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Anisakid nematode larvae in the liver of Atlantic cod Gadus morhua L. from West Greenland

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Abstract

Anisakid nematode larvae occur frequently in the liver of Atlantic cod, but merely few infection data from cod in waters around Greenland exist. The present study reports the occurrence of third-stage anisakid larvae in the livers of 200 Atlantic cod caught on fishing grounds along the West coast of Greenland (fjord systems of Maniitsoq) in May, June, August and September 2017. Classical and molecular helminthological techniques were used to identify the nematodes. A total of 200 cod livers were examined, and 194 were infected with third-stage nematode larvae (overall prevalence of infection 97%) with a mean intensity of 10.3 (range between 1 and 44 parasites per fish). Prevalences recorded were 96% for Anisakis simplex (s.l.), 55% for Pseudoterranova decipiens (s.l.) and 8% for Contracaecum osculatum (s.l.). Sequencing the mtDNA cox2 from 8 out of 23 these latter larvae conferred these to C. osculatum sp. B. A clear seasonal variation was observed, with a rise in A. simplex (s.l.) and P. decipiens (s.l.) occurrence in June and August and a decline in September. The study may serve as a baseline for future investigations using the three anisakids as biological indicators in Greenland waters.

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References

  • Abollo E, Pascual S (2000) An SEM study of Phocascaris cystophorae Berland, 1964 (Nematoda: Anisakidae), a parasite of the hooded seal Cystophora cristata. Syst Parasitol 51:155–158

    Article  Google Scholar 

  • Ackman RG (1976) Volatile ketones and alcohols of codworms (Terranova decipiens) from axenic culture and fresh fish muscle. J Fish Res Board Can 33:2819–2821

    Article  CAS  Google Scholar 

  • Ackman RG, Gjelstad RT (1975) Gas-chromatographic resolution of isomeric pentanols and pentanones in identification of volatile alcohols and ketones in codworm Terranova decipiens (Krabbe, 1878). Anal Biochem 67:684–687

    Article  CAS  PubMed  Google Scholar 

  • ICES Advisory Committee (2017) ICES NWWG report 2017: report of the North Western Working Group (NWWG) - cod (Gadus morhua) in NAFO Subdivisions 1A-1E (Offshore West Greenland). ICES 332–368

  • Aspholm PE (1995) Anisakis simplex Rudolphi, 1809, infection in fillets of Barents Sea cod Gadus morhua L. Fish Res 23:375–379

    Article  Google Scholar 

  • Aspholm PE, Ugland KI, Jodestol KA, Berland B (1995) Seal worm (Pseudoterranova decipiens) infection in common seals (Phoca vitulina) and potential intermediate fish hosts from the outer Oslo Fjord. Int J Parasitol 25:367–373

    Article  CAS  PubMed  Google Scholar 

  • Boily F, Marcogliese DJ (1995) Geographical variations in abundance of larval anisakine nematodes in Atlantic cod (Gadus morhua) and American plaice (Hippoglossoides platessoides) from the Gulf of St. Lawrence. Can J Fish Aquat Sci 52:105–115

    Article  Google Scholar 

  • Boje J, Riget F, Køie M (1997) Helminth parasites as biological tags in population studies of Greenland halibut (Reinhardtius hippoglossoides (Walbaum)), in the north-west Atlantic. ICES J Mar Sci 54:886–895

    Article  Google Scholar 

  • Bonanomi S, Pellissier L, Therkildsen NO, Hedeholm RB, Retzel A, Meldrup D, Olsen SM, Nielsen A, Pampoulie C, Hemmer-Hansen J, Wisz MS, Grønkjær P, Nielsen EE (2015) Archived DNA reveals fisheries and climate induced collapse of a major fishery. Nature Sci Rep 5:1–8

    Google Scholar 

  • Bonanomi S, Therkildsen NO, Retzel A, Hedeholm RB, Pedersen MW, Meldrup D, Pampoulie C, Hansen JH, Grønkjær P, Nielsen EE (2016) Historical DNA documents long distance natal homing in marine fish. Mol Ecol 25:2727–2734

    Article  CAS  PubMed  Google Scholar 

  • Brattey J, Bishop CA (1992) Larval Anisakis simplex (Nematoda: Ascaridoidea) infection in the musculature of Atlantic cod, Gadus morhua, from Newfoundland and Labrador. Can J Fish Aquat Sci 49:2635–2647

    Article  Google Scholar 

  • Brattey J, Clark KJ (1992) Effect of temperature on egg hatching and survival of larvae of Anisakis simplex B (Nematoda: Ascaridoidea). Can J Zool 70:274–279

    Article  Google Scholar 

  • Brattey J, Bishop CA, Ransom AM (1990) Geographic distribution and abundance of Pseudoterranova decipiens (Nematoda: Ascaridoidea) in the musculature of Atlantic cod, Gadus morhua, from Newfoundland and Labrador. Can J Fish Aquat Sci 222:67–82

    Google Scholar 

  • Buch E, Horsted SA, Hovgård H (1994) Fluctuations in the occurrence of cod in Greenland waters and their possible causes. ICES Mar Sci Symp 198:158–174

    Google Scholar 

  • Buchmann K (2007) Fish parasitological methods - classical and molecular techniques. Biofolia, Frederiksberg

    Google Scholar 

  • Buchmann K, Kania PW (2012) Emerging Pseudoterranova decipiens (Krabbe, 1878) problems in Baltic cod, Gadus morhua L., associated with grey seal colonization of spawning grounds. J Fish Dis 35:861–866

    Article  CAS  PubMed  Google Scholar 

  • Buchmann K, Mehrdana F (2016) Effects of anisakid nematodes Anisakis simplex (s.l.), Pseudoterranova decipiens (s.l.) and Contracaecum osculatum (s.l.) on fish and consumer health. Food Waterb Parasitol 4:13–22

    Article  Google Scholar 

  • Chai JY, Murrell KD (2005) Fish-borne parasitic zoonoses. Int J Parasitol 35:1233–1241

    Article  PubMed  Google Scholar 

  • Chandra CV, Khan RA (1988) Nematode infestation of fillets from Atlantic cod, Gadus morhua, off eastern Canada. J Parasitol 74:1038–1040

    Article  CAS  PubMed  Google Scholar 

  • Cohen DM, Inada T, Iwamoto T, Scialabba N (1990) Gadiform fishes of the world (order Gadiformes): an annotated and illustrated catalogue of cods, hakes, grenadiers and other gadiform fishes known to date. FAO Species Catalogue 10:40–48

    Google Scholar 

  • Coltman DW, Stenson G, Hammill MO, Haug T, Davis CS, Fulton TL (2007) Panmictic population structure in the hooded seal (Cystophora cristata). Mol Ecol 16:1639–1648

    Article  CAS  PubMed  Google Scholar 

  • Dogiel VA, Bychovsky BE (1939) Parasites of fishes of the Caspian Sea. Trudy Kompleksnoi izucheniyu Kaspiiskogo morya 7:1–150

    Google Scholar 

  • Dzido J, Kijewska A, Rokicha M, Swiatalska-Koseda A, Rokicki J (2009) Report on anisakid nematodes in polar regions – preliminary results. Polar Science 3:207–2011

    Article  Google Scholar 

  • Fagerholm (1982) Fish in Finland. Acta Academiae Aboensis 5:1–128

    Google Scholar 

  • Fowler M, Stobo WT (2001) Patterns of abundance and maturity among three species of parasitic nematodes (Pseudoterranova decipiens, Contracaecum osculatum, Anisakis simplex) co-existing in Sable Island grey seals (Halichoerus grypus). NAMMCO Sci Publ 3:149–160

    Article  Google Scholar 

  • Fowler M, Stobo WT (2011) Abundance and maturity of three species of parasitic anisakine nematodes (Pseudoterranova decipiens, Contracaecum osculatum, Anisakis simplex) occurring in Sable Island harbour seals (Phoca vitulina). Can J Zool 80:442–449

    Google Scholar 

  • Gay M, Bao M, MacKenzie K, Pascual S, Buchmann K, Bourgau O, Couvreur C, Mattiucci S, Paoletti M, Hastie LC, Levsen A, Pierce GJ (2018) Infection levels and species diversity of ascaridoid nematodes in Atlantic cod, Gadus morhua, are correlated with geographic area and fish size. Fish Res 202:90–102

    Article  Google Scholar 

  • Getsevitjute S (1955) Seasonal parasitic infection of Baltic cod liver. Trudy Akad Nauk Lit SSR Ser B 2:127–129 (in Russian)

    Google Scholar 

  • Greenland Institute of Natural Resources (2019) www.natur.gl/en/birds-and-mammals/marine-mammals

  • Haarder S, Kania PW, Galatius A, Buchmann K (2014) Increased Contracaecum osculatum infection in baltic cod (Gadus morhua) livers (1982-2012) associated with increasing grey seal (Halichoerus gryphus) populations. J Wildl Dis 50:537–543

    Article  CAS  PubMed  Google Scholar 

  • Hauksson E (2011) The prevalence, abundance, and density of Pseudoterranova sp.a larvae in the flesh of cod (Gadus morhua) relative to proximity of grey seal (Halichoerus grypus) colonies on the coast off Drangar, Northwest Iceland. J Mar Biol 23:1687–9481

    Google Scholar 

  • Hemmingsen W, MacKenzie K (2001) The parasite fauna of the Atlantic cod, Gadus morhua L. Adv Mar Biol 40:1–80

    Article  Google Scholar 

  • Hemmingsen W, Lombardo I, MacKenzie K (1991) Parasites as biological tags for cod, Gadus morhua L., in northern Norway: a pilot study. Fish Res 12:365–373

    Article  Google Scholar 

  • Hemmingsen W, Halvorsen O, MacKenzie K (2000) The occurrence of some metazoan parasites of Atlantic cod, Gadus morhua L., in relation to age and sex of the host in Balsfjord (70°N), North Norway. Polar Biol 23:368–372

    Article  Google Scholar 

  • Herrington WC, Bearse HM, Firth FE (1939) Observations on the life history, occurrence and distribution of the redfish parasite Sphyrion lumpi. United States Bureau of Fisheries Special Report 5:1–18

    Google Scholar 

  • Højgaard PD (1998) Impact of temperature, salinity, and light on hatching of eggs of Anisakis simplex (Nematoda, Anisakidae) isolated by a new method and some remarks on survival of larvae. Sarsia 83:21–28

    Article  Google Scholar 

  • ICES-Fish Map (2005) Cod (Gadus morhua). ICES Species Factsheet Jan 13:2018

    Google Scholar 

  • Jensen T, Idås K (1992) Infection with Pseudoterranova decipiens (Krabbe, 1878) larvae in cod (Gadus morhua) relative to proximity of seal colonies. Sarsia 76:227–230

    Article  Google Scholar 

  • Johansen CE (2010) Helminth parasites in ringed seals (Pusa hispida) from Svalbard, Norway with special emphasis on nematodes: variation with age, sex, diet, and location of host. J Parasitol 96:946–953

    Article  PubMed  Google Scholar 

  • Klapper R, Carballeda-Sangiao N, Kuhn T, Jensen HM, Buchmann K, Gonzalez-Muñoz M, Karl H (2018) Anisakid infection levels in fresh and canned cod liver: significant reduction through liver surface layer removal. Food Control 92:17–24

    Article  CAS  Google Scholar 

  • Klimpel S, Palm HW, Rückert S, Piatkowski U (2004) The life cycle of Anisakis simplex in the Norwegian Deep (northern North Sea). Parasitol Res 94:1–9

    Article  PubMed  Google Scholar 

  • Link JS, Garrison L (2002) Trophic ecology of Atlantic cod Gadus morhua on the Northeast US Continental Shelf. Mar Ecol Progr Ser 227:109–123

    Article  Google Scholar 

  • Lunneryd S, Boström MK, Aspholm PE (2015) Sealworm (Pseudoterranova decipiens) infection in grey seals, cod and shorthorn sculpin in the Baltic Sea. Parasitol Res 114:257–264

    Article  PubMed  Google Scholar 

  • MacKenzie K (1999) Parasites as pollution indicators of marine ecosystems: a proposed early warning system. Mar Pollut Bull 38:955–959

    Article  CAS  Google Scholar 

  • MacKenzie K, Abaunza P (1998) Parasites as biological tags for stock discrimination of marine fish: a guide to procedures and methods. Fish Res 38:45–56

    Article  Google Scholar 

  • Marcogliese DJ (2001) Distribution and abundance of sealworm (Pseudoterranova decipiens) and other anisakid nematodes in fish and seals in the Gulf of St. Lawrence: potential importance of climatic conditions. NAMMCO Scientific Publications 3: 113–128

  • Mattiucci S, Nascetti G (2008) Advances and trends in the molecular systematics of anisakid nematodes, with implications for their evolutionary ecology and host-parasite co-evolutionary processes. Adv Parasitol 66:47–148

    Article  PubMed  Google Scholar 

  • Mattiucci S, Cipriani P, Paoletti M, Levsen A, Nascetti G (2017) Reviewing biodiversity and epidemiological aspects of anisakid nematodes from the North-east Atlantic Ocean. J Helminthol 91:422–439

    Article  CAS  PubMed  Google Scholar 

  • McClelland G (2002) The trouble with sealworms (Pseudoterranova decipiens species complex, Nematoda). Parasitology 124:183–203

    Article  Google Scholar 

  • McClelland G, Misra RK, Martell DJ (1985) Variations in abundance of larval anisakines, sealworm (Pseudoterranova decipiens) and related species, in eastern Canadian cod and flatfish. Can Tech Rep Fish Aquat Sci 1392:1–57

    Google Scholar 

  • McClelland G, Misra RK, Martell DJ (1990) Larval anisakine nematodes in various fish species from Sable Island Bank and vicinity. Can J Fish Aquat Sci 222:83–118

    Google Scholar 

  • Measures LN (1996) Effect of temperature and salinity on development and survival of eggs and free-living larvae of sealworm (Pseudoterranova decipiens). Can J Fish Aquat Sci 53:2804–2807

    Article  Google Scholar 

  • Measures LN, Béland P, Martineau D, De Guise S (1995) Helminths of an endangered population of belugas, Delphinapterus leucas, in the St. Lawrence estuary, Canada. Can J Zool 73:1402–1409

    Article  Google Scholar 

  • Mehrdana F, Bahlool Q, Skov J, Marana M, Sindberg D, Mundeling M, Overgaard B, Korbut R, Strøm S, Kania P, Buchmann K (2014) Occurrence of zoonotic nematodes Pseudoterranova decipiens, Contracaecum osculatum and Anisakis simplex in cod from the Baltic Sea. Vet Parasitol 205:581–587

    Article  PubMed  Google Scholar 

  • Mehrdana F, Bahlool Q, Skov J, Marana M, Sindberg D, Mundeling M, Overgaard BC, Korbut R, Strøm S, Kania PW, Buchmann K (2015) Occurrence of zoonotic nematodes Pseudoterranova decipiens, Contracaecum osculatum and Anisakis simplex in cod (Gadus morhua) from the Baltic Sea. Vet Parasitol 205:581–587

    Article  Google Scholar 

  • Mouritsen KN, Hedeholm R, Schack HB, Møller LN, Storr-Paulsen M, Dzido J, Rokichi J (2010) Occurrence of anisakid nematodes in Atlantic cod (Gadus morhua) and Greenland cod (Gadus ogac), West Greenland. Acta Parasitol 55:81–89

    Article  Google Scholar 

  • Münster J, Klimpel S, Fock HO, MacKenzie K, Kuhn TA (2015) Parasites as biological tags to track an ontogenetic shift in the feeding behaviour of Gadus morhua off West and East Greenland. Parasitol Res 114:2723–2733

    Article  PubMed  Google Scholar 

  • Myjak P, Szostakowska B, Wojciechowski J, Pietkiewicz H, Rokicki J (1994) Anisakid larvae in cod from the southern Baltic Sea. Arch Fishery Mar Res 42:149–161

    Google Scholar 

  • Nadler SA, Hudspeth DS (2000) Phylogeny of the Ascaridoidea (Nematoda: Ascaridida) based on three genes and morphology: hypotheses of structural and sequence evolution. J Parasitol 86:380–393

    Article  CAS  PubMed  Google Scholar 

  • Nadolna K, Podolska M (2014) Anisakid larvae in the liver of cod (Gadus morhua L.) from the Southern Baltic Sea. J Helminthol 88:237–246

    Article  CAS  PubMed  Google Scholar 

  • Nielsen RJ, Andersen M (2001) Feeding habits and density patterns of Greenland cod, Gadus ogac (Richardson 1836), at West Greenland compared to those of coexisting Atlantic cod, Gadus morhua L. J Northw Atl Fish Sci 29:1–22

    Article  Google Scholar 

  • Ólafsdóttir D, Hauksson E (1998) Anisakid nematodes in the common seal (Phoca vitulina L.) in icelandic waters. Sarsia 83:309–316

    Article  Google Scholar 

  • Overgaard-Therkildsen N, Hemmer-Hansen J, Hedeholm RB, Wisz MS, Pampoulie C, Meldrup D, Bonanomi S, Retzel A, Malskær Olsen S, Nielsen EE (2013) Spatiotemporal SNP analysis reveals pronounced biocomplexity at the northern range margin of Atlantic cod Gadus morhua. Evol Appl 6:690–705

    Article  Google Scholar 

  • Petrushevski GK, Shulman GG (1955) Infection of Baltic cod liver with roundworms. Trud Akad Nauk Lit SSR Ser B 2:119–125 (in Russian)

    Google Scholar 

  • Platt NE (1973) The incidence of codworm in stocks of cod from Greenland and Iceland waters. ICES Council Meeting Document F 28:1–7

    Google Scholar 

  • Platt NE (1975) Infestation of cod (Gadus morhua L.) with larvae of codworm (Terranova decipiens Krabbe) and herringworm (Anisakis sp. Nematoda Ascaridata), in North Atlantic and Arctic waters. J Appl Ecol 12:437–450

    Article  Google Scholar 

  • Platt NE (1976) Codworm - a possible biological indicator of the degree of mixing of Greenland and Iceland cod stocks. ICES J Mar Sci 37:41–45

    Article  Google Scholar 

  • Poulin R (1992) Toxic pollution and parasitism in freshwater fish. Parasitol Today 8:58–61

    Article  CAS  PubMed  Google Scholar 

  • Poulin R (2000) Variation in the intraspecific relationship between fish length and intensity of parasitic infection: biological and statistical causes. J Fish Biol 56:123–137

    Article  Google Scholar 

  • Pufall EL, Jones-Bitton A, McEwen SA, Brown TM, Edge VL, Rokicki J, Karpiej K, Peregrine AS, Simard M (2012) Prevalence of zoonotic anisakid nematodes in Inuit-harvested fish and mammals from the eastern Canadian Arctic. Foodb Pathog Dis 9:1002–1009

    Article  Google Scholar 

  • Rosing-Asvid A, Teilmann J, Dietz R, Tange Olsen M (2010) First confirmed record of grey seals in Greenland. ARCTIC Journal 63:471–473

    Google Scholar 

  • Skov J, Kania PW, Marana Olsen M, Lauridsen JH, Buchmann K (2009) Nematode infections of maricultured and wild fishes in Danish waters: a comparative study. Aquaculture 1:24–28

    Article  Google Scholar 

  • Sokolova M, Buchmann K, Huwer B, Kania PW, Krumme U, Galatius A, Hemmer-Hansen J, Behrens JW (2018) Spatial patterns in infection of cod Gadus morhua with the seal-associated liver worm Contracaecum osculatum from the Skagerrak to the central Baltic Sea. Mar Ecol Progr Ser 606:105–118

    Article  Google Scholar 

  • Storr-Paulsen M, Wieland K (2006) Den Atlantiske torsk i de grønlandske farvande 2005. Pinngortitaleriffik, Grønlands Naturinstitut, Teknisk Rapport:1–15 (In Danish)

  • Thorsteinsson V, Marteinssdottir G (1998) Size specific time and duration of spawning of cod (Gadus morhua) in Icelandic waters. ICES 5:18

    Google Scholar 

  • Ugland KI, Strømnes E, Berland B, Aspholm PE (2004) Growth, fecundity and sex ratio of adult whaleworm (Anisakis simplex; Nematoda, Ascaridoidea, Anisakidae) in three whale species from the North-East Atlantic. Parasitol Res 92:484–489

    Article  PubMed  Google Scholar 

  • Valtonen ET, Fagerholm HP, Helle E (1988) Contracaecum osculatum (Nematoda, Anisakidae) in fish and seals in Bothnian Bay (northeastern Baltic Sea). Int J Parasitol 18:365–370

    Article  CAS  PubMed  Google Scholar 

  • Wieland K (2002) Distribution and drift of Atlantic cod (Gadus morhua) eggs and larvae in Greenland offshore waters. J Northw Atl Fish Sci 30:61–76

    Article  Google Scholar 

  • Wieland K, Storr-Paulsen M (2005) Spawning and life history information for North Atlantic cod stocks. ICES Coop Res Rep 274:39–49

    Google Scholar 

  • Zhu XQ, D'amelio S, Palm HW, Paggi L, George-Nascimento M, Gasser RB (2002) SSCP-based identification of members within the Pseudoterranova decipiens complex (Nematoda: Ascaridoidea: Anisakidae) using genetic markers in the internal transcribed spacers of ribosomal DNA. Parasitology 124:615–623

    Article  CAS  PubMed  Google Scholar 

  • Zuo S, Kania PW, Mehrdana F, Marana MH, Buchmann K (2018) Contracaecum osculatum and other anisakid nematodes in grey seals and cod in the Baltic Sea: molecular and ecological links. J Helminthol 92:81–89

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors owe their thanks to Royal Greenland for providing frozen liver samples and data from their Atlantic cod fishery in West Greenland.

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Severin, N.L., Yurchenko, M., Sørensen, J.S. et al. Anisakid nematode larvae in the liver of Atlantic cod Gadus morhua L. from West Greenland. Parasitol Res 119, 3233–3241 (2020). https://doi.org/10.1007/s00436-020-06807-z

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