Advertisement

Parasitology Research

, Volume 94, Issue 1, pp 1–9 | Cite as

The life cycle of Anisakis simplex in the Norwegian Deep (northern North Sea)

  • Sven KlimpelEmail author
  • Harry W. Palm
  • Sonja Rückert
  • Uwe Piatkowski
Original Paper

Abstract

Copepoda (Calanus finmarchicus n=1,722, Paraeuchaeta norvegica n=1,955), Hyperiidae (n=3,019), Euphausiacea (Meganyctiphanes norvegica n=4,780), and the fishes Maurolicus muelleri (n=500) and Pollachius virens (n=33) were collected in the Norwegian Deep (northern North Sea) during summer 2001 to examine the importance of pelagic invertebrates and vertebrates as hosts of Anisakis simplex and their roles in the transfer of this nematode to its final hosts (Cetaceans). Third stage larvae (L3) of A. simplex were found in P. norvegica, M. muelleri and P. virens. The prevalence of A. simplex in dissected P. norvegica was 0.26%, with an intensity of 1. Prevalences in M. muelleri and P. virens were 49.6% and 100.0%, with mean intensities of 1.1–2.6 (total fish length ≥6.0–7.2) and 193.6, respectively. All specimens of C. finmarchicus and M. norvegica examined were free of anisakid nematode species and no other parasites were detected. P. norvegica, which harboured the third stage larvae, is the obligatory first intermediate host of A. simplex in the investigated area. Though there was no apparent development of larvae in M. muelleri, this fish can be considered as the obligatory second intermediate host of A. simplex in the Norwegian Deep. However, it is unlikely that the larva from P. norvegica can be successfully transmitted into the cetacean or pinniped final hosts, where they reach the adult stage. An additional growth phase and a second intermediate host is the next phase in the life cycle. Larger predators such as P. virens serve as paratenic hosts, accumulating the already infective stage from M. muelleri. The oceanic life cycle of A. simplex in the Norwegian Deep is very different in terms of hosts and proposed life cycle patterns of A. simplex from other regions, involving only a few intermediate hosts. In contrast to earlier suggestions, euphausiids have no importance at all for the successful transmission of A. simplex in the Norwegian Deep. This demonstrates that this nematode is able to select definite host species depending on the locality, apparently having a very low level of host specificity. This could explain the wide range of different hosts that have been recorded for this species, and can be seen as the reason for the success of this parasite in reaching its marine mammal final hosts in an oceanic environment.

Keywords

Intermediate Host Final Host Harbour Porpoise Paratenic Host Mesopelagic Fish 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We are grateful to Prof. Dr. Heinz Mehlhorn (Institute of Zoomorphology, Cell Biology and Parasitology, Düsseldorf), Dr. Mark Lenz (Leibniz-Institute of Marine Sciences, Kiel), and Svenja Hauschildt for kindly revising an earlier draft of the manuscript. We are especially thankful to Annett Seehagen for her great assistance in the field and laboratory. The scientific staff, and the crew of R.V. Heincke is thanked for their help during the collection of the material. The present study was supported by the Commission of the European Community (Q5RS-2000-30183, LIFECO) and the international project MAR-ECO coordinated by the University of Bergen and the Institute of Marine Research of Norway.

References

  1. Abollo E, Gestal C, Pascual S (2001) Anisakis infestation in marine fish and cephalopods from Galician waters: an updated perspective. Parasitol Res 87:492–499CrossRefPubMedGoogle Scholar
  2. Badcock J (1984) Sternoptychidae. In: Whitehead PJP, Bauchot ML, Hureau JC, Nielsen J, Tortonese E (eds) Fishes of the North-eastern Atlantic and the Mediterranean. UNESCO, Paris, pp 311–312Google Scholar
  3. Banning van P, Becker HB (1978) Long-term survey data (1965–1972) on the occurrence of Anisakis larvae (Nematoda: Ascaridida) in herring, Clupea harengus L., from the North Sea. J Fish Biol 12:25–33Google Scholar
  4. Bergstad OA (1990) Ecology of the fishes of the Norwegian Deep: distribution and species assemblages. Neth J Sea Res 25:237–266CrossRefGoogle Scholar
  5. Bergstad OA (1991a) Distribution and trophic ecology of some gadoid fish of the Norwegian Deep. 1. Accounts of individual species. Sarsia 75:269–313Google Scholar
  6. Bergstad OA (1991b). Distribution and trophic ecology of some gadoid fish of the Norwegian Deep. 2. Food web linkages and comparison of diets and distributions. Sarsia 75:315–325Google Scholar
  7. Berland B (1961) Nematodes from some Norwegian marine fishes. Sarsia 2:1–50Google Scholar
  8. Börjesson P, Berggren P, Ganning B (2003) Diet of harbor porpoises in the Kattegat and Skagerrak Seas: accounting for individual variation and sample size. Mar Mamm Sci 19:38–58Google Scholar
  9. Boehlert GW, Wilson CD, Mizuno K (1994) Populations of the Sternoptychid Fish Maurolicus muelleri on Seamounts in the Central North Pacific. Pac Sci 48:57–69Google Scholar
  10. Bush AO, Lafferty KH, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583PubMedGoogle Scholar
  11. Fontaine PM, Hammill MO, Barette C, Kingsley MC (1994) Summer diet of the harbour porpoise (Phocoena phocoena) in the estuary and the northern Gulf of St. Lawrence. Can J Fish Aquat Sci 51:172–178Google Scholar
  12. Furnes GK, Hackett B, Saetre R (1986) Retroflection of Atlantic water in the Norwegian Trench. Deep Sea Res 33:247–265CrossRefGoogle Scholar
  13. Giske J, Aksnes DL, Balino BM, Kaartvedt S, Lie U, Nordeide JT, Salvanes AGV, Wakili SM, Aadnesen A (1990) Vertical distribution and trophic interactions of zooplankton and fish in Masfjorden, Norway. Sarsia 75:65–81Google Scholar
  14. Gjøsæter J (1981) Life history and ecology of Maurolicus muelleri (Gonostomatidae) in Norwegian waters. Fiskeridir Skr Ser Havunders 17:109–131Google Scholar
  15. Hamre LA, Karlsbakk E (2002) Metazoan parasites of Maurolicus muelleri (Gmelin) (Sternoptychidae) in Herdlefjorden, western Norway. Sarsia 87:47–54CrossRefGoogle Scholar
  16. Hays GC, Proctor CA, John AWG, Warner AJ (1994) Interspecific differences in the diel vertical migration of marine copepods: the implications of size, color, and morphology. Limnol Oceanogr 39:1621–1629Google Scholar
  17. Hays R, Measures LN, Huot J (1998a) Euphausiids as intermediate hosts of Anisakis simplex in the St. Lawrence estuary. Can J Zool 76:1226–1235CrossRefGoogle Scholar
  18. Hays R, Measures LN, Huot J (1998b) Capelin (Mallotus villosus) and herring (Clupea harengus) as paratenic hosts of Anisakis simplex, a parasite of beluga (Delphinapterus leucas) in the St. Lawrence estuary. Can J Zool 76:1411–1417CrossRefGoogle Scholar
  19. Herreras MV, Kaarstad SE, Balbuena JA, Kinze CC, Raga JA (1997) Helminth parasites of the digestive tract of the harbour porpoise Phocoena phocoena in Danish waters: a comparative geographical analysis. Dis Aquat Org 28:163–167Google Scholar
  20. Højgaard DP (1999) Food and parasitic nematodes of saithe, Pollachius virens (L.), from the Faroe Islands. Sarsia 84:473–478Google Scholar
  21. Hyslop EJ (1980) Stomach content analysis—a review of methods and their application. J Fish Biol 17:411–429Google Scholar
  22. Ikeda T (1996) Metabolism, body composition, and energy budget of the mesopelagic fish Maurolicus muelleri in the Sea of Japan. Fish Bull 94:49–58Google Scholar
  23. Kaartvedt S, Knutsen T, Holst JC (1998) Schooling of the vertically migrating mesopelagic fish Maurolicus muelleri in light summer nights. Mar Ecol Prog Ser 170:287–290Google Scholar
  24. Kerstan SL (1992) Der Befall von Fischen aus dem Wattenmeer und dem Nordatlantik 1988–1990 mit Nematodenlarven und eine Bibliographie über parasitische Nematoden in Fischen und Seesäugern. Ber Inst Meereskd Kiel 219:1–205Google Scholar
  25. Kijewska A, Slominska M, Wegrzyn G, Rokicki J (2000) A PCR-RFLP assay for identification of Anisakis simplex from different geographical regions. Mol Cell Probes 14:349–354CrossRefPubMedGoogle Scholar
  26. Kijewska A, Rokicki J, Sitko J, Wegrzyn G (2002) Ascaridoidea: a simple DNA assay for identification of 11 species infection marine and freshwater fish, mammals, and fish-eating birds. Exp Parasitol 101:35–39CrossRefPubMedGoogle Scholar
  27. Klimpel S, Palm HW, Seehagen A (2003a) Metazoan parasites and food composition of juvenile Etmopterus spinax (L., 1758) (Dalatiidae, Squaliformes) from the Norwegian Deep. Parasitol Res 89:245–251PubMedGoogle Scholar
  28. Klimpel S, Seehagen A, Palm HW (2003b) Metazoan parasites and feeding behaviour of four small-sized fish species from the central North Sea. Parasitol Res 91:290–297CrossRefPubMedGoogle Scholar
  29. Køie M (1993) Aspects of the life-cycle and morphology of Hysterothylacium aduncum (Rudolphi, 1802) (Nematoda, Ascaridoidea, Anisakidae). Can J Zool 71:1289–1296Google Scholar
  30. Køie M (2001) Experimental infections of copepods and sticklebacks Gasterosteus aculeatus with small ensheathed and large third-stage larvae of Anisakis simplex (Nematoda, Ascaridoidea, Anisakidae). Parasitol Res 87:32–36CrossRefPubMedGoogle Scholar
  31. Køie M, Berland B, Burt MDB (1995) Development to third-stage larvae occurs in the eggs of Anisakis simplex and Pseudoterranova decipiens (Nematoda, Ascaridoidea, Anisakidae). Can J Fish Aquat Sci 52:134–139Google Scholar
  32. Kristoffersen JB, Salvanes GV (1998) Life history of Maurolicus muelleri in fjordic and oceanic environments. J Fish Biol 53:1324–1341CrossRefGoogle Scholar
  33. Lick R (1991) Untersuchungen zu Lebenszyklus (Krebse—Fische—marine Säuger) und Gefrierresistenz anisakider Nematoden in Nord- und Ostsee. Ber Inst Meereskd Kiel 218:1–195Google Scholar
  34. Lile NK (1998) Alimentary tract helminths of four pleuronectid flatfish in relation to host phylogeny and ecology. J Fish Biol 53:945–953CrossRefGoogle Scholar
  35. Mattiucci M, Nascetti G, Cianchi R, Paggi L, Arduino P, Margolis L, Brattey J, Webb S, D’amelio S, Orecchia P, Bullini L (1997) Genetic and ecological data on the Anisakis simplex complex, with evidence for a new species (Nematoda, Ascaridoidea, Anisakidae). J Parasitol 83:401–416CrossRefPubMedGoogle Scholar
  36. Mattiucci S, Paggi L, Nascetti G, Ishikura H, Kikuchi K, Sato N, Cianchi R, Bullini L (1998) Allozyme and morphological identification of Anisakis, Cotracaecum and Pseudoterranova from Japanese waters (Nematoda, Ascaridoidea). Syst Parasitol 40:81–92CrossRefGoogle Scholar
  37. Mattiucci S, Paggi L, Nascetti G, Santos CP, Costa G, Di Beneditto AP, Ramos R, Argyrou M, Cianchi R, Bullini L (2002) Genetic markers in the study of Anisakis typica (Diesing, 1860): larval identification and genetic relationships with other species of Anisakis Dujardin, 1845 (Nematoda: Anisakidae). Syst Parasitol 51:159–170CrossRefPubMedGoogle Scholar
  38. McDonald TE, Margolis L (1995) Synopsis of the parasites of fishes of Canada: Supplement (1978–1993). Can Spec Publ Fish Aquat Sci 122:1–265Google Scholar
  39. Palm HW, Klimpel S, Bucher C (1999) Checklist of metazoan fish parasites of German coastal waters. Ber Inst Meereskd Kiel 307:1–148Google Scholar
  40. Park T (1995) Taxonomy and distribution of the marine calanoid copepod family Euchaetidae. Bull Scripps Inst Oceanogr 29:1–107Google Scholar
  41. Rae BB (1965) The food of the common porpoise (Phocaena phocaena). J Zool 146:114–122Google Scholar
  42. Rasmussen OI, Giske J (1994) Life-history parameters and vertical distribution of Maurolicus muelleri in Masfjorden in summer. Mar Biol 120:649–664Google Scholar
  43. Recchia CA, Read AJ (1989) Stomach contents of harbour porpoise, Phocaena phocaena (L.), from the Bay of Fundy (Canada). Can J Zool 67:2140–2146Google Scholar
  44. Reid JB, Evans PGH, Northridge SP (2003) Atlas of Cetacean distribution in north-west European waters. Joint Nature Conservation Committee, PeterboroughGoogle Scholar
  45. Riemann F (1988) Nematoda. In: Higgins RP, Thiel H (eds) Introduction to the study of meiofauna. Smithsonian Institution Press, Washington, pp 293–301Google Scholar
  46. Skarra H, Kaartvedt S (2003) Vertical distribution and feeding of the carnivorous copepod Paraeuchaeta norvegica. Mar Ecol Prog Ser 249:215–222Google Scholar
  47. Smith JW (1971) Thysanoessa inermis and T. longicauda (Euphausiidae) as first intermediate hosts of Anisakis sp. (Nematoda: Ascaridata) in the northern North Sea, to the North of Scotland and at Faroe. Nature 234:478PubMedGoogle Scholar
  48. Smith JW (1983) Larval Anisakis simplex (Rudolphi, 1809, det. Krabbe, 1878) and larval Hysterothylacium sp. (Nematoda: Ascaridoidea) in euphausiids (Crustacea: Malacostraca) in the north-east Atlantic and northern North Sea. J Helminthol 57:167-177Google Scholar
  49. Strømnes E, Andersen K (1998) Distribution of whaleworm (Anisakis simplex; Nematoda, Ascaridoidea) L3 larvae in three species of marine fish; saithe (Pollachius virens (L.)), Cod (Gadus morhua L.) and redfish (Sebastes marinus (L.)) from Norwegian waters. Parasitol Res 84:281–285CrossRefPubMedGoogle Scholar
  50. Strømnes E, Andersen K (2000) “Spring rise” of whaleworm (Anisakis simplex; Nematoda, Ascaridoidea) third-stage larvae in some fish species from Norwegian waters. Parasitol Res 86:619–624PubMedGoogle Scholar
  51. Ugland KI, Strømnes E, Berland B, Aspholm PE (2004) Growth, fecundity and sex ratio of adult whaleworm (Anisakis simplex; Nematoda, Ascaridoidea, Ansiakidae) in three whale species from the north-east Atlantic. Parasitol Res 92:484–489CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • Sven Klimpel
    • 1
    Email author
  • Harry W. Palm
    • 1
    • 2
  • Sonja Rückert
    • 1
  • Uwe Piatkowski
    • 3
  1. 1.Institute of Zoomorphology, Cell Biology and ParasitologyHeinrich-Heine-UniversityDüsseldorfGermany
  2. 2.Faculty of Fisheries and Marine ScienceBogor Agricultural UniversityBogorIndonesia
  3. 3.Research Division 3: Marine EcologyLeibniz Institute of Marine SciencesKielGermany

Personalised recommendations