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Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE

First report of nymphs of the introduced pentastomid, Linguatula serrata, in red-necked wallabies (Notamacropus rufogriseus) in Australia

Diane P. Barton https://orcid.org/0000-0002-7462-9501 A C , Megan Porter A B , Ashleigh Baker https://orcid.org/0000-0003-2082-2581 A B , Xiaocheng Zhu A B , David J. Jenkins A B and Shokoofeh Shamsi A B
+ Author Affiliations
- Author Affiliations

A School of Animal and Veterinary Sciences, Charles Sturt University, Wagga Wagga, NSW 2678, Australia.

B Graham Centre for Agricultural Innovation, Charles Sturt University, Wagga Wagga, NSW 2678, Australia.

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

Australian Journal of Zoology 67(2) 106-113 https://doi.org/10.1071/ZO20017
Submitted: 18 March 2020  Accepted: 6 May 2020   Published: 25 May 2020

Abstract

The presence of nymphs of the introduced pentastomid parasite Linguatula serrata is verified in a native Australian animal, the red-necked wallaby (Notamacropus rufogriseus), for the first time. Morphological and genetic analyses confirmed the species identification, with a 100% genetic match to samples collected from various introduced animals from the same location in Kosciuszko National Park. Previous reports of pentastomids, including possible Linguatula sp. infections, in native animals are discussed. More research is required to confirm the validity of these reports.


References

Barnard, C. E., and Park, A. (1893). Notes on Spiroptera associated with tuberculosis in cattle. Report of the Australian Association for the Advancement of Science 5, 642–645.

Barton, D. P., Baker, A., Porter, M., Zhu, X., Jenkins, D. J., and Shamsi, S. (2020). Verification of rabbits as intermediate hosts for Linguatula serrata (Pentastomida) in Australia. Parasitology Research 119, 1553–1562.
Verification of rabbits as intermediate hosts for Linguatula serrata (Pentastomida) in Australia.Crossref | GoogleScholarGoogle Scholar | 32236709PubMed |

Beveridge, I., and Gasser, R. B. (2014). Diversity in parasitic helminths of Australasian marsupials and monotremes: a molecular perspective. International Journal for Parasitology 44, 859–864.
Diversity in parasitic helminths of Australasian marsupials and monotremes: a molecular perspective.Crossref | GoogleScholarGoogle Scholar | 24992656PubMed |

Chen, S.-H., Liu, Q., Zhang, Y.-N., Chen, J.-X., Li, H., Chen, Y., Steinmann, P., and Zhou, X.-N. (2010). Multi-host model-based identification of Armillifer agkistrodontis (Pentastomida), a new zoonotic parasite from China. PLoS Neglected Tropical Diseases 4, e647.
Multi-host model-based identification of Armillifer agkistrodontis (Pentastomida), a new zoonotic parasite from China.Crossref | GoogleScholarGoogle Scholar | 20386597PubMed |

Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
jModelTest 2: more models, new heuristics and parallel computing.Crossref | GoogleScholarGoogle Scholar | 22847109PubMed |

Davis, N. E., Forsyth, D. M., Triggs, B., Pascoe, C., Benshemesh, J., Robley, A., Lawrence, J., Ritchie, E. G., Nimmo, D. G., and Lumsden, L. F. (2015). Interspecific and geographic variation in the diets of sympatric carnivores: dingoes/wild dogs and red foxes in south-eastern Australia. PLoS One 10, e0120975.
Interspecific and geographic variation in the diets of sympatric carnivores: dingoes/wild dogs and red foxes in south-eastern Australia.Crossref | GoogleScholarGoogle Scholar | 26042803PubMed |

Durie, P. H., and Riek, R. F. (1952). The role of the dingo and wallaby in the infestation of cattle with hydatids (Echinococcus granulosus (Batsch, 1786) Rudolphi, 1805) in Queensland. Australian Veterinary Journal 28, 249–254.
The role of the dingo and wallaby in the infestation of cattle with hydatids (Echinococcus granulosus (Batsch, 1786) Rudolphi, 1805) in Queensland.Crossref | GoogleScholarGoogle Scholar |

Eslami, G., Khalatbari-Limaki, S., Oryan, A., Zohortabar, A., Amiri, A., and Hajimohammadi, B. (2017). A survey on prevalence and molecular characteristics of Linguatula serrata isolated from slaughtered sheep and goat in Yazd slaughterhouse. Journal of Veterinary Research 72, 403–410.
A survey on prevalence and molecular characteristics of Linguatula serrata isolated from slaughtered sheep and goat in Yazd slaughterhouse.Crossref | GoogleScholarGoogle Scholar |

Fleming, P. J. S., Allen, L. R., Lapidge, S. J., Robley, A., Saunders, G. R., and Thomson, P. C. (2006). A strategic approach to mitigating the impacts of wild canids: proposed activities of the Invasive Animals Cooperative Research Centre. Australian Journal of Experimental Agriculture 46, 753–762.
A strategic approach to mitigating the impacts of wild canids: proposed activities of the Invasive Animals Cooperative Research Centre.Crossref | GoogleScholarGoogle Scholar |

Ghorashi, S. A., Tavassoli, M., Peters, A., Shamsi, S., and Hajipour, N. (2016). Phylogenetic relationships among Linguatula serrata isolates from Iran based on 18S rRNA and mitochondrial cox1 gene sequences. Acta Parasitologica 61, 195–200.
Phylogenetic relationships among Linguatula serrata isolates from Iran based on 18S rRNA and mitochondrial cox1 gene sequences.Crossref | GoogleScholarGoogle Scholar | 27149706PubMed |

Gjerde, B. (2013). Phylogenetic position of Linguatula arctica and Linguatula serrata (Pentastomida) as inferred from the nuclear 18S rRNA gene and the mitochondrial cytochrome c oxidase subunit I gene. Parasitology Research 112, 3517–3525.
Phylogenetic position of Linguatula arctica and Linguatula serrata (Pentastomida) as inferred from the nuclear 18S rRNA gene and the mitochondrial cytochrome c oxidase subunit I gene.Crossref | GoogleScholarGoogle Scholar | 23873617PubMed |

Glen, A. S., and Dickman, C. R. (2006). Diet of the spotted-tailed quoll (Dasyurus maculatus) in eastern Australia: effects of season, sex and size. Journal of Zoology 269, 241–248.
Diet of the spotted-tailed quoll (Dasyurus maculatus) in eastern Australia: effects of season, sex and size.Crossref | GoogleScholarGoogle Scholar |

Gomez-Puerta, L. A., Pacheco, J. I., Angulo-Tisoc, J. M., Lopez-Urbina, M. T., and Gonzalez, A. E. (2017). First finding of nymphal stages of Linguatula serrata in a South American camelid, a vicuña from Peru. Veterinary Parasitology 244, 21–24.
First finding of nymphal stages of Linguatula serrata in a South American camelid, a vicuña from Peru.Crossref | GoogleScholarGoogle Scholar | 28917312PubMed |

Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.
BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT.Crossref | GoogleScholarGoogle Scholar |

Jenkins, D. J., and Macpherson, C. N. L. (2003). Transmission ecology of Echinococcus in wild-life in Australia and Africa. Parasitology 127, S63–S72.
Transmission ecology of Echinococcus in wild-life in Australia and Africa.Crossref | GoogleScholarGoogle Scholar | 15027605PubMed |

Johnson, E. A. (1910). Note on a new Linguatula. Transactions and Proceedings of the Royal Society of South Australia 34, 248–250.

Johnston, T. H. (1911). Notes and exhibits. Proceedings of the Linnean Society of New South Wales 36, 157–158.

Johnston, T. H., and Cleland, J. B. (1910). A note on the occurrence of pentastomes in Australian cattle. Journal and Proceedings of the Royal Society of New South Wales 44, 315–318.

King, J. S., Jenkins, D. J., Ellis, J. T., Fleming, P., Windsor, P. A., and Šlapeta, J. (2011). Implications of wild dog ecology on the sylvatic and domestic life cycle of Neospora caninum in Australia. Veterinary Journal 188, 24–33.
Implications of wild dog ecology on the sylvatic and domestic life cycle of Neospora caninum in Australia.Crossref | GoogleScholarGoogle Scholar |

Mackerras, J. (1958). Catalogue of Australian mammals and their recorded internal parasites. I–IV. Proceedings of the Linnean Society of New South Wales 83, 101–160.

Mohanta, U. K., and Itagaki, T. (2017). Molecular characterization and phylogeny of Linguatula serrata (Pentastomida: Linguatulidae) based on the nuclear 18S rDNA and mitochondrial cytochrome c oxidase I gene. The Journal of Veterinary Medical Science 79, 398–402.
Molecular characterization and phylogeny of Linguatula serrata (Pentastomida: Linguatulidae) based on the nuclear 18S rDNA and mitochondrial cytochrome c oxidase I gene.Crossref | GoogleScholarGoogle Scholar | 27941305PubMed |

Pullar, E. M. (1936). A note on the occurrence of Linguatula serrata (Frochlich, 1789) in Australia. Australian Veterinary Journal 12, 61–64.
A note on the occurrence of Linguatula serrata (Frochlich, 1789) in Australia.Crossref | GoogleScholarGoogle Scholar |

Ralph, T. S. (1865). On the parasitic origin of pleuro-pneumonia in cattle; being the report made to the pleuro-pneumonia commission. The Australian Medical Journal 10, 1–10.

Rezaei, H., Ashrafihelan, J., Nematollahi, A., and Mostafavi, E. (2012). The prevalence of Linguatula serrata nymphs in goats slaughtered in Tabriz, Iran. Journal of Parasitic Diseases 36, 200–202.
The prevalence of Linguatula serrata nymphs in goats slaughtered in Tabriz, Iran.Crossref | GoogleScholarGoogle Scholar | 24082527PubMed |

Riley, J. (1986). The biology of pentastomids. Advances in Parasitology 25, 45–128.
The biology of pentastomids.Crossref | GoogleScholarGoogle Scholar | 3535437PubMed |

Riley, J., Spratt, D. M., and Presidente, P. J. A. (1985). Pentastomids (Arthropoda) parasitic in Australian reptiles and mammals. Australian Journal of Zoology 33, 39–53.
Pentastomids (Arthropoda) parasitic in Australian reptiles and mammals.Crossref | GoogleScholarGoogle Scholar |

Ronquist, F., and Huelsenbeck, J. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
MrBayes 3: Bayesian phylogenetic inference under mixed models.Crossref | GoogleScholarGoogle Scholar | 12912839PubMed |

Shamsi, S., McSpadden, K., Baker, S., and Jenkins, D. (2017). Occurrence of tongue worm, Linguatula cf. seratta (Pentastomida: Linguatilidae) in wild canids and livestock in south-eastern Australia. International Journal for Parasitology: Parasites and Wildlife 6, 271–277.
Occurrence of tongue worm, Linguatula cf. seratta (Pentastomida: Linguatilidae) in wild canids and livestock in south-eastern Australia.Crossref | GoogleScholarGoogle Scholar | 28971014PubMed |

Shamsi, S., Barton, D. P., Zhu, X., and Jenkins, D. J. (2020a). Characterisation of the tongue worm, Linguatula serrata (Pentastomida: Linguatulidae), in Australia. International Journal for Parasitology: Parasites and Wildlife 11, 149–157.
Characterisation of the tongue worm, Linguatula serrata (Pentastomida: Linguatulidae), in Australia.Crossref | GoogleScholarGoogle Scholar | 32071862PubMed |

Shamsi, S., Halajian, A., Barton, D. P., Zhu, X., Smit, W. J., Roux, F., and Luus-Pwell, W. J. (2020b). Occurrence and characterisation of tongue worms, Linguatula spp., in South Africa. International Journal for Parasitology: Parasites and Wildlife 11, 268–281.
Occurrence and characterisation of tongue worms, Linguatula spp., in South Africa.Crossref | GoogleScholarGoogle Scholar | 32211289PubMed |

Slattery, D. (2016). ‘Australian Alps: Kosciuszko, Alpine and Namadgi National Parks.’ (CSIRO Publishing: Melbourne.)

Sparkes, J., Ballard, G., Fleming, P. J. S., van de Ven, R., and Körtner, G. (2016). Contact rates of wild-living and domestic dog populations in Australia: a new approach. Oecologia 182, 1007–1018.
Contact rates of wild-living and domestic dog populations in Australia: a new approach.Crossref | GoogleScholarGoogle Scholar | 27660202PubMed |

Spratt, D. M. (2002). Parasites and pathology of the respiratory tracts of native and feral mammals in Australia – a review. Australian Mammalogy 24, 177–192.
Parasites and pathology of the respiratory tracts of native and feral mammals in Australia – a review.Crossref | GoogleScholarGoogle Scholar |

Spratt, D. M., and Beveridge, I. (2018). Wildlife parasitology in Australia: past, present and future. Australian Journal of Zoology 66, 286–305.
Wildlife parasitology in Australia: past, present and future.Crossref | GoogleScholarGoogle Scholar |

Turni, C., and Smales, L. R. (2001). Parasites of the bridled nailtail wallaby (Onychogalea fraenata) (Marsupialia: Macropodidae). Wildlife Research 28, 403–411.
Parasites of the bridled nailtail wallaby (Onychogalea fraenata) (Marsupialia: Macropodidae).Crossref | GoogleScholarGoogle Scholar |