Acta Parasitologica

, Volume 59, Issue 2, pp 284–293 | Cite as

Annual and spatial variability in endo- and ectoparasite infections of North Sea cod (Gadus morhua Linnaeus, 1758) larvae, post-larvae and juveniles

  • Foojan Mehrdana
  • Qusay Z. M. Bahlool
  • Alf Skovgaard
  • Jesper A. Kuhn
  • Per W. Kania
  • Peter Munk
  • Kurt Buchmann
Original Paper


A parasitological investigation was performed on a total of 5380 Atlantic cod larvae, post-larvae and small juveniles sampled from the North Sea during a period of five years. The copepod Caligus elongatus (Von Nordmann, 1832) and the nematode Hysterothylacium aduncum (Rudolphi, 1802) were found at a relatively high prevalence of infection (4.6% and 5.2%, respectively). The infection by both parasites showed annual and spatial variability. C. elongatus showed a higher prevalence in 1992 compared to the following years, whereas the prevalence of H. aduncum increased from 1992 to 2001.We observed a relation between parasite distribution and parameters such as latitude and water depth. Adult digeneans (Lecithaster gibbosus and Derogenes varicus) and larval cestodes were also found with lower infection rates. Since changes of infection levels coincided with increasing North Sea water temperature in the studied period, it is hypothesized that temperature may affect parasite population levels. However, it is likely that other environmental factors may contribute to the observed variations. Absence of infection intensities higher than one nematode per fish in small larvae and post-larvae suggests that host survival may be affected by a high infection pressure. The relatively high levels of infection in the younger stages of cod, and the annual/spatial variability of these infections should be considered in the understanding of the early life dynamics of the species.


Atlantic cod North Sea Hysterothylacium aduncum Caligus elongatus growth temperature latitude 


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  1. Andersen K. 1993. Hysterothylacium aduncum (Rudolphi, 1862) infection in cod from the Oslofjord: seasonal occurrence of third- and fourth-stage larvae as well as adult worms. Parasitology Research, 79, 67–72.PubMedCrossRefGoogle Scholar
  2. Anderson R.M., May R.M. 1978. Regulation and stability of hostparasite population interactions: I. Regulatory processes. Journal of Animal Ecology, 47, 219–247.CrossRefGoogle Scholar
  3. Barta J.R., Martin D.S., Liberator P.A., Dashkevicz M., Anderson J.W., Feighner S.D., Elbrecht A., Perkins-Barrow A., Jenkins M.C., Danforth H.D., Ruff M.D., Profous-Juchelka H. 1997. Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. The Journal of Parasitology, 83, 262–271.PubMedCrossRefGoogle Scholar
  4. Berland B. 1961. Nematodes from some Norwegian marine fishes. Sarsia, 2, 1–50. DOI: 10.1080/00364827.1961.10410245.Google Scholar
  5. Buchmann K. 2012. Fish immune responses against endoparasitic nematodes — experimental models. Journal of Fish Diseases, 35, 623–635. DOI: 10.1111/j.1365-2761.2012.01385.x.PubMedCrossRefGoogle Scholar
  6. Bush A.O., Lafferty K.D., Lotz J.M., Shostak A.W. 1997. Parasitology meets ecology on its own terms: Margolis et al. Revisited. The Journal of Parasitology, 83, 575–583.CrossRefGoogle Scholar
  7. Campana S.E. 1983. Feeding periodicity and the production of daily growth increments in otoliths of steelhead trout (Salmo gairdneri) and starry flounder (Platichthys stellatus). Canadian Journal of Zoology, 61, 1591–1597. DOI: 10.1139/z83-214.CrossRefGoogle Scholar
  8. Campana S.E. 1984. Interactive effects of age and environmental modifiers on the production of daily growth increments in otoliths of plainfin midshipman, Porichthys notatus. Fishery Bulletin, 82, 165–177.Google Scholar
  9. Chettri J.K., Raida M.K., Kania P.W., Buchmann K. 2012. Differential immune response of rainbow trout (Oncorhynchus mykiss) at early developmental stages (larvae and fry) against the bacterial pathogen Yersinia ruckeri. Developmental and Comparative Immunology, 36, 463–474. DOI: 10.1016/j.dci.2011.08.014.PubMedCrossRefGoogle Scholar
  10. Conley D.C., Curtis M.A. 1993. Effects of temperature and photoperiod on the duration of hatching, swimming, and copepodid survival of the parasitic copepod Salmincola edwardsii. Canadian Journal of Zoology, 71, 972–976. DOI: 10.1139/z93-128.CrossRefGoogle Scholar
  11. Fagerholm H.P. 1982. Parasites of fish in Finland: IV. Nematodes. Åbo Akademi, Finland, 128 pp.Google Scholar
  12. Folkvord A. 2005. Comparison of size-at-age of larval Atlantic cod (Gadus morhua) from different populations based on size and temperature-dependent growth models. Canadian Journal of Fisheries and Aquatic Sciences, 62, 1037–1052. DOI: 10.1139/F05-008.CrossRefGoogle Scholar
  13. González L., Carvajal J. 2003. Life cycle of Caligus rogercresseyi, (Copepoda: Caligidae) parasite of Chilean reared salmonids. Aquaculture, 220, 101–117. DOI: 10.1016/S0044-8486(02)00512-4.CrossRefGoogle Scholar
  14. Hemmingsen W., MacKenzie K. 2001. The parasite fauna of the Atlantic cod, Gadus morhua L. Advances in Marine Biology, 40, 2–60. DOI: 10.1016/S0065-2881(01)40002-2.Google Scholar
  15. Heuch P.A., Jansen P.A., Hansen H., Sterud E., MacKenzie K., Haugen P., Hemmingsen W. 2011. Parasite faunas of farmed cod and adjacent wild cod populations in Norway: a comparison. Aquaculture Environment Interactions, 2, 1–13. DOI: 10.3354/aei00027.CrossRefGoogle Scholar
  16. Hogans W.E. 1995. Infection dynamics of sea lice, Lepeophtheirus salmonis (Copepoda: Caligidae): parasitic on Atlantic salmon (Salmo salar) cultured in marine waters of the Lower Bay of Fundy. Canadian Technical Report of Fisheries and Aquatic Sciences, Canada, 2067, 10 pp.Google Scholar
  17. Horwood J., O’Brien C., Darby C. 2006. North Sea cod recovery? ICES Journal of Marine Science, 63, 961–968. DOI: 10.1016/j.icesjms.2006.05.001.CrossRefGoogle Scholar
  18. Johnson S.C., Treasurer J.W., Bravo S., Nagasawa K., Kabata Z. 2004. A review of the impact of parasitic copepods on marine aquaculture. Zoological Studies, 43, 229–243.Google Scholar
  19. Kabata Z. 1979. Parasitic Copepoda of British Fishes. The Ray Society Publications, London, 720 pp.Google Scholar
  20. Karlsbakk E., Otterlei E., Høie H., Nylund A. 2001. Parasites of cultured cod (Gadus morhua) postlarvae fed natural zooplankton. Bulletin of the European Association of Fish Pathologists, 21, 63–70.Google Scholar
  21. Kennedy C.R. 1975. Dispersion of parasites within a host-parasite system. In: Ecological animal parasitology. Blackwell Scientific Publications, Oxford, London, Edinburgh, Melbourne, 61–75.Google Scholar
  22. Khan R.A. 2004. Disease outbreaks and mass mortality in cultured Atlantic cod, Gadus morhua L., associated with Trichodina murmanica (Ciliophora). Journal of Fish Diseases, 27, 181–184. DOI: 10.1111/j.1365-2761.2004.00525.x.PubMedCrossRefGoogle Scholar
  23. Khan R.A. 2012. Host-parasite interactions in some fish species. Journal of Parasitology Research, 2012, 7 pages. DOI: 10.1155/2012/237280.Google Scholar
  24. Køie M. 1984. Digenetic trematodes from Gadus morhua L. (Osteichthyes, Gadidae) from Danish and adjacent waters, with special reference to their life histories. Ophelia, 23, 195–222. DOI: 10.1080/00785326.1984.10426614.CrossRefGoogle Scholar
  25. Køie M. 1993. Aspects of the life cycle and morphology of Hysterothylacium aduncum (Rudolphi, 1802) (Nematoda, Ascaridoidea, Anisakidae). Canadian Journal of Zoology, 71, 1289–1296. DOI: 10.1139/z93-178.CrossRefGoogle Scholar
  26. MacKinnon B.M. 1993. Host response of Atlantic salmon (Salmo salar) to infection by sea lice (Caligus elongatus). Canadian Journal of Fisheries and Aquatic Sciences, 50, 789–792. DOI: 10.1139/f93-09150:789-792.CrossRefGoogle Scholar
  27. Nielsen R., Munk P. 2004. Growth pattern and growth dependent mortality of larval and pelagic juvenile North Sea cod Gadus morhua. Marine Ecology Progress Series, 278, 261–270. DOI: 10.3354/meps278261.CrossRefGoogle Scholar
  28. Øines Ø, Simonsen J.H., Knutsen J.A., Heuch P.A. 2006. Host preference of adult Caligus elongatus Nordmann in the laboratory and its implications for Atlantic cod aquaculture. Journal of Fish Diseases, 29, 167–174. DOI: 10.1111/j.1365-2761.2006.00702.x.PubMedCrossRefGoogle Scholar
  29. Perdiguero-Alonso D., Montero F.E., Raga J.A., Kostadinova A. 2008. Composition and structure of the parasite faunas of cod, Gadus morhua L. (Teleostei: Gadidae), in the Northeast Atlantic. Parasites and Vectors, 1, 23. DOI: 10.1186/1756-3305-1-23.PubMedCentralPubMedCrossRefGoogle Scholar
  30. Piasecki W. 1996. The developmental stages of Caligus elongatus von Nordmann, 1832 (Copepods: Caligidae). Canadian Journal of Zoology, 74, 1459–1478. DOI: 10.1139/z96-161.CrossRefGoogle Scholar
  31. Revie C.W., Gettinby G., Treasurer J.W., Rae G.H., Clark N. 2002. Temporal, environmental and management factors influencing the epidemiological patterns of sea lice (Lepeophtheirus salmonis) infestations on farmed Atlantic salmon (Salmo salar) in Scotland. Pest Management Science, 58, 576–584. DOI: 10.1002/ps.476.PubMedCrossRefGoogle Scholar
  32. Schrøder M.B., Villena A.J., Jørgensen T.O. 1998. Ontogeny of lymphoid organs and immunoglobulin producing cells in Atlantic cod (Gadus morhua L.). Developmental and Comparative Immunology, 22, 507–517. DOI: 10.1016/S0145-305X(98)00030-5.PubMedCrossRefGoogle Scholar
  33. Secor D.H., Dean J.M., Laban E.H. 1992. Otolith removal and preparation for microstructural examination. In: (Eds. D.K. Stevenson and S.E. Campana) Otolith microstructure examination and analysis. Canadian Special Publication of Fisheries and Aquatic Sciences 117, 19–57.Google Scholar
  34. Skovgaard A., Bahlool Q.Z.M., Munk P., Berge T., Buchmann K. 2011. Infection of North Sea cod, Gadus morhua L., larvae with the parasitic nematode Hysterothylacium aduncum Rudolphi. Journal of Plankton Research, 33, 1311–1316. DOI: 10.1093/plankt/fbr027.CrossRefGoogle Scholar
  35. Szostakowska B., Myjak P., Wyszyński M., Pietkiewicz H., Rokicki J. 2005. Prevalence of anisakin nematodes in fish from southern Baltic Sea. Polish Journal of Microbiology, 54, 41–45.PubMedGoogle Scholar
  36. Wootten R. 1978. The occurrence of larval anisakid nematodes in small gadoids from Scottish waters. Journal of the Marine Biological Association of the United Kingdom, 58, 347–356. DOI: 10.1017/S0025315400028022.CrossRefGoogle Scholar
  37. Wootten R., Smith J.W., Needham E.A. 1982. Aspects of the biology of the parasitic copepods Lepeophtheirus salmonis and Caligus elongatus on farmed salmonids, and their treatment. In: Proceedings of the Royal Society of Edinburgh. Section B. Biological Sciences, January 1982, 81, 185–197. DOI: 10.1017/S0269727000003389.CrossRefGoogle Scholar
  38. Zagmutt-Vergara F.J., Carpenter T.E., Farver T.B., Hedrick R.P. 2005. Spatial and temporal variations in sea lice (Copepoda: Caligidae) infestations of three salmonid species farmed in net pens in southern Chile. Diseases of Aquatic Organisms, 64, 163–173.PubMedCrossRefGoogle Scholar
  39. Zhu X.Q., Podolska M., Liu J.S., Yu H.Q., Chen H.H., Lin Z.X., Luo C.B., Song H.Q., Lin R.Q. 2007. Identification of anisakid nematodes with zoonotic potential from Europe and China by single-strand conformation polymorphism analysis of nuclear ribosomal DNA. Parasitology Research, 101, 1703–1707. DOI: 10.1007/s00436-007-0699-0.PubMedCrossRefGoogle Scholar

Copyright information

© Versita Warsaw and Springer-Verlag Wien 2014

Authors and Affiliations

  • Foojan Mehrdana
    • 1
  • Qusay Z. M. Bahlool
    • 1
  • Alf Skovgaard
    • 1
  • Jesper A. Kuhn
    • 2
  • Per W. Kania
    • 1
  • Peter Munk
    • 3
  • Kurt Buchmann
    • 1
  1. 1.Laboratory of Aquatic Pathobiology, Department of Veterinary Disease Biology, Faculty of Health and Medical SciencesUniversity of CopenhagenFrederiksberg CDenmark
  2. 2.Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and EconomicsUniversity of TromsøTromsøNorway
  3. 3.National Institute of Aquatic ResourcesTechnical University of Denmark (DTU)CharlottenlundDenmark

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