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

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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.

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References

  • Abollo E, Gestal C, Pascal S (2001) Anisakis infestation in marine fish and cephalopods from Galician waters: an updated perspective. Parasitol Res 87:492–499

    Article  PubMed  CAS  Google Scholar 

  • Baumgartner MF, Mullin KD, May LN, Leming TD (2001) Cetacean habitats in the northern Gulf of Mexico. Fish Bull 99:219–239

    Google Scholar 

  • Beatson EL (2007) The diet of pygmy sperm whales, Kogia breviceps, stranded in New Zealand: implications for conservation. Rev Fish Biol Fisher 17:295–303

    Article  Google Scholar 

  • Bush O, Lafferty AD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on his own terms: Margolis et al. revisited. J Parasitol 83:575–583

    Article  PubMed  CAS  Google Scholar 

  • 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 105:1239–1252

    Article  PubMed  Google Scholar 

  • 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 129:797–809

    CAS  Google Scholar 

  • 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 289:117–130

    Article  Google Scholar 

  • 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 14:490–507

    Article  Google Scholar 

  • Froese R, Pauly D (2010) Fishbase. World wide web electronic publication. www.fishbase.org, Version (03/2010)

  • 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 8:307–313

    Google Scholar 

  • 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 9:179–184

    Article  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MrBayes: bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Jefferson TA, Leatherwood S, Webber MA (1993) FAO species identification guide. Marine mammals of the world. UNEP/FAO, Rome

  • Jefferson TA, Webber MA, Pitman RL (2008) Marine mammals of the world, a comprehensive guide to their identification. Elsevier, Amsterdam

    Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  PubMed  CAS  Google Scholar 

  • 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 104:43–53

    Article  PubMed  Google Scholar 

  • Klimpel S, Busch MW, Kellermanns E, Kleinertz S, Palm HW (2009) Metazoan deep-sea fish parasites. Acta Biologica Benrodis, Supplement 11. Verlag Natur & Wissenschaft, Solingen

    Google Scholar 

  • 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 403:1–11

    Article  CAS  Google Scholar 

  • Larget B, Simon B (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Mol Biol Evol 16:750–759

    CAS  Google Scholar 

  • Mattiucci S, Nascetti G (2006) Molecular systematics, phylogeny and ecology of anisakid nematodes of the genus Anisakis Dujardin, 1845: an update. Parasite 13:99–113

    PubMed  CAS  Google Scholar 

  • 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 66:47–148

    Article  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, Contracaecum and Pseudoterranova from Japanese waters (Nematoda, Ascaridoidea). Syst Parasitol 40:81–92

    Article  Google Scholar 

  • 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 61:157–171

    Article  PubMed  Google Scholar 

  • Mattiucci S, Paoletti M, Damiano S, Nascetti G (2007) Molecular detection of sibling species in anisakid nematodes. Parassitologia 49:147–153

    PubMed  CAS  Google Scholar 

  • 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 75:199–217

    Article  Google Scholar 

  • 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 13:701–704

    Article  Google Scholar 

  • Moiseev SI (1991) Observation of the vertical distribution and behaviour of nektonic squids using manned submersibles. Bull Mar Sci 49:446–456

    Google Scholar 

  • 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 92:773–786

    Google Scholar 

  • 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 98:7384–7389

    Article  PubMed  CAS  Google Scholar 

  • Palm HW (1999) Ecology of Pseudoterranova decipiens (Krabbe, 1878) (Nematoda: Anisakidae) from Antarctic waters. Parasitol Res 85:638–646

    Article  PubMed  CAS  Google Scholar 

  • 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 45:3–12

  • 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 466–471

  • Pauly D, Trites AW, Capuli E, Christesen V (1998) Diet composition and trophic level of marine mammals. ICES J Mar Sci 55:467–481

    Article  Google Scholar 

  • 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 99–128

    Google Scholar 

  • Perrin WF, Wursig B, Thewissen JGM (2009) Encyclopedia of marine mammals. Academic Press, London

    Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • 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 767–768

    Google Scholar 

  • 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, Bonn

  • 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 11:259–327

    Google Scholar 

  • Swofford DL (2003) PAUP* phylogenetic analysis using parsimony (*and other methods) version 4. Sinauer Associates, Sunderland

    Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • 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 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  • 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 92:156–166

    Article  PubMed  CAS  Google Scholar 

  • 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 13:53–62

    Google Scholar 

  • 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 25:944–948

    Article  Google Scholar 

  • Westgate AJ, Read AJ, Bergren P, Koopman HN, Gaskin DE (1995) Diving behavior of harbor porpoises, Phocoena phocoena. Can J Fish Aqua Sci 52:1064–1073

    Article  Google Scholar 

  • Willis PM, Baird RW (1998) Status of the dwarf sperm whale, Kogia simus, with consideration of special reference to Canada. Can Field Nat 112:114–125

    Google Scholar 

  • Yang XG (2009) Bayesian inference of cetacean phylogeny based on mitochondrial genomes. Biologia 64:811–818

    Article  CAS  Google Scholar 

  • Zhu X, Gasser RB, Jacobs DE, Hung GC, Chilton NB (2000) Relationship among some ascaridoid nematodes based on ribosomal DNA sequence data. Parasitol Res 86:738–744

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The present study was financially supported by the German Research Council (DFG KL 2087/1-1, 1-2, PA 664/4-2, 664/6-1), by the Research and Innovation funds of the Heinrich-Heine-University Düsseldorf and the Gesellschaft für Ichthyologie e.V. (GiF). The study was a contribution to Mar-Eco, a field study of the Census of Marine Life program.

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Authors and Affiliations

  1. Institute for Ecology, Evolution and Diversity, Biodiversity and Climate Research Centre (BiK-F, LOEWE), Goethe-University, Senckenberganlage 25, 60325, Frankfurt am Main, Germany

    Sven Klimpel, Thomas Kuhn & Markus W. Busch

  2. Max Rubner—Institute, Federal Research Institute for Nutrition and Food, Department of Safety and Quality of Milk and Fish Products, Palmaille 9, 22767, Hamburg, Germany

    Horst Karl

  3. Aquaculture and Sea-Ranching, Faculty of Agricultural and Environmental Sciences, University Rostock, Justus-von-Liebig-Weg 6, 18059, Rostock, Germany

    Harry W. Palm

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  1. Sven Klimpel
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Correspondence to Harry W. Palm.

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Klimpel, S., Kuhn, T., Busch, M.W. et al. Deep-water life cycle of Anisakis paggiae (Nematoda: Anisakidae) in the Irminger Sea indicates kogiid whale distribution in north Atlantic waters. Polar Biol 34, 899–906 (2011). https://doi.org/10.1007/s00300-010-0946-1

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