Polar Biology

, Volume 34, Issue 6, pp 899–906 | Cite as

Deep-water life cycle of Anisakis paggiae (Nematoda: Anisakidae) in the Irminger Sea indicates kogiid whale distribution in north Atlantic waters

  • Sven Klimpel
  • Thomas Kuhn
  • Markus W. Busch
  • Horst Karl
  • Harry W. Palm
Original Paper

Abstract

The study of the beryciform Anoplogaster cornuta from the Irminger Sea (north Atlantic) revealed the presence of the anisakid nematode Anisakis paggiae inside the body cavity, representing a new host and locality record. This deep-sea fish was infected with Anisakis larvae at a prevalence of 57.1% and a mean intensity of 2.2, with no correlation between the fish standard length and the number of accumulated A. paggiae. Kogiid whales (Kogia breviceps, K. sima), the typical final hosts of this parasitic nematode, have not yet been recorded so far in the north. Because A. cornuta does not migrate outside the Irminger Sea, and by using the parasite as an indicator for the presence of the final hosts, A. paggiae must have been introduced through migratory kogiid final hosts. This would extend their range of distribution into the Irminger Sea. The depth range of the meso- and bathypelagic A. cornuta and the frequent occurrence of Anisakis inside this deep-sea fish demonstrate an oceanic deep-water life cycle for A. paggiae in the north Atlantic.

Keywords

Deep-sea fish Anisakis paggiae Zoogeography Metazoan parasites Irminger Sea Kogiidae Sibling species 

References

  1. Abollo E, Gestal C, Pascal S (2001) Anisakis infestation in marine fish and cephalopods from Galician waters: an updated perspective. Parasitol Res 87:492–499PubMedCrossRefGoogle Scholar
  2. Baumgartner MF, Mullin KD, May LN, Leming TD (2001) Cetacean habitats in the northern Gulf of Mexico. Fish Bull 99:219–239Google Scholar
  3. Beatson EL (2007) The diet of pygmy sperm whales, Kogia breviceps, stranded in New Zealand: implications for conservation. Rev Fish Biol Fisher 17:295–303CrossRefGoogle Scholar
  4. Bush O, Lafferty AD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on his own terms: Margolis et al. revisited. J Parasitol 83:575–583PubMedCrossRefGoogle Scholar
  5. Colón-Llavina MM, Mignucci-Giannoni AA, Mattiucci S, Paoletti M, Nascetti G, Williams EH Jr (2009) Additional records of metazoan parasites from Caribbean marine mammals, including genetically identified anisakid nematodes. Parasitol Res 105:1239–1252PubMedCrossRefGoogle Scholar
  6. Croll DA, Acevedo-Gutierrez A, Tershy BR, Urban-Ramirez J (2001) The diving behaviour of blue and fin whales: is diving duration shorter than expected based on oxygen stores? Comp Biochem Physiol 129:797–809Google Scholar
  7. Croll DA, Marinovic B, Benson S, Chavez FP, Black N, Ternullo R, Tershy BR (2005) From wind to whales: trophic links in a coastal upwelling system. Mar Ecol Prog Ser 289:117–130CrossRefGoogle Scholar
  8. Davis RW, Fargion GS, May N, Leming TD, Baumgartner M, Evans WE, Hansen LJ, Mullin K (1998) Physical habitats of cetaceans along the continental slope of north-central and western Gulf of Mexico. Mar Mamm Sci 14:490–507CrossRefGoogle Scholar
  9. Froese R, Pauly D (2010) Fishbase. World wide web electronic publication. www.fishbase.org, Version (03/2010)
  10. Heide-Jørgensen MP, Bloch D, Stefansson E, Mikkelsen B, Ofstad LH, Dietz R (2002) Diving behaviour of long-finned pilot whales Globicephala melas around the Faroe Islands. Wildl Biol 8:307–313Google Scholar
  11. Ho JS (1987) Tautochondria dolichoura n.g., n.sp., a copepod parasitic on the bathypelagic fish Anoplogaster cornuta (Valenciennes) in the western north Atlantic. Syst Parasitol 9:179–184CrossRefGoogle Scholar
  12. Huelsenbeck JP, Ronquist F (2001) MrBayes: bayesian inference of phylogeny. Bioinformatics 17:754–755PubMedCrossRefGoogle Scholar
  13. Jefferson TA, Leatherwood S, Webber MA (1993) FAO species identification guide. Marine mammals of the world. UNEP/FAO, RomeGoogle Scholar
  14. Jefferson TA, Webber MA, Pitman RL (2008) Marine mammals of the world, a comprehensive guide to their identification. Elsevier, AmsterdamGoogle Scholar
  15. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120PubMedCrossRefGoogle Scholar
  16. Klimpel S, Kellermanns E, Palm HW (2008) The role of pelagic swarm fish (Myctophidae: Teleostei) in the oceanic life cycle of Anisakis sibling species at the Mid-Atlantic Ridge. Parasitol Res 104:43–53PubMedCrossRefGoogle Scholar
  17. Klimpel S, Busch MW, Kellermanns E, Kleinertz S, Palm HW (2009) Metazoan deep-sea fish parasites. Acta Biologica Benrodis, Supplement 11. Verlag Natur & Wissenschaft, SolingenGoogle Scholar
  18. Klimpel S, Busch MW, Kuhn T, Rohde A, Palm HW (2010) The Anisakis simplex complex off the South Shetland Islands (Antarctica): endemic populations versus introduction through migratory hosts. Mar Ecol Prog Ser 403:1–11CrossRefGoogle Scholar
  19. Larget B, Simon B (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Mol Biol Evol 16:750–759Google Scholar
  20. 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
  21. Mattiucci S, Nascetti G (2008) Advances and trends in the molecular systematic of anisakid nematodes, with implications for their evolutionary ecology and host-parasite co-evolutionary processes. Adv Parasit 66:47–148CrossRefGoogle Scholar
  22. Mattiucci S, Paggi L, Nascetti G, Ishikura H, Kikuchi K, Sato N, Cianchi R, Bullini L (1998) Allozyme and morphological identification of Anisakis, Contracaecum and Pseudoterranova from Japanese waters (Nematoda, Ascaridoidea). Syst Parasitol 40:81–92CrossRefGoogle Scholar
  23. 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 relationship between congeners (Nematoda: Anisakidae). Syst Parasitol 61:157–171PubMedCrossRefGoogle Scholar
  24. Mattiucci S, Paoletti M, Damiano S, Nascetti G (2007) Molecular detection of sibling species in anisakid nematodes. Parassitologia 49:147–153PubMedGoogle Scholar
  25. Mattiucci S, Paoletti M, Webb SC (2009) Anisakis nascetti n. sp. from beaked whales of the southern hemisphere: morphological description, genetic relationships between congeners and ecological data. Syst Parasitol 75:199–217CrossRefGoogle Scholar
  26. McAlpine DF, Murison L, Hoberg E (1997) New records for the pygmy sperm whale Kogia breviceps (Physeteridae) from Atlantic Canada with notes on diet and parasites. Mar Mammal Sci 13:701–704CrossRefGoogle Scholar
  27. Moiseev SI (1991) Observation of the vertical distribution and behaviour of nektonic squids using manned submersibles. Bull Mar Sci 49:446–456Google Scholar
  28. Mullin KD, Hoggard W, Roden CL, Lohoefener RR, Rogers CM, Taggart B (1994) Cetaceans on the upper continental slope in the north-central Gulf of Mexico. Fish Bull 92:773–786Google Scholar
  29. Nikaido M, Matsuno F, Hamilton H, Brownell RL Jr, Cao Y, Ding W, Zuoyan Z, Shedlock AM, Fordyce RE, Hasegawa M, Okada N (2001) Retroposon analysis of major cetacean lineages: the monophyly of toothed whales and the paraphyly of river dolphins. Proc Natl Acad Sci USA 98:7384–7389PubMedCrossRefGoogle Scholar
  30. Palm HW (1999) Ecology of Pseudoterranova decipiens (Krabbe, 1878) (Nematoda: Anisakidae) from Antarctic waters. Parasitol Res 85:638–646PubMedCrossRefGoogle Scholar
  31. 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 45:3–12Google Scholar
  32. Panigada S, Pesante G, Zanardelli M, Oehen S (2003) Day and night-time behavior of fin whales in the western Ligurian Sea. In: Proceedings of the conference Ocean 2003, San Diego, California, USA, pp 466–471Google Scholar
  33. Pauly D, Trites AW, Capuli E, Christesen V (1998) Diet composition and trophic level of marine mammals. ICES J Mar Sci 55:467–481CrossRefGoogle Scholar
  34. Perrin WF, Gilpatrick JW Jr (1994) Spinner dolphin–Stenella longirostris (Gray, 1928). In: Ridgway SH, Harrison SR (eds) Handbook of marine mammals. Volume 5: the first book of dolphins. Academic Press, London, pp 99–128Google Scholar
  35. Perrin WF, Wursig B, Thewissen JGM (2009) Encyclopedia of marine mammals. Academic Press, LondonGoogle Scholar
  36. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  37. Post A (1986) Anoplogastridae. In: Whitehead PJP, Bauchot ML, Hureau JC, Nielsen J, Tortonese E (eds) Fishes of the north-eastern Atlantic and the Mediterranean. UNESCO, Paris, pp 767–768Google Scholar
  38. Reyes JC (1991) The conservation of small cetaceans: a review. Report prepared for the secretariat of the convention on the conservation of migratory species of wild animals. UNEP/CMS Secretariat, BonnGoogle Scholar
  39. Ross GJB (1978) Records of pygmy and dwarf sperm whales, genus Kogia, from southern Africa, with biological notes and some comparisons. Ann Cape Prov Mus Nat Hist 11:259–327Google Scholar
  40. Swofford DL (2003) PAUP* phylogenetic analysis using parsimony (*and other methods) version 4. Sinauer Associates, SunderlandGoogle Scholar
  41. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  42. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCrossRefGoogle Scholar
  43. Valentini A, Mattiucci S, Bondanelli P, Webb SC, Mignucci-Giannone A, Cólon-Llavina MM, Nascetti G (2006) Genetic relationship among Anisakis species (Nematoda: Anisakidae) inferred from mitochondrial cox-2 sequences, and comparison with allozyme data. J Parasitol 92:156–166PubMedCrossRefGoogle Scholar
  44. Wang MC, Walker WA, Shao KT, Chou LS (2002) Comparative analysis of the diets of pygmy sperm whales and dwarf sperm whales in Taiwanese waters. Acta Zool Taiwan 13:53–62Google Scholar
  45. West K, Walker W, Baird R, White W, Levine G, Brown E, Schofield D (2009) Diet of pygmy sperm whale (Kogia breviceps) in the Hawaiian Archipelago. Mar Mammal Sci 25:944–948CrossRefGoogle Scholar
  46. Westgate AJ, Read AJ, Bergren P, Koopman HN, Gaskin DE (1995) Diving behavior of harbor porpoises, Phocoena phocoena. Can J Fish Aqua Sci 52:1064–1073CrossRefGoogle Scholar
  47. Willis PM, Baird RW (1998) Status of the dwarf sperm whale, Kogia simus, with consideration of special reference to Canada. Can Field Nat 112:114–125Google Scholar
  48. Yang XG (2009) Bayesian inference of cetacean phylogeny based on mitochondrial genomes. Biologia 64:811–818CrossRefGoogle Scholar
  49. Zhu X, Gasser RB, Jacobs DE, Hung GC, Chilton NB (2000) Relationship among some ascaridoid nematodes based on ribosomal DNA sequence data. Parasitol Res 86:738–744PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Sven Klimpel
    • 1
  • Thomas Kuhn
    • 1
  • Markus W. Busch
    • 1
  • Horst Karl
    • 2
  • Harry W. Palm
    • 3
  1. 1.Institute for Ecology, Evolution and Diversity, Biodiversity and Climate Research Centre (BiK-F, LOEWE)Goethe-UniversityFrankfurt am MainGermany
  2. 2.Max Rubner—Institute, Federal Research Institute for Nutrition and Food, Department of Safety and Quality of Milk and Fish ProductsHamburgGermany
  3. 3.Aquaculture and Sea-Ranching, Faculty of Agricultural and Environmental SciencesUniversity RostockRostockGermany

Personalised recommendations