman and Fleming, 1963). In the Pacific Ocean, the prevalence of the myxosporeans M. arcticus and H. salmincola in sockeye salmon was used to provide estimates of stock composition in British Columbia from 1977 to 1984, until an increase in Myxolobolus-infected sockeye salmon in one stock changed enough to result in a decline in the ability to differentiate among the three stocks (Beacham et al. 1998). Along similar lines, Margolis (1998) cautions that although stable as a qualitative tag, annual variability of H. salmincola in steelhead limits the use of this parasite for quantitative estimates of stock composition. Such results caution that long-term infection dynamics may change so that the value of parasites as tags may not be consistent over time. The lifespan of several freshwater parasites in seawater was evaluated by Bailey et al. (1989). They found that four of their taxa (Diplostomulum sp. metacercaria, Eubothrium sp., Proteocephalus sp. and Neoechinorhynchus salmonis) survived as long in sockeye salmon reared in seawater as those reared in fresh water, demonstrating the importance of testing and validating assumptions of criteria used for the use of parasites as biological tags.

David J. Marcogliese and Kym C. Jacobson

In addition, life histories of fish species may preclude the use of parasites as natural tags. In contrast to sockeye salmon, which typically spend 1–3 years rearing in freshwater lakes before migrating to the ocean, pink salmon (Oncorhynchus gorbuscha) spend only a few days to a few months rearing in fresh water before ocean entry. Thus freshwater parasites as natural tags for this salmon species are not an option. A few marine parasites were identified as having potential, but interannual variability from 1955 to 1957 discouraged further research efforts (Margolis, 1963). Similar to pink salmon, chum salmon (Oncorhynchus keta) also have an all too brief freshwater residency and thus the usefulness of parasites as any type of natural tag would have to rely solely on marine parasite species. WHAT COULD WE LEARN FROM NON-TAGGING STUDIES?

An effective biological tag requires a parasite’s distribution to be limited in one way or another by environmental conditions (Williams et al. 1992). Parasites are known to be good indicators of pollution (Khan and Thulin, 1991; MacKenzie et al. 1995; Marcogliese, 2004, 2005). While the guidelines for the selection of hosts and parasites as biological tags differ somewhat from those for the use of parasites as indicators of pollution, they are not necessarily incompatible (Williams et al. 1992; MacKenzie, 1993; MacKenzie et al. 1995). Indeed, if parasites indicate that fish samples from polluted and unpolluted environments are different, presumably we can assume that the stocks of fish are also different, with no or only limited inter-mixing. Thus, pollution studies that use parasites as indicators may also be used to differentiate among stocks of fish or migration patterns. For example, Siddall et al. (1994) attributes the lack of differences in parasite communities of long rough dab, also known as American plaice, from polluted and unpolluted habitats in the Firth of Clyde, Scotland, to mixing of fish between sites. In contrast, significant differences in the prevalence and abundance of certain parasites in common dab (Limanda limanda) between a dump and reference sites in the Firth of Clyde led the same authors to conclude that these fish do form temporally distinct local populations (Siddall et al. 1994). Communities of silver perch (Bairdiella chrysoura) differ among estuaries along the Florida coast, depending on their contaminant load (Landsberg et al. 1998). While the data were not analysed to search for similarities or differences among the various estuarine parasite communities, the parasite communities in some estuaries clearly differed from others, suggesting that they are composed of different stocks of fish. Using multivariate analyses of parasite communities, samples of spottail shiners (Notropis hudsonius)

84

and johnny darters (Etheostoma nigrum) from different areas of the St Lawrence River in eastern Canada are quite different from each other (Marcogliese et al. 2006; Krause et al. 2010). Also, myxozoan communities in spottail shiners are quite different upstream and downstream of the island of Montreal in the same river (Marcogliese et al. 2009; Krause et al. 2010). Similarly, based on their parasite communities, estuarine and freshwater samples of mummichogs (Fundulus heteroclitus) prove quite different from each other in two New Brunswick rivers (Blanar et al. 2011). While the above studies do not concern commercial fishes, these species are important forage fishes and the information is certainly relevant if any fisheries employ a more comprehensive ecosystem approach or need to comprehend the resource base for a particular commercial fish species. Nevertheless, if discriminating between stocks using results from a pollution study, caution must be taken regarding the choice of discriminating parasites. If environmental conditions are toxic to a parasite, then the absence of that parasite does not necessarily discriminate between fish stocks in and out of a contaminated area. In both tagging and pollution studies, it is advisable to know the environmental limits of the parasites in question (Williams et al. 1992; MacKenzie et al. 1995). Ultimately, we are advocating that data acquired from studies with other primary objectives may provide useful tagging information, analogous to the initial observations on the problematic sealworm and Sphyrion lumpi on Atlantic cod and redfish, respectively, in the Northwest Atlantic. CONCLUSIONS

While a variety of pelagic and demersal fish have been studied on both the Pacific and Atlantic coasts of North America, emphasis has been on Atlantic cod, Atlantic herring and the redfishes in the Atlantic and on the salmonids in the Pacific. Also, close to four times the number of studies has been conducted in the Northwest Atlantic compared with the Pacific. We speculate that this is due to a number of reasons including a longer history of exploitation, more jurisdictional boundaries (e.g. Canadian provinces), and a relatively greater number of exploited species on the east coast. While the reasons for the unbalanced number of studies remain conjecture, on first glance, partitioning of stocks also appears to be greater on the east coast. Differences in bathymetry, topography and hydrography off the two coasts may contribute to the relative disparity in fish stock distinctness between the North Atlantic and the North Pacific. Atlantic fish populations may be separated by deep channels between offshore banks as well as a very heterogeneous coastline with many disrupting features (e.g.

Biological tags of North American fishes

the Gulf of Maine, the Gulf of St Lawrence, the island of Newfoundland). The deep ocean trenches, channels and similar hydrographic features that separate populations of Atlantic cod (Bentzen et al. 1996) and haddock (Zwanenburg et al. 1992), for example, in the northwestern Atlantic are lacking in the Northeast Pacific. Although deep channel fjord systems along the coasts of Southeast Alaska and British Columbia and Washington’s Puget Sound, may separate groundfish and Pacific herring populations, the majority of commercially important Pacific populations may be most influenced by oceanographic currents, water temperature, and even freshwater outflow, which affect the distribution of pelagic and demersal fish species as well as their prey. For the same reason, parasites which prove useful as biological tags on the Atlantic coast, such as the anisakid nematodes, may have fewer barriers to dispersal in Pacific waters. In contrast to Atlantic waters, myxosporeans appear to be excellent tags in the Pacific, especially for salmonids. However, they are rarely used on the Atlantic side of North America (but see Scott, 1981). For those fishes where results from tagging studies are equivocal (e.g. Scott, 1969, 1987; Lubieniecki, 1973; Pippy, 1980; Barse and Hocutt, 1990), further studies using myxosporeans may prove fruitful. Use of more powerful statistical approaches has expanded the range of taxa included in studies of parasites as biological tags. Other promising recent developments include the application of molecular tools to the parasites themselves as indicators of fish host population structure. In addition, the use of parasites as indicators of pollution holds the possibility of contributing to fisheries management because it provides complementary information. Finally, few studies have been conducted off the eastern coast of the USA, and this remains an area open for future research. In addition, with the exception of preliminary work on some large pelagics (see Table 1), we know of no tagging studies in the Caribbean or the Gulf of Mexico. In summary, there are clearly more opportunities for parasites to contribute information on stock delineation and migration of North American fishes. Host genetic tools are replacing the usefulness of parasites for some species, but not all. Nevertheless, parasites have and can continue to provide much needed information on fish behaviour (e.g. migration patterns, habitat preference, nursery grounds) in concert with stock identification obtained through host genetics and other complementary techniques.

ACKNOWLEDGEMENTS

We would like to thank Cheryl Morgan of the Oregon State University Cooperative Institute for Marine Resources Studies for extensive and invaluable assistance with Table 1 and organization of the literature. Dr Kate Meyers also

85 provided insightful discussion and commentary on Pacific salmon. Dr Jane L. Cook is graciously acknowledged for comments on the manuscript. We also are grateful to Andrée Gendron for preparing Fig. 1.

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