Advertisement

Parasitology Research

, Volume 104, Issue 1, pp 43–53 | Cite as

The role of pelagic swarm fish (Myctophidae: Teleostei) in the oceanic life cycle of Anisakis sibling species at the Mid-Atlantic Ridge, Central Atlantic

  • Sven Klimpel
  • Esra Kellermanns
  • Harry W. Palm
Original Paper

Abstract

First information is provided on the parasitation and feeding ecology of the myctophid fish species Myctophum punctatum and Notoscopelus kroyeri from the Mid-Atlantic Ridge (MAR), Central Atlantic. Four different parasite species were found in both fish with a similar high prevalence and intensity of infestation. The digeneans Gonocerca phycidis and Lethadena sp. were isolated as adults from the stomach, larval tetraphyllidean cestodes (Scolex pleuronectis) from the intestine, and genetically identified larval anisakid nematodes of Anisakis simplex (s.s.) from the body cavity. No further Anisakis sibling species could be identified. Both myctophids had small pelagic crustaceans, mainly copepods and hyperiids, within their stomach contents. Ostracods, euphausiids, decapods, and amphipods were minor food components, demonstrating the pelagic environment for both fish. The recorded parasites including the anisakid A. simplex (s.s.) perform pelagic life cycles within the region, benefiting from extensive diurnal vertical migrations of their fish hosts. Comparison of the host range among the anisakis sibling species suggests that the A. simplex complex has low host specificity, infecting toothed and baleen whales on their extensive oceanic migrations. This contrasts the Anisakis physeteris complex that is restricted to toothed whales of the families Kogiidae and Physeteridae. Specificity in the teleost intermediate hosts for both complexes seems to be low, and sympatric occurrence of different siblings within the same intermediate hosts is likely. Myctophid swarm fish as important copepod feeders at the MAR significantly contribute to the oceanic anisakid nematode life cycle, especially considering the 100% prevalence and high intensity of infestation. Further genetic identification of Anisakis nematodes is needed in order to understand the sibling species distribution, along the MAR and within other oceanic environments.

Keywords

Prey Item Intermediate Host Final Host Baleen Whale Anisakis Simplex 
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

Acknowledgments

The authors thank the scientific staff and the crew of the Norwegian research vessel G.O. Sars for their help during the collection of the material. We thank M.W. Busch, Heinrich-Heine University Düsseldorf, for his technical assistance during the present study. The present study was financially supported by the German Research Council (DFG KL 2087/1-1, 1-2; DFG PA 664/4-1).

References

  1. Amundsen PA, Gabler HM, Staldvik FJ (1996) A new approach to graphical analysis of feeding strategy from stomach contents data—modification of the Costello (1990) method. J Fish Biol 48:607–614Google Scholar
  2. Bray RA (2004) The bathymetric distribution of the digenean parasites of deep-sea fishes. Folia Parasitol 51:268–274PubMedGoogle Scholar
  3. Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583CrossRefGoogle Scholar
  4. D’Amelio S, Mathiopoulos KD, Santos CP, Pugachev ON, Webb SC, Picanço M, Paggi L (2000) Genetic markers in ribosomal DNA for the identification of members of the genus Anisakis (Nematoda: Ascaridoidae) defined by polymerase chain reaction-based restriction fragment length polymorphism. Int J Parasitol 30:223–226PubMedCrossRefGoogle Scholar
  5. Davey JT (1971) A revision of the genus Anisakis Dujardin, 1875 (Nematoda: Ascaridata). J Helminthol 45:51–72CrossRefGoogle Scholar
  6. Foxton P (1970) The vertical distribution of pelagic decapods (Crustacea: Natantia) collected on the SOND cruise 1965. J Mar Biol Assoc UK 50:961–1000Google Scholar
  7. Froese R, Pauly D (2008) FishBase. World Wide Web electronic publication. http://www.fishbase.org, version (04/2008)
  8. Gartner JV, Zwerner DE (1989) The parasite faunas of meso- and bathypelagic fishes of Norfolk Submarine Canyon, western North Atlantic. J Fish Biol 34:79–95CrossRefGoogle Scholar
  9. Gibson DI, Jones A, Bray RA (2002) Keys to the trematodes, vol. 1. CAB International, WallingfordGoogle Scholar
  10. Gjøsaeter J, Kawaguchi K (1980) A review of the world resources of mesopelagic fish. FAO Fish Tech Pap 193:1–151Google Scholar
  11. 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
  12. Hays R, Measures LN, Huot J (1998b) Capelin (Mallotus villosus) 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
  13. Hyslop EJ (1980) Stomach content analysis - a review of methods and their application. J Fish Biol 17:411–429CrossRefGoogle Scholar
  14. Kellermanns E, Klimpel S, Palm HW (2007) Molecular identification of ascaridoid nematodes from the deep-sea onion-eye grenadier (Macrourus berglax) from the East Greenland Sea. Deep-Sea Res Pt I 54:2194–2202CrossRefGoogle Scholar
  15. Klimpel S, Seehagen A, Palm HW, Rosenthal H (2001) Deep-water metazoan fish parasites of the world. Logos, BerlinGoogle Scholar
  16. Klimpel S, Palm HW, Rückert S, Piatkowski U (2004) The life cycle of Anisakis simplex in the Norwegian Deep (northern North Sea). Parasitol Res 94:1–9PubMedCrossRefGoogle Scholar
  17. Klimpel S, Palm HW, Busch MW, Kellermanns E, Rückert S (2006a) Fish parasites in the Arctic deep-sea: Poor diversity in pelagic fish species vs. heavy parasite load in a demersal fish. Deep-Sea Res Pt I 53:1167–1181Google Scholar
  18. 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
  19. Klimpel S, Kellermanns E, Palm HW, Moravec F (2007) Zoogeography of fish parasites of the pearlside (Maurolicus muelleri), with genetic evidence of Anisakis simplex (s.s.) form the Mid-Atlantic Ridge. Mar Biol 152:725–732CrossRefGoogle Scholar
  20. Klimpel S, Palm HW, Busch MW, Kellermanns E (2008) Fish parasites in the bathyal zone: The halosaur Halosauropsis macrochir (Günther, 1878) from the Mid-Atlantic Ridge. Deep-Sea Res Pt II 55:229–235Google Scholar
  21. Køie M (2000) Metazoan parasites of teleost fishes from Atlantic waters off the Faroe Islands. Ophelia 52:25–44Google Scholar
  22. Køie M (2001) Experimental infections of copepods and sticklebacks Gasterosteus aculeatus with small ensheated and large third-stage larvae of Anisakis simplex (Nematoda, Ascaridoidea, Anisakidae). Parasitol Res 87:32–36PubMedGoogle Scholar
  23. 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
  24. Mattiucci S, 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 83:401–416CrossRefGoogle Scholar
  25. Mattiucci S, Paggi L, Nascetti G, Portes Santos C, 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 51:159–170PubMedCrossRefGoogle Scholar
  26. Mattiucci S, Nascetti G, Dailey M, Webb SC, Barros NB, Cianchi R, Bullini L (2005) Evidence for a new species of Anisakis Dujardin, 1845: morphological description and genetic relationships between congeners (Nemtoda: Anisakidae). Syst Parasitol 61:151–171CrossRefGoogle Scholar
  27. Mattiucci S, Nascetti G (2006) Molecular systematics, phylogeny and ecology of anisakid nematodes of the genus Anisakis Dujardin, 1845: an update. Parasite 13:99–113PubMedGoogle Scholar
  28. Mattiucci S, Nascetti G (2007) Genetic diversity and infection levels of anisakid nematodes parasitic in fish and marine mammals from Boreal and Austral hemispheres. Vet Parasitol 148:43–57PubMedCrossRefGoogle Scholar
  29. Mattiucci S, Paoletti M, Damiano S, Nascetti G (2007) Molecular detection of sibling species in anisakid nematodes. Parassitologia 49:147–153PubMedGoogle Scholar
  30. Mauchline J, Gordon JDM (1984) Incidence of parasitic worms in stomachs of pelagic and demersal fish of the Rockall Trough, northeastern Atlantic Ocean. J Fish Biol 24:281–285CrossRefGoogle Scholar
  31. Mignucci-Giannoni AA, Hoberg EP, Siegel-Causey D, Williams EH (1998) Metazoan parasites and other symbionts of cetaceans in the Caribbean. J Parasitol 84:939–946PubMedCrossRefGoogle Scholar
  32. Moku M, Kawaguchi K, Watanabe H, Ohno A (2000) Feeding habits of three dominant myctophid fishes, Diaphus theta, Stenobrachius leucopsarus and S. nannochir, in the subarctic and transitional waters of the western North Pacific. Mar Ecol Prog Ser 207:129–140CrossRefGoogle Scholar
  33. Mordvinova TN (2000) Helminthofauna of myctophid fishes from the world ocean. Ecol Morya 53:59–63 (In Russian)Google Scholar
  34. Nadler SA, D’Amelio S, Dailey MD, Paggi L, Siu S, Sakanari JA (2005) Molecular phylogenetics and diagnosis of Anisakis, Pseudoterranova, and Contracaecum from northern Pacific marine mammals. J Parasitol 91:1413–1429PubMedCrossRefGoogle Scholar
  35. Paggi L, Nascetti G, Webb SC, Mattiucci S, Cianchi R, Bullini L (1998) A new species of Anisakis Dujardin, 1845 (Nematoda, Anisakidae) from beaked whales (Ziphiidae): allozyme and morphological evidence. Syst Parasitol 40:161–174CrossRefGoogle Scholar
  36. Palm HW (1999) Ecology of Pseudoterranova decipiens Krabbe, 1878 (Nematoda: Anisakidae) from Antarctic waters. Parasitol Res 85:638–656PubMedCrossRefGoogle Scholar
  37. Palm HW, Damriyasa IM, Linda Oka IBM (2008) Molecular genotyping of Anisakis Dujardin, 1845 (Nematoda: Ascaridoidea: Anisakidae) larvae from marine fish of Balinese and Javanese waters, Indonesia. Helminthologia 45:3–12CrossRefGoogle Scholar
  38. Perrin WF (2002) Stenella frontalis. Mamm Spec 702:1–6CrossRefGoogle Scholar
  39. Petter AG (1972) Redescription of Anisakis insignis (Diesing) (Ascaridoidea), parasite of the Amazone dolphin Inia geoffrensis. Invest Cetacea 4:93–99Google Scholar
  40. Pusch C, Beckmann A, Porteiro FM, Westernhagen von H (2004) The influence of seamounts on mesopelagic fish communities. Arch Fish Mar Res 51:165–186Google Scholar
  41. Sprent JF (1982) Ascaridoid nematodes of South American mammals, with a definition of a new genus. J Helminthol 56:275–295PubMedCrossRefGoogle Scholar
  42. Sutton TT, Hopkins TL (1996) Trophic ecology of the stomiid (Pisces: Stomiidae) fish assemblage of the eastern Gulf of Mexico: strategies, selectivity and impact of a top mesopelagic predator group. Mar Biol 127:179–192CrossRefGoogle Scholar
  43. Sutton TT, Porteiro FM, Heino M, Byrkjedal I, Langhelle G, Anderson CIH, Horne J, Søiland H, Falkenhaug T, Godø OR, Bergstad OA (2008) Vertical structure, biomass and topographic association of deep-pelagic fishes in relation to a mid-ocean ridge system. Deep-Sea Res Pt II 55:161–184Google Scholar
  44. 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 22:4673–4680PubMedCrossRefGoogle Scholar
  45. Valentini A, Mattiucci S, Bondanelli P, Webb SC, Mignucci-Giannone AA, Colom-Llavina MM, Nascetti G (2006) Genetic relationship among Anisakis species (Nematoda: Anisakidae) inferred from mitochondrial cox2 sequences, and comparison with allozym data. J Parasitol 92:156–166PubMedCrossRefGoogle Scholar
  46. Yamaguchi M, Miya M, Okiyama M, Nishida M (2000) Molecular phylogeny and larval morphological diversity of the lanternfish genus Hygophum (Teleostei: Myctophidae). Mol Phyl Evol 15:103–114CrossRefGoogle Scholar
  47. Zhu X, Gasser RB, Jacobs DE, Hung GC, Chilton NB (2000) Relationships among some ascaridoid nematodes based on ribosomal DNA sequence data. Parasitol Res 86:738–744PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Sven Klimpel
    • 1
  • Esra Kellermanns
    • 1
  • Harry W. Palm
    • 1
  1. 1.Institute of Zoomorphology, Cell Biology and ParasitologyHeinrich-Heine University DüsseldorfDüsseldorfGermany

Personalised recommendations