Abstract
We confirm the presence of nymphs of the introduced pentastomid, Linguatula serrata, in the introduced rabbit, Oryctolagus cuniculus, in Australia, based on morphological and molecular results. Two nymphs were collected from a single rabbit near the Kosciuszko National Park in New South Wales. Unlike reports of nymphs from domestic animals, these nymphs were not encapsulated, despite having the morphological features of infective nymphs. The possibility of different development pathways in lagomorphs is discussed. Examination of feral deer for L. serrata was unsuccessful and potential reasons for a lack of infection in these animals are postulated. Our results reiterate the need for a combined morphological and molecular approach to the identification of L. serrata. Further sampling of a range of feral and native animals is required to determine the true range of intermediate hosts and their relative importance in the transmission of L. serrata in Australia.
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References
Anon (2011) Feral deer. Australian Government, Canberra Retrieved from https://www.environment.gov.au/system/files/resources/c6679b32-5f03-4839-aa57-9c5723153b0f/files/fs-feral-deer.pdf. Accessed 29 January 2020
Banaja AA (1983) Scanning electron microscopy examination of larval Linguatula serrata Frölich (Linguatulidae: Pentastomida). Z Parasitenkd 69:271–277
Bentley A (1998) An introduction to the deer of Australia, with special reference to Victoria, Rev. edn. Australian Deer Research Foundation, Melbourne
Coman BJ (1973) The diet of red foxes, Vulpes vulpes L., in Victoria. Aust J Zool 21:391–401
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772
Davis NE, Bennett A, Forsyth DM, Bowman DMJS, Lefroy EC, Wood SW, Woolnough AP, West P, Hampton JO, Johnson CN (2016) A systematic review of the impacts and management of introduced deer (family Cervidae) in Australia. Wildl Res 42:515–532. https://doi.org/10.1071/WR16148
Diakou A, Sokos C, Papadopoulos E (2014) Endoparasites found in European brown hares (Lepus europaeus) hunted in Macedonia, Greece. Helminthol 51:345–351. https://doi.org/10.2478/s11687-014-0251-6
Doherty TS, Davis NE, Dickman CR, Forsyth DM, Letnic M, Nimmo DG, Palmer R, Ritchie EG, Benshemesh J, Edwards G, Lawrence J, Lumsden L, Pascoe C, Sharp A, Stokeld D, Myers C, Story G, Story P, Triggs B, Venosta M, Wysong M, Newsome TM (2019) Continental patterns in the diet of a top predator: Australia’s dingo. Mammal Rev 49:31–44. https://doi.org/10.1111/mam.12139
Fard SN, Ghalekhani N, Kheirandish R, Fathu S, Asl EN (2012) The prevalence of Linguatula serrata nymphs in camels slaughtered in Mashhad slaughterhouse, northeast Iran. Asian Pac J Trop Biomed 2:885–888. https://doi.org/10.1016/S2221-1691(12)60247-0
Fenner F (2010) Deliberate introduction of the European rabbit, Oryctolagus cuniculus, into Australia. Rev Sci Tech 29:103–111. https://doi.org/10.20506/rst.29.1.1964
Forsyth DM, Woodford L, Moloney PD, Hampton JO, Woolnough AP, Tucker M (2014) How does a carnivore guild utilise a substantial but unpredictable anthropogenic food source? Scavenging on hunter-shot ungulate carcasses by wild dogs/dingoes, red foxes and feral cats in South-Eastern Australia revealed by camera traps. PLOSOne. 9:e97937. https://doi.org/10.1371/journal.pone.0097937
Forsyth DM, Latham ADM, Davis NE, Caley P, Letnic M, Moloney PD, Woodford LP, Woolnough AP (2019) Interactions between dingoes and introduced wild ungulates: concepts, evidence and knowledge gaps. Aust Mammal 41:12–26. https://doi.org/10.1071/AM17042
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. Parasitol Res 112:3517–3525. https://doi.org/10.1007/s00436-013-3534-9
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98 citeulike-article-id:691774
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
McCully RM, Basson PA, van Niekirk JW, Bigalke RD (1966) Observations on Besnoitia cysts in the cardio-vascular system of some wild antelopes and domestic cattle. Onderstepoort J Vet 33:245–276
Palmer RA (1995) Diet of the red fox (Vulpes vulpes) in south-western Queensland. Rangel J 17:99–108
Pullar EM (1936) A note on the occurrence of Linguatula serrata (Frochlich, 1789) in Australia. Aust Vet J:61–64
Rambaut A (2014) FigTree v1.4.2, a graphical viewer of phylogenetic trees. Retrieved from http://tree.bio.ed.ac.uk/software/figtree/
Rezaei H, Ashrafihelan J, Nematollahi A, Mostafavi E (2012) The prevalence of Linguatula serrata nymphs in goats slaughtered in Tabriz, Iran. J Parasit Dis 36:200–202
Rezaei F, Tavassoli M, Hashemnia M, Naem S, Gholizadeh M (2016) Some morphological data on various stages of Linguatula serrata. Istanbul Univ Vet Fak Derg 42:38–46. https://doi.org/10.16988/iuvfd.2016.48454
Riley J (1986) The biology of pentastomids. Adv Parasitol 25:45–128
Riley J, Spratt DM, Presidente PJA (1985) Pentastomids (Arthropoda) parasitic in Australian reptiles and mammals. Aust J Zool 33:39–53
Ronquist F, Huelsenbeck J (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Shamsi S, McSpadden K, Baker S, Jenkins D (2017) Occurrence of tongue worm, Linguatula cf. seratta (Pentastomida: Linguatilidae) in wild canids and livestock in south-eastern Australia. Int J Parasitol Parasites Wildl 6:271–277. https://doi.org/10.1016/j.ijppaw.2017.08.008
Shamsi S, Barton DP, Zhu X, Jenkins DJ (2020) Characterisation of the tongue worm, Linguatula serrata (Pentastomida: Linguatulidae), in Australia. Int J Parasitol Parasites Wildl. https://doi.org/10.1016/j.ijppaw.2020.01.010
Tavassoli M, Hobbenaghi R, Kargozari A, Rezaei H (2018) Incidence of Linguatula serrata nymphs and pathological lesions of mesenteric lymph nodes in cattle from Urmia, Iran. Bulg J Vet Med 21:206–211. https://doi.org/10.15547/bjvm.1040
Acknowledgments
The authors are indebted to the various people who provided the rabbit and deer carcasses examined in this study. The authors are also grateful to Dr. David Spratt (CSIRO) for advice and for sharing his data regarding infections with L. serrata nymphs in mammals in the region. We would also like to thank Dr. Malcolm Bryant (QM) and Dr. Andrea Crowther (SAM) for the loan of specimens for comparison with specimens collected in this study; and especially Dr. Bryant for allowing the dissection of one of the specimens. In addition, AB would like to thank Craig Poynter and Gail Fuller (SPAN CSU) for the production of the map and Ashleigh Van Oosterum (NaLSH CSU) for assistance with the SEM.
Funding
This study was partially funded by a School of Animal and Veterinary Sciences (Charles Sturt University) Honours operating fund awarded to AB, a Graham Centre for Agricultural Innovation grant awarded to DJ, and a Charles Sturt University Research Fellowship awarded to SS.
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Diane P. Barton: processing and identification of parasite specimens, manuscript preparation.
Ashleigh Baker: dissection of animals, collection of parasites, parasite examination, scanning electron microscopy, manuscript preparation.
Megan Porter: dissection of animals, collection of parasites.
Xiaocheng Zhu: molecular analyses, preparation of manuscript.
David J Jenkins: funding of project, organization of supply of animals, dissection of animals, Animal Ethics applications.
Shokoofeh Shamsi: funding of project, study design, contribution to data analyses, preparation of manuscript.
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The authors declare that they have no competing interests.
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Animal collection was conducted under the following permits provided by the NSW National Parks and Wildlife Services (SL102219) and Australian Capital Territory Parks and Conservation Services (LT20192). The project was conducted under approval by the Charles Sturt University Animal Ethics Committee (A19001).
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Barton, D.P., Baker, A., Porter, M. et al. Verification of rabbits as intermediate hosts for Linguatula serrata (Pentastomida) in Australia. Parasitol Res 119, 1553–1562 (2020). https://doi.org/10.1007/s00436-020-06670-y
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DOI: https://doi.org/10.1007/s00436-020-06670-y