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Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Genetic characterisation and taxonomy of species of Anisakis (Nematoda : Anisakidae) parasitic in Australian marine mammals

Shokoofeh Shamsi A C , Robin Gasser B and Ian Beveridge B
+ Author Affiliations
- Author Affiliations

A School of Animal and Veterinary Sciences, Charles Sturt University, Boorooma Street, Estella, NSW 2678, Australia.

B Department of Veterinary Science, The University of Melbourne, 250 Princes Highway, Werribee, Vic. 3030, Australia.

C Corresponding author. Email: sshamsi@csu.edu.au

Invertebrate Systematics 26(2) 204-212 https://doi.org/10.1071/IS11019
Submitted: 11 May 2011  Accepted: 6 February 2012   Published: 6 August 2012

Abstract

Three species of Anisakis from Australian marine mammals, including Anisakis brevispiculata, A. simplex C and A. pegreffii, are described and characterised genetically on the basis of sequence data for the first and second internal transcribed spacers (ITS-1 and ITS-2) of nuclear rDNA. Parasite specimens were collected from Delphinus delphis, Tursiops truntatus and Kogia sima in Australia. A. brevispiculata is reported for the first time in Australia. However, analyses of sequence data suggests that A. brevispiculata in Australia is genetically distinct from specimens considered to represent the same species from other parts of the world. Fourth larval and adult stages of A. pegreffii were found in dolphins. Assigning larvae to A. pegreffii was based on the ITS-1 and ITS-2 sequences. A description of these larvae also is provided. Furthermore, fourth-stage larvae of A. simplex C were found in Kogia sima. Alignments of ITS-1 and ITS-2 sequences for members of A. simplex sensu lato revealed that nucleotide differences in ITS-1 can be used to differentiate among members of A. simplex sensu lato. This study reinforces the use of a combined molecular and morphological approach for the specific identification of anisakid nematodes.


References

Abe, N., Ohya, N., and Yanagiguchi, R. (2005). Molecular characterization of Anisakis pegreffii larvae in Pacific cod in Japan. Journal of Helminthology 79, 303–306.
Molecular characterization of Anisakis pegreffii larvae in Pacific cod in Japan.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xnt12jtQ%3D%3D&md5=a91953fb94a976026b6180e537c87afdCAS |

Abollo, E., Lopez, A., Gestal, C., Benavente, P., and Pascual, S. (1998). Long-term recording of gastric ulcers in cetaceans stranded on the Galician (NW Spain) coast. Diseases of Aquatic Organisms 32, 71–73.
Long-term recording of gastric ulcers in cetaceans stranded on the Galician (NW Spain) coast.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1czktV2msg%3D%3D&md5=f7a7095e766a43986446feb9e8d3848dCAS |

Abollo, E., Paggi, L., Pascual, S., and D’Amelio, S. (2003). Occurrence of recombinant genotypes of Anisakis simplex s.s. and Anisakis pegreffii (Nematoda: Anisakidae) in an area of sympatry. Infection, Genetics and Evolution 3, 175–181.
Occurrence of recombinant genotypes of Anisakis simplex s.s. and Anisakis pegreffii (Nematoda: Anisakidae) in an area of sympatry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXns1KlsL4%3D&md5=6d8a3ba04bf423b26d31940d9280a4b0CAS |

Anderson, R. C. (2000). ‘Nematode Parasites of Vertebrates: their Development and Transmission.’ (CABI Publishing: Wallingford, UK.)

Andrews, R. H., and Chilton, N. B. (1999). Multilocus enzyme electrophoresis: a valuable technique for providing answers to problems in parasite systematics. International Journal for Parasitology 29, 213–253.
Multilocus enzyme electrophoresis: a valuable technique for providing answers to problems in parasite systematics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXisVWjt74%3D&md5=64ff0664c4300c1ca9ce4eacd23a97e4CAS |

Baylis, H. A. (1923). An ascarid from the sperm whale. Annals & Magazine of Natural History 9, 2011–2017.

Cannon, L. R. G. (1977a). Some aspects of the biology of Peponocephala electra (Cetacea: Delphinidae). II. Parasites. Australian Journal of Marine and Freshwater Research 28, 717–722.
Some aspects of the biology of Peponocephala electra (Cetacea: Delphinidae). II. Parasites.Crossref | GoogleScholarGoogle Scholar |

Cannon, L. R. G. (1977b). Some larval ascaridoids from south-eastern Queensland marine fishes. International Journal for Parasitology 7, 233–243.
Some larval ascaridoids from south-eastern Queensland marine fishes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2s3islSmsg%3D%3D&md5=0a909d3c6c8aeccad5296c3a66491a4bCAS |

Cheng, T. C. (1982). Anisakiasis. In ‘CRC Handbook for Zoonoses. Section C: Parasitic Zoonoses. Vol. II’. (Ed. J. H. Steele.) pp. 37–54. (CRC Press: Boca Raton, FL.)

Chilton, N. B., Gasser, R. B., and Beveridge, I. (1995). Differences in a ribosomal DNA sequence of morphologically indistinguishable species within the Hypodontus macropi complex (Nematoda: Strongyloidea). International Journal for Parasitology 25, 647–651.
Differences in a ribosomal DNA sequence of morphologically indistinguishable species within the Hypodontus macropi complex (Nematoda: Strongyloidea).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmsVKjs7c%3D&md5=c6428f95b02bd76f5da49bd0808b9205CAS |

D’Amelio, S., Mathiopoulos, K. D., Santos, C. P., Pugachev, O. N., Webb, S. C., Picanço, M., and Paggi, L. (2000). Genetic markers in ribosomal DNA for the identification of members of the genus Anisakis (Nematoda: Ascaridoidea) defined by polymerase-chain-reaction-based restriction fragment length polymorphism. International Journal for Parasitology 30, 223–226.
Genetic markers in ribosomal DNA for the identification of members of the genus Anisakis (Nematoda: Ascaridoidea) defined by polymerase-chain-reaction-based restriction fragment length polymorphism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXis1Sgs7w%3D&md5=b2d8579d65c008c3282bdfdcc01e4544CAS |

Davey, J. T. (1971). A revision of the genus Anisakis Dujardin, 1845 (Nematoda: Ascaridata). Journal of Helminthology 45, 51–72.
A revision of the genus Anisakis Dujardin, 1845 (Nematoda: Ascaridata).Crossref | GoogleScholarGoogle Scholar |

Dollfus, R. P. (1966). Helminthofaune de Kogia breviceps (Blainville 1838) cetacé odontocète. Annales de la Société des Sciences Naturelle. Charente-Maritime 4, 3–6.

Dollfus, R. P. (1968). Nematodes des cetacés odontocètes (Globicephalus et Tursiops). Bulletin de l’Institut des Peches Maritimes du Maroc 16, 35–53.

Dujardin, F. (1845). ‘Histoire Naturelle des Helminthes ou vers intestinaux.’ (Libraire Encyclopédique de Roret: Paris.)

Fagerholm, H. P. (1991). Systematic implications of male caudal morphology in ascaridoid nematode parasites. Systematic Parasitology 19, 215–229.
Systematic implications of male caudal morphology in ascaridoid nematode parasites.Crossref | GoogleScholarGoogle Scholar |

Geraci, J. R., and St Aubin, D. J. (1987). Effects of parasites on marine mammals. International Journal for Parasitology 17, 407–414.
Effects of parasites on marine mammals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2s3itFWlsA%3D%3D&md5=d045a8d3700a54cec63b396df95f195fCAS |

Grabda, J. (1976). Studies on the life cycle and morphogenesis of Anisakis simplex (Rudolphi, 1809) (Nematoda: Anisakidae) cultured in vitro. Acta Ichthyologica et Piscatoria 6, 119–141.

Hartwich, G. (1964). Revision der vogelparasitischen Nematoden mitteleuropas, II. Der Gattung Contracaecum Railliet & Henry, 1912. Mitteilungen aus dem Zoologischen Museum, Berlin 40, 15–53.

Jefferies, D. J., Hanson, H. M., and Harris, E. A. (1990). The prevalence of Pseudoterranova decipiens (Nematoda) and Corynosoma strumosum (Acanthocephala) in otters Lutra lutra from coastal sites in Britain. Journal of Zoology 221, 316–321.
The prevalence of Pseudoterranova decipiens (Nematoda) and Corynosoma strumosum (Acanthocephala) in otters Lutra lutra from coastal sites in Britain.Crossref | GoogleScholarGoogle Scholar |

Johnston, T. H. (1938). Parasitic nematoda. Scientific Reports of the Australian Antarctic Expedition. Series C 10, 1–31.

Johnston, T. H., and Mawson, P. M. (1939). Internal parasites of the pigmy sperm whale. Records of the South Australian Museum 6, 263–274.

Johnston, T. H., and Mawson, P. M. (1941). Nematodes from Australian marine mammals. Records of the South Australian Museum 6, 429–434.

Johnston, T. H., and Mawson, P. M. (1945). Parasitic nematodes. British, Australian and New Zealand Antarctic Research Expedition. Reports, Series B 5, 73–159.

Johnston, T. H., and Mawson, P. M. (1951). Report on some parasitic nematodes from the Australian Museum. Records of the Australian Museum 22, 289–297.
Report on some parasitic nematodes from the Australian Museum.Crossref | GoogleScholarGoogle Scholar |

Johnston, T. H., and Mawson, P. M. (1952). Some nematodes from Australian birds and mammals. Transactions of the Royal Society of South Australia 75, 30–37.

Johnston, T. H., and Mawson, P. M. (1953). Parasitic nematodes and trematodes from Campbell and Auckland Islands (Cape Expedition). Records of the Dominion Museum 2, 63–71.

Lymbery, A. J., Doupe, R. G., Munshi, M. A., and Wong, T. (2002). Larvae of Contracaecum sp. among inshore fish species of southwestern Australia. Diseases of Aquatic Organisms 51, 157–159.
Larvae of Contracaecum sp. among inshore fish species of southwestern Australia.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38ngvVOmtw%3D%3D&md5=3789ec11cd46823d64960dfe58a87349CAS |

Mackerras, M. J. (1958). Catalogue of Australian mammals and their recorded internal parasites. I–IV. Part IV. Man. Proceedings of the Linnean Society of New South Wales 83, 153–160.

Mattiucci, S., and Nascetti, G. (2006). Molecular systematics, phylogeny and ecology of anisakid nematodes of the genus Anisakis Dujardin, 1845: an update. Parasite (Paris, France) 13, 99–113.
| 1:STN:280:DC%2BD28zotl2itQ%3D%3D&md5=a29b7ef7b36e42081d99bd8c57ae983aCAS |

Mattiucci, S., and Nascetti, G. (2008). Advances and trends in the molecular systematics of anisakid nematodes, with implications for their evolutionary ecology and host–parasite co-evolutionary processes. Advances in Parasitology 66, 47–148.
Advances and trends in the molecular systematics of anisakid nematodes, with implications for their evolutionary ecology and host–parasite co-evolutionary processes.Crossref | GoogleScholarGoogle Scholar |

Mattiucci, S., Nascetti, G., Bullini, L., Orecchia, P., and Paggi, L. (1986). Genetic structure of Anisakis physeteris, and its differentiation from the Anisakis simplex complex (Ascaridida: Anisakidae). Parasitology 93, 383–387.
Genetic structure of Anisakis physeteris, and its differentiation from the Anisakis simplex complex (Ascaridida: Anisakidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xmt1eitL4%3D&md5=901330238e11b694eeea00954d6a81a0CAS |

Mattiucci, S., Nascetti, G., Cianchi, R., Paggi, L., Arduino, P., Margolis, L., Brattey, J., Webb, S., D’Amelio, S., Orecchia, P., and Bullini, L. (1997). Genetic and ecological data on the Anisakis simplex complex, with evidence for a new species (Nematoda, Ascaridoidea, Anisakidae). The Journal of Parasitology 83, 401–416.
Genetic and ecological data on the Anisakis simplex complex, with evidence for a new species (Nematoda, Ascaridoidea, Anisakidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlsFCis7w%3D&md5=377f72010cf6aedd3095b00bc1d36250CAS |

Mattiucci, S., Paggi, L., Nascetti, G., Abollo, E., Webb, S. C., Pascual, S., Cianchi, R., and Bullini, L. (2001). Genetic divergence and reproductive isolation between Anisakis brevispiculata and Anisakis physeteris (Nematoda: Anisakidae). International Journal for Parasitology 31, 9–14.
Genetic divergence and reproductive isolation between Anisakis brevispiculata and Anisakis physeteris (Nematoda: Anisakidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXpslOmtw%3D%3D&md5=b726d869e244ecaf6e600fb175d14798CAS |

Mattiucci, S., Turchetto, M., Bragantini, F., and Nascetti, G. (2002). On the occurrence of the sibling species of Contracaecum rudolphii complex (Nematoda: Anisakidae) in cormorants (Phalacrocorax carbo sinensis) from Venice and Caorle Lagoons: genetic markrs and ecological studies. Parassitologia 44, 105.

Mattiucci, S., Nascetti, G., Dailey, M., Webb, S. C., Barros, N. B., Cianchi, R., and Bullini, L. (2005). Evidence for a new species of Anisakis Dujardin, 1845: morphological description and genetic relationships between congeners (Nematoda: Anisakidae). Systematic Parasitology 61, 157–171.
Evidence for a new species of Anisakis Dujardin, 1845: morphological description and genetic relationships between congeners (Nematoda: Anisakidae).Crossref | GoogleScholarGoogle Scholar |

Mawson, P. (1953). Parasitic nematoda collected by the Australian national Antarctic research expedition: Heard Island and Macquarie Island, 1948–1951. Parasitology 43, 291–297.
Parasitic nematoda collected by the Australian national Antarctic research expedition: Heard Island and Macquarie Island, 1948–1951.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaG2c%2Fjt1Ontw%3D%3D&md5=db158d625c2e5f6a5120cb6a9745cd3cCAS |

McColl, K. A., and Obendorf, D. L. (1982). Helminth parasites and associated pathology in stranded Fraser’s dolphins, Lagenodelphis hosei (Fraser, 1956). Aquatic Mammals 9, 30–34.

Nadler, S. A., D’Amelio, S., Dailey, M. D., Paggi, L., Siu, S., and Sakanari, J. A. (2005). Molecular phylogenetics and diagnosis of Anisakis, Pseudoterranova, and Contracaecum from northern Pacific marine mammals. The Journal of Parasitology 91, 1413–1429.
Molecular phylogenetics and diagnosis of Anisakis, Pseudoterranova, and Contracaecum from northern Pacific marine mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XitVGksLc%3D&md5=7b654a53a863077b21fc3201cf4ed2a4CAS |

Nascetti, G., Paggi, L., Orecchia, P., Mattiucci, S., and Bullini, L. (1983). Two sibling species within Anisakis simplex (Ascaridida: Anisakidae). Parassitologia 25, 306–307.

Nascetti, G., Paggi, L., Orecchia, P., Smith, J. W., Mattiucci, S., and Bullini, L. (1986). Electrophoretic studies on the Anisakis simplex (Ascaridida: Anisakidae) from the Mediterranean and north-east Atlantic. International Journal for Parasitology 16, 633–640.
Electrophoretic studies on the Anisakis simplex (Ascaridida: Anisakidae) from the Mediterranean and north-east Atlantic.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXotFyrsg%3D%3D&md5=8bdbebf29ab402a44513fb6cdae3ecbfCAS |

Paggi, L., Nascetti, G., Webb, S. C., Mattiucci, S., Cianchi, R., and Bullini, L. (1998). A new species of Anisakis Dujardin, 1845 (Nematoda, Anisakidae) from beaked whales (Ziphiidae): allozyme and morphological evidence. Systematic Parasitology 40, 161–174.
A new species of Anisakis Dujardin, 1845 (Nematoda, Anisakidae) from beaked whales (Ziphiidae): allozyme and morphological evidence.Crossref | GoogleScholarGoogle Scholar |

Paggi, L., Mattiucci, S., and D’Amelio, S. (2001). Allozyme and PCR-RFLP markers in anisakid nematodes, aetiological agents of human anisakidosis. Parassitologia 43, 21–27.

Quiazon, K. M. A., Yoshinaga, T., Ogawa, K., and Yukami, R. (2008). Morphological differences between larvae and in vitro-cultured adults of Anisakis simplex (sensu stricto) and Anisakis pegreffii (Nematoda: Anisakidae). Parasitology International 57, 483–489.
Morphological differences between larvae and in vitro-cultured adults of Anisakis simplex (sensu stricto) and Anisakis pegreffii (Nematoda: Anisakidae).Crossref | GoogleScholarGoogle Scholar |

Shamsi, S., Gasser, R., Beveridge, I., and Shabani, A. A. (2008). Contracaecum pyripapillatum n. sp. and a description of C. multipapillatum (von Drasche, 1882) from the Australian pelican, Pelecanus conspicillatus. Parasitology Research 103, 1031–1039.
Contracaecum pyripapillatum n. sp. and a description of C. multipapillatum (von Drasche, 1882) from the Australian pelican, Pelecanus conspicillatus.Crossref | GoogleScholarGoogle Scholar |

Shamsi, S., Norman, R., Gasser, R., and Beveridge, I. (2009a). Genetic and morphological evidences for the existence of sibling species within Contracaecum rudolphii (Hartwich, 1964) (Nematoda: Anisakidae) in Australia. Parasitology Research 105, 529–538.
Genetic and morphological evidences for the existence of sibling species within Contracaecum rudolphii (Hartwich, 1964) (Nematoda: Anisakidae) in Australia.Crossref | GoogleScholarGoogle Scholar |

Shamsi, S., Norman, R., Gasser, R., and Beveridge, I. (2009b). Redescription and genetic characterization of selected Contracaecum spp. (Nematoda: Anisakidae) from various hosts in Australia. Parasitology Research 104, 1507–1525.
Redescription and genetic characterization of selected Contracaecum spp. (Nematoda: Anisakidae) from various hosts in Australia.Crossref | GoogleScholarGoogle Scholar |

Shamsi, S., Eisenbarth, A., Saptarshi, S., Beveridge, I., Gasser, R. B., and Lopata, A. L. (2011). Occurrence and abundance of anisakid nematode larvae in five species of fish from southern Australian waters. Parasitology Research 108, 927–934.
Occurrence and abundance of anisakid nematode larvae in five species of fish from southern Australian waters.Crossref | GoogleScholarGoogle Scholar |

Stroud, R. K., and Roffe, T. J. (1979). Causes of death in marine mammals stranded along the Oregon coast. Journal of Wildlife Diseases 15, 91–97.
| 1:STN:280:DyaE1M3hvFWksw%3D%3D&md5=6ed56c0826a704fd33783e56a1cf5a6bCAS |

Thompson, J. D., Gibson, T. J., Plewniac, F., Jeanmougin, F., and Higgins, D. G. (1997). The Clustal X windows interface : flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.
The Clustal X windows interface : flexible strategies for multiple sequence alignment aided by quality analysis tools.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntFyntQ%3D%3D&md5=7634ff92091e34d81ff1696f63bf889cCAS |

Van Dyke, S., and Strahan, R. (2008). ‘The Mammals of Australia.’ (Reed New Holland: Sydney.)