Marine Biology

, Volume 152, Issue 3, pp 725–732 | Cite as

Zoogeography of fish parasites of the pearlside (Maurolicus muelleri), with genetic evidence of Anisakis simplex (s.s.) from the Mid-Atlantic Ridge

  • Sven KlimpelEmail author
  • Esra Kellermanns
  • Harry W. Palm
  • František Moravec
Research Article


A total of 200 Maurolicus muelleri from the Mid-Atlantic Ridge (MAR) and the Norwegian Deep (ND) were studied for parasitic helminths. Two different metazoans were isolated from the MAR and five species from the ND. The predominant parasite species in both areas were tetraphyllidean cestode larvae (Scolex pleuronectis) and the anisakid nematode Anisakis simplex sensu stricto (s.s.), the latter being identified using genetic analysis of the internal transcribed spacer (ITS-1, ITS-2) and 5.8S regions of the rDNA. The parasite fauna of M. muelleri from the MAR was less species rich in comparison to ND, due to the deep-sea and oceanic environment. The digeneans Brachyphallus crenatus and Lecithaster confusus as well as the raphidascarid fish nematode Hysterothylacium aduncum were only collected from the ND. This can be explained either by the deep origin of the sampled fish specimens or the lack of suitable intermediate or final hosts in the region. Based on the frequent occurrence of A. simplex (s.s.) around the MAR and the ND, a pelagic life cycle is suggested at both localities, involving baleen and toothed whales as final and pelagic and mesopelagic fish and invertebrates as intermediate or paratenic hosts.


Intermediate Host Sibling Species Killer Whale Parasite Fauna Final Host 
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.



We would like to thank Prof. R. Gasser for helpful comments of an earlier draft of the manuscript. The scientific staff and the crew of the Norwegian research vessel G.O. Sars are thanked for their help during the collection of the material. This study was initiated by the international Census of Marine Life project Mar-Eco coordinated by the Institute of Marine Research in Bergen, Norway. The present study was supported by the German Research Council (DFG KL 2087/1-1, PA 664/4-1) and the German Academic Exchange Service (DAAD Klimpel D/05/51605).


  1. Abe N, Ohya N, Yanagiguchi R (2005) Molecular characterization of Anisakis pegreffii larvae in Pacific cod in Japan. J Helminthol 79:303–306CrossRefGoogle Scholar
  2. Abollo E, Gestal C, Pascual S (2001) Anisakis infestation in marine fish and cephalopods from Galician waters: an updated perspective. Parasitol Res 87:492–499CrossRefGoogle Scholar
  3. Abollo E, Paggi L, Pascual S, D’Amelio S (2003) Occurrence of recombinant genotypes of Anisakis simplex s.s. and Anisakis pegreffii (Nematoda: Anisakidae) in an area of sympatry. Infect Genet Evol 3:175–181CrossRefGoogle Scholar
  4. Anderson RC (2000) Nematode parasites of vertebrates: their development and transmission. Oxford University Press/CAB International, WallingfordCrossRefGoogle Scholar
  5. Badcock J (1984) Sternoptychidae. In: Whitehead PJP, Bauchot ML, Hureau JC, Nielsen J, Tortonese E (eds) Fishes of the North-eastern Atlantic and Mediterranean. UNESCO, Paris, pp 311–312Google Scholar
  6. Bergstad OA (1990) Ecology of the fishes of the Norwegian Deep: distribution and species assemblage. Neth J Sea Res 25:237–266CrossRefGoogle Scholar
  7. Bray RA (2004) The bathymetric distribution of the digenean parasites of deep-sea fishes. Folia Parasitol 51:268–274CrossRefGoogle Scholar
  8. Bush O, Lafferty AD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583CrossRefGoogle Scholar
  9. Froese R, Pauly D (2007) FishBase. World Wide Web electronic publication., version 01/2007
  10. Gibson DI, Harris EA, Bray RA, Jepson PD, Kuiken T, Baker JR, Simpson VR (1998) A survey of the helminth parasites of cetaceans stranded on the coast of England and Wales during the period 1990–1994. J Zool (Lond) 244:563–574CrossRefGoogle Scholar
  11. Gibson DI, Jones A, Bray RA (2002) Keys to the Trematoda, vol 1.CAB International and The Natural History Museum London, WallingfordGoogle Scholar
  12. Hamre LA, Karlsbakk E (2002) Metazoan parasites of Maurolicus muelleri (Gmelin) (Sternoptychidae) in Herdlefjorden, western Norway. Sarsia 87:47–54CrossRefGoogle Scholar
  13. Hays R, Measures LN, Huot J (1998) Euphausiids as intermediate hosts of Anisakis simplex in the St Lawrence estuary. Can J Zool 76:1226–1235CrossRefGoogle Scholar
  14. Hunningen AV, Cable RM (1943) The life history of Lecithaster confusus Odhner (Trematoda: Hemiuridae). J Parasitol 29:71–79CrossRefGoogle Scholar
  15. Hyslop EJ (1980) Stomach content analysis—a review of methods and their application. J Fish Biol 17:411–429CrossRefGoogle Scholar
  16. Justine JL, Cassone J, Petter A (2002) Moravecnema segonzaci gen. et sp. n. (Nematoda: Cystidicolidae) from Pachycara thermophilum (Zoarcidae), a deep-sea hydrothermal vent fish from the Mid-Atlantic Ridge. Folia Parasitol 49:299–303CrossRefGoogle Scholar
  17. Kaartvedt S, Knust T, Holst JC (1998) Schooling of the vertically migrating mesopelagic fish Maurolicus muelleri in light summer nights. Mar Ecol Prog Ser 170:287–290CrossRefGoogle Scholar
  18. Khalil LF, Jones A, Bray RA (1994) Keys to the cestode parasites of vertebrates. CAB International, WallingfordGoogle Scholar
  19. Klimpel S, Rückert S (2005) Life cycle strategy of Hysterothylacium aduncum to become the most abundant anisakid fish nematode in the North Sea. Parasitol Res 97:141–149CrossRefGoogle Scholar
  20. Klimpel S, Seehagen A, Palm HW, Rosenthal H (2001) Deep-water metazoan fish parasites of the world. Logos Verlag BerlinGoogle Scholar
  21. Klimpel S, Palm HW, Seehagen A (2003) Metazoan parasites and food composition of juvenile Etmopterus spinax (L., 1758) (Dalatiidae, Squaliformes) from the Norwegian Deep. Parasitol Res 89:245–251PubMedGoogle Scholar
  22. Klimpel S, Palm HW, Rückert S, Piatkowski U (2004) The life cycle of Anisakis simplex in the Norwegian Deep (northern North Sea). Parasitol Res 94:1–9CrossRefGoogle Scholar
  23. Klimpel S, Palm HW, Busch MW, Kellermanns E, Rückert S (2006a) Fish parasites in the Arctic deep-sea: Poor diversity in meso-/ bathypelagial vs. heavy parasite load in a demersal fish. Deep-Sea Res Pt I 53:1167–1181CrossRefGoogle Scholar
  24. Klimpel S, Rückert S, Piatkowski U, Palm HW, Hanel R (2006b) Diet and metazoan parasites of silver scabbard fish Lepidopus caudatus from the Great Meteor Seamount (North Atlantic). Mar Ecol Prog Ser 315:249–257CrossRefGoogle Scholar
  25. Køie M (1992) Life cycle and structure of the fish digenean Brachyphallus crenatus (Hemiuridae). J Parasitol 78:338–343CrossRefGoogle Scholar
  26. Køie M (1993) Aspects of the life-cycle and morphology of Hysterothylacium aduncum (Rudolphi, 1802) (Nematoda, Ascaridoidea, Anisakidae). Can J Zool 71:1289–1296CrossRefGoogle Scholar
  27. Marques JF, Cabral HN, Busi M, D’Amelio S (2006) Molecular identification of Anisakis species from Pleuronectiformes off the Portugeses coast. J Helminthol 80:47–51CrossRefGoogle Scholar
  28. Mattiucci S, Nascetti G, Cianchi R, Paggi L, Arduino P, Margolis L, Brattey J, Webb SC, 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 83:401–416CrossRefGoogle Scholar
  29. McManus DP, Bowles J (1996) Molecular genetic approaches to parasite identification: their value in diagnostic parasitology and systematics. Int J Parasitol 26:687–704CrossRefGoogle Scholar
  30. Nascetti G, Paggi L, Orecchia P, Smith JW, Mattiucci S, Bullini L (1986) Electrophoretic studies on the Anisakis simplex complex (Ascaridida: Anisakidae) from the Mediterranean and North-East Atlantic. Int J Parasitol 16:633–640CrossRefGoogle Scholar
  31. Pauly D, Trites AW, Capuli E, Christensen V (1998) Diet composition and trophic levels of marine mammals. ICES J Mar Sci 55:467–481CrossRefGoogle Scholar
  32. Pusch C, Schnack-Schiel S, Mizdalski E, von Westernhagen H (2004) Feeding ecology of three myctophid species at the Great Meteor Seamount (North-east Atlantic). Arch Fish Mar Res 51:251–271Google Scholar
  33. Rasmussen OI, Giske J (1994) Life-history parameters and vertical distribution of Maurolicus muelleri in Masfjorden in summer. Mar Biol 120:649–664CrossRefGoogle Scholar
  34. Reid JB, Evons PGH, Northridge SP (2003) Atlas of Cetacean distribution in north-west European waters. Joint Nature Conservation Committee, PeterboroughGoogle Scholar
  35. Reimer L (1975) Helminthen von Fischen des Mesopelagials von Nordwestafrika. Wissenschaftliche Zeitschrift der Pädagogischen Hochschule Güstrow 2:151–172Google Scholar
  36. Riemann F (1988) Nematoda. In: Higgins RP, Thiel H (eds) Introduction to the study of meiofauna. Smithsonian Institution Press, Washington, pp 293–301Google Scholar
  37. Smith JW, Snyder JM (2005) New locality records for third-stage larvae of Anisakis simplex (sensu lato) (Nematoda: Ascaridoidea) in euphausiids Euphausia pacifica and Thysanoessa raschii from Prince William Sound, Alaska. Parasitol Res 97:539–542CrossRefGoogle Scholar
  38. Thompson TE (1988) Molluscs: Benthic opisthobranchs (Mollusca: Gastropoda). Synopses of the British Fauna 8Google Scholar
  39. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefGoogle Scholar
  40. Zhu XQ, Gasser RB, Podolska M, Chilton NB (1998) Characterisation of anisakid nematodes with zoonotic potential by nuclear ribosomal DNA sequences. Int J Parasitol 28:1911–1921CrossRefGoogle Scholar
  41. Zhu X, Gasser RB, Jacobs DE, Hung GC, Chilton NB (2000) Relationships among some ascaridoid nematodes based on ribosomal DNA sequence data. Parasitol Res 86:738–744CrossRefGoogle Scholar
  42. 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 124:615–623CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Sven Klimpel
    • 1
    Email author
  • Esra Kellermanns
    • 1
  • Harry W. Palm
    • 1
  • František Moravec
    • 2
  1. 1.Institute of Zoomorphology, Cell Biology and ParasitologyHeinrich-Heine-University DüsseldorfDüsseldorfGermany
  2. 2.Institute of ParasitologyAcademy of Science of the Czech RepublicCeske BudejoviceCzech Republic

Personalised recommendations