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

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.

Access this article

Log in via an institution

Subscribe and save

• Starting from 10 chapters or articles per month
• Access and download chapters and articles from more than 300k books and 2,500 journals
• Cancel anytime View plans

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

• Abollo E, Gestal C, Pascual S (2001) Anisakis infestation in marine fish and cephalopods from Galician waters: an updated perspective. Parasitol Res 87:492–499
  Article CAS PubMed Google Scholar
• 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 311–312
• 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 12:25–33
  Google Scholar
• Bergstad OA (1990) Ecology of the fishes of the Norwegian Deep: distribution and species assemblages. Neth J Sea Res 25:237–266
  Article Google Scholar
• Bergstad OA (1991a) Distribution and trophic ecology of some gadoid fish of the Norwegian Deep. 1. Accounts of individual species. Sarsia 75:269–313
  Google Scholar
• 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 75:315–325
  Google Scholar
• Berland B (1961) Nematodes from some Norwegian marine fishes. Sarsia 2:1–50
  Google Scholar
• 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 19:38–58
  Google Scholar
• Boehlert GW, Wilson CD, Mizuno K (1994) Populations of the Sternoptychid Fish Maurolicus muelleri on Seamounts in the Central North Pacific. Pac Sci 48:57–69
  Google Scholar
• Bush AO, Lafferty KH, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583
  CAS PubMed Google Scholar
• 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 51:172–178
  Google Scholar
• Furnes GK, Hackett B, Saetre R (1986) Retroflection of Atlantic water in the Norwegian Trench. Deep Sea Res 33:247–265
  Article Google Scholar
• 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 75:65–81
  Google Scholar
• Gjøsæter J (1981) Life history and ecology of Maurolicus muelleri (Gonostomatidae) in Norwegian waters. Fiskeridir Skr Ser Havunders 17:109–131
  Google Scholar
• Hamre LA, Karlsbakk E (2002) Metazoan parasites of Maurolicus muelleri (Gmelin) (Sternoptychidae) in Herdlefjorden, western Norway. Sarsia 87:47–54
  Article Google Scholar
• 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 39:1621–1629
  Google Scholar
• Hays R, Measures LN, Huot J (1998a) Euphausiids as intermediate hosts of Anisakis simplex in the St. Lawrence estuary. Can J Zool 76:1226–1235
  Article Google Scholar
• 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 76:1411–1417
  Article Google Scholar
• 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 28:163–167
  Google Scholar
• Højgaard DP (1999) Food and parasitic nematodes of saithe, Pollachius virens (L.), from the Faroe Islands. Sarsia 84:473–478
  Google Scholar
• Hyslop EJ (1980) Stomach content analysis—a review of methods and their application. J Fish Biol 17:411–429
  Google Scholar
• Ikeda T (1996) Metabolism, body composition, and energy budget of the mesopelagic fish Maurolicus muelleri in the Sea of Japan. Fish Bull 94:49–58
  Google Scholar
• Kaartvedt S, Knutsen T, Holst JC (1998) Schooling of the vertically migrating mesopelagic fish Maurolicus muelleri in light summer nights. Mar Ecol Prog Ser 170:287–290
  Google Scholar
• 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 219:1–205
  Google Scholar
• 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 14:349–354
  Article CAS PubMed Google Scholar
• 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 101:35–39
  Article CAS PubMed Google Scholar
• 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 89:245–251
  PubMed Google Scholar
• 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 91:290–297
  Article PubMed Google Scholar
• Køie M (1993) Aspects of the life-cycle and morphology of Hysterothylacium aduncum (Rudolphi, 1802) (Nematoda, Ascaridoidea, Anisakidae). Can J Zool 71:1289–1296
  Google Scholar
• 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 87:32–36
  Article PubMed Google Scholar
• 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 52:134–139
  Google Scholar
• Kristoffersen JB, Salvanes GV (1998) Life history of Maurolicus muelleri in fjordic and oceanic environments. J Fish Biol 53:1324–1341
  Article Google Scholar
• Lick R (1991) Untersuchungen zu Lebenszyklus (Krebse—Fische—marine Säuger) und Gefrierresistenz anisakider Nematoden in Nord- und Ostsee. Ber Inst Meereskd Kiel 218:1–195
  Google Scholar
• Lile NK (1998) Alimentary tract helminths of four pleuronectid flatfish in relation to host phylogeny and ecology. J Fish Biol 53:945–953
  Article Google Scholar
• 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 83:401–416
  Article CAS PubMed Google Scholar
• 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 40:81–92
  Article Google Scholar
• 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 51:159–170
  Article CAS PubMed Google Scholar
• McDonald TE, Margolis L (1995) Synopsis of the parasites of fishes of Canada: Supplement (1978–1993). Can Spec Publ Fish Aquat Sci 122:1–265
  Google Scholar
• Palm HW, Klimpel S, Bucher C (1999) Checklist of metazoan fish parasites of German coastal waters. Ber Inst Meereskd Kiel 307:1–148
  Google Scholar
• Park T (1995) Taxonomy and distribution of the marine calanoid copepod family Euchaetidae. Bull Scripps Inst Oceanogr 29:1–107
  Google Scholar
• Rae BB (1965) The food of the common porpoise (Phocaena phocaena). J Zool 146:114–122
  Google Scholar
• Rasmussen OI, Giske J (1994) Life-history parameters and vertical distribution of Maurolicus muelleri in Masfjorden in summer. Mar Biol 120:649–664
  Google Scholar
• Recchia CA, Read AJ (1989) Stomach contents of harbour porpoise, Phocaena phocaena (L.), from the Bay of Fundy (Canada). Can J Zool 67:2140–2146
  Google Scholar
• Reid JB, Evans PGH, Northridge SP (2003) Atlas of Cetacean distribution in north-west European waters. Joint Nature Conservation Committee, Peterborough
• Riemann F (1988) Nematoda. In: Higgins RP, Thiel H (eds) Introduction to the study of meiofauna. Smithsonian Institution Press, Washington, pp 293–301
• Skarra H, Kaartvedt S (2003) Vertical distribution and feeding of the carnivorous copepod Paraeuchaeta norvegica. Mar Ecol Prog Ser 249:215–222
  Google Scholar
• 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 234:478
  CAS PubMed Google Scholar
• 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 57:167-177
  Google Scholar
• 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 84:281–285
  Article PubMed Google Scholar
• 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 86:619–624
  PubMed Google Scholar
• 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 92:484–489
  Article PubMed Google Scholar

Download references

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.

Author information

Authors and Affiliations

1. Institute of Zoomorphology, Cell Biology and Parasitology, Heinrich-Heine-University, Universitätsstrasse 1, 40225 , Düsseldorf, Germany
   Sven Klimpel, Harry W. Palm & Sonja Rückert
2. Faculty of Fisheries and Marine Science, Bogor Agricultural University, Campus IPB Darmaga, 16680 , Bogor, Indonesia
   Harry W. Palm
3. Research Division 3: Marine Ecology, Leibniz Institute of Marine Sciences, Düsternbrooker Weg 20, 24105 , Kiel, Germany
   Uwe Piatkowski

Authors

1. Sven Klimpel
2. Harry W. Palm
3. Sonja Rückert
4. Uwe Piatkowski

Corresponding author

Correspondence toSven Klimpel.

Rights and permissions

About this article

Cite this article

Klimpel, S., Palm, H.W., Rückert, S. et al. The life cycle of Anisakis simplex in the Norwegian Deep (northern North Sea).Parasitol Res 94, 1–9 (2004). https://doi.org/10.1007/s00436-004-1154-0

Download citation

• Received: 13 May 2004
• Accepted: 11 June 2004
• Published: 23 July 2004
• Issue date: September 2004
• DOI: https://doi.org/10.1007/s00436-004-1154-0

Keywords