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.
Similar content being viewed by others
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
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
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
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
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
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
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
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
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
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
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
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
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
Buchmann K (2007) Fish parasitological methods - classical and molecular techniques. Biofolia, Frederiksberg
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
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
Chai JY, Murrell KD (2005) Fish-borne parasitic zoonoses. Int J Parasitol 35:1233–1241
Chandra CV, Khan RA (1988) Nematode infestation of fillets from Atlantic cod, Gadus morhua, off eastern Canada. J Parasitol 74:1038–1040
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
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
Dogiel VA, Bychovsky BE (1939) Parasites of fishes of the Caspian Sea. Trudy Kompleksnoi izucheniyu Kaspiiskogo morya 7:1–150
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
Fagerholm (1982) Fish in Finland. Acta Academiae Aboensis 5:1–128
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
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
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
Getsevitjute S (1955) Seasonal parasitic infection of Baltic cod liver. Trudy Akad Nauk Lit SSR Ser B 2:127–129 (in Russian)
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
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
Hemmingsen W, MacKenzie K (2001) The parasite fauna of the Atlantic cod, Gadus morhua L. Adv Mar Biol 40:1–80
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
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
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
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
ICES-Fish Map (2005) Cod (Gadus morhua). ICES Species Factsheet Jan 13:2018
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
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
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
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
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
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
MacKenzie K (1999) Parasites as pollution indicators of marine ecosystems: a proposed early warning system. Mar Pollut Bull 38:955–959
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
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
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
McClelland G (2002) The trouble with sealworms (Pseudoterranova decipiens species complex, Nematoda). Parasitology 124:183–203
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
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
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
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
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
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
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
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
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
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
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
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
Ólafsdóttir D, Hauksson E (1998) Anisakid nematodes in the common seal (Phoca vitulina L.) in icelandic waters. Sarsia 83:309–316
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
Petrushevski GK, Shulman GG (1955) Infection of Baltic cod liver with roundworms. Trud Akad Nauk Lit SSR Ser B 2:119–125 (in Russian)
Platt NE (1973) The incidence of codworm in stocks of cod from Greenland and Iceland waters. ICES Council Meeting Document F 28:1–7
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
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
Poulin R (1992) Toxic pollution and parasitism in freshwater fish. Parasitol Today 8:58–61
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
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
Rosing-Asvid A, Teilmann J, Dietz R, Tange Olsen M (2010) First confirmed record of grey seals in Greenland. ARCTIC Journal 63:471–473
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
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
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
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
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
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
Wieland K, Storr-Paulsen M (2005) Spawning and life history information for North Atlantic cod stocks. ICES Coop Res Rep 274:39–49
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
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
Acknowledgements
The authors owe their thanks to Royal Greenland for providing frozen liver samples and data from their Atlantic cod fishery in West Greenland.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Section Editor: Simonetta Mattiucci
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-020-06807-z