Abstract
Filarioid nematodes (Nematoda: Filarioidea) parasitic in Australasian monotremes, marsupials and murid rodents are described from three genera, Breinlia (Breinlia), Pelecitus and Sprattia. New host and geographic records are presented for 24 previously described species from these genera, a second subgenus, Breinlia (Johnstonema) and an additional three genera, Cercopithifilaria, Monanema and Pelecitus. Nine species are described as new, B. (B.) beveridgei sp. nov. from the peritoneal cavity of Macropus parryi Bennett, B. (B.) bigenera sp. nov. from the peritoneal and pleural cavities of Aepyprymnus rufescens (Gray), Onychogalea fraenata (Gould), O. unguifera (Gould) and possibly Antechinus swainsonii (Waterhouse), B. (B.) dorcopsis sp. nov. from the peritoneal cavity of Dorcopsis hageni Heller and D. luctuosa (D’Albertis), B. (B.) melomyos sp. nov. from the peritoneal cavity of Melomys cf. burtoni, B. (B.) oweni sp. nov. from the peritoneal cavity of Dactylopsila trivirgata Gray, B. (B.) presidentei sp. nov. from the peritoneal cavity of Mesembriomys gouldii (Gray), M. macrurus (Peters) and the pleural and peritoneal cavities of Conilurus penicillatus (Gould), B. (B.) tricondylus sp. nov. from the peritoneal cavity of Macropus rufogriseus banksianus (Quoy & Gaimard), B. (B.) zyzomyos sp. nov. from the peritoneal cavity of Zyzomys woodwardi (Thomas) and Z. argurus (Thomas), and Sprattia spearei sp. nov. from the lung (probably blood vessels) of Isoodon macrourus (Gould) . The female of B. (J.) woerlei from the pulmonary artery, right ventricle and lung cysts of Petrogale brachyotis (Gould) is described for the first time. Breinlia (J.) andersoni Spratt & Varughese, 1975 from the subcutaneous connective tissues of Macropus rufus (Desmarest), M. giganteus Shaw, M. robustus erubescens Sclater and Wallabia bicolor (Desmarest) is placed as a synonym of B. (J.) annulipapillata (Johnston & Mawson, 1938) from the subcutaneous connective tissues of M. dorsalis (Gray), O. fraenata and W. bicolor. In general, filarioids predominate in macropodoid hosts and in the north of Australia.
References
Anderson, R.C. & Bain, O. (1976) Keys to genera of the order Spirurida. Part 3. Diplotriaenoidea, Aproctoidea and Filarioidea. In: Anderson, R.C., Chabaud, A.G. & Willmott, S. (Eds.) CIH Keys to the Nematode Parasites of Vertebrates, No. 3. Commonwealth Agricultural Bureaux, Farnham Royal, England, pp. 59–116.
Bain, O., Baker, M. & Chabaud, A.G. (1982, issued 1983) Nouvelles données sur la lignée Dipetalonema (Filarioidea; Nematoda). Annales de Parasitologie humaine et comparée 57, 593–620.
Bain, O., Tibayrenc, M. & Mak, J.W. (1979) Deux espèces de Breinlia (Filarioidea) chez un Ecureuil en Malaisie. Bulletin du Muséum National d’Histoire naturelle, Paris, 4e sér., 1, 191–197.
Bain, O., Petit, G., Ratanaworabhan, N., Yenbutra, S. & Chabaud, A.G. (1981) Une nouvelle filaire d’Ecureuil en Thailand, Breinlia (B.) manningi n. sp. et son développement chez Aedes. Annales de Parasitologie humaine et comparée 56, 193–201.
Bartlett, C.M. & Greiner, E.C. (1986) A revision of Pelecitus Railliet & Henry, 1920 (Filarioidea, Dirofilariinae) and evidence for the “capture” by mammals of filarioids of birds. Bulletin du Muséum National d’Histoire naturelle, Paris, 4e sér., 8, 47–99.
Baylis, H.A. (1925) Notes on some Australian parasitic nematodes. Annals and Magazine of natural History 15, 112–115.
Baylis, H.A.(1934) On two filariid parasites of marsupials from Queensland. Annals and Magazine of natural History 13, 549–554
Begg, R., Walsh, B., Woerle, F. & King, S. (1983) Ecology of Melomys burtoni, the grassland melomys (Rodentia: Muridae) at Cobourg Penninsula, N.T. Australian Wildlife Research 10, 259–267.
Begg, M., Beveridge, I., Chilton, N.B., Johnson, P.M. & O’Callaghan, M.G. (1995) Parasites of the Proserpine rock wallaby, Petrogale persephone (Marsupialia: Macropodidae). Australian Mammalogy 18, 45–53.
Beveridge, I. & Arundel, J.H. (1979) Helminth parasites of Grey Kangaroos, Macropus giganteus Shaw and M. fuliginosus (Desmarest) in Eastern Australia. Australian Wildlife Research 6, 69–77.
Beveridge, I., Presidente, P.J.A. & Speare, R. (1985) Parasites and associated pathology of the swamp wallaby, Wallabia bicolor (Marsupialia). Journal of Wildlife Diseases 21, 377–385.
Beveridge, I., Speare, R. Johnson, P.M. & Spratt, D.M. (1992) Helminth parasite communities of macropodoid marsupials of the genera Hypsiprymnodon, Aepyprymnus, Thylogale, Onychogalea, Lagorchestes and Dendrolagus from Queensland. Wildlife Research 19, 359–376.
Beveridge, I., Spratt, D.M. & Johnson, P.M. (2010) Diversity and distribution of helminth parasites in macropodoid marsupials. Chap 21, In: Coulson, G. & Eldridge, M. (Eds.) Macropods: The Biology of Kangaroos, Wallabies and Rat-kangaroos. CSIRO Publishing, Collingwood, Australia, pp. 231–242.
Beveridge, I., Spratt, D.M., Close, R.L. Barker, S.C. & Sharman, G.B. (1989) Helminth parasites of rock–wallabies, Petrogale spp. (Marsupialia), from Queensland. Australian Wildlife Research 16, 273–287.
Bianco, A.E. & Muller, R.L. (1977) A hard tick as vector of a new rodent filaria. Transactions of the Royal Society of Tropical medicine and Hygiene 71, 383.
Bianco, A.E., Muller, R. & Nelson, G.S. (1983) Biology of Monanema globulosa , a rodent filaria with skin-dwelling microfilariae. Journal of Helminthology 57, 259–278.
Bolliger, A. (1951) Sheathed microfilaria in the common phalanger (Trichosurus vulpecula). Australian Journal of Science 14, 22–23.
Boulenger, M.A. (1928) Report on a collection of parasitic nematodes mainly from Egypt. Part V. Filarioidea. Parasitology 20, 32–55.
Breinl, A. (1913) Nematodes observed in North Queensland. Report of the Australian Institute of tropical Medicine for 1911, pp. 39–48.
Chabaud, A.G. & Bain, O. (1976) La lignée Dipetalonema. Nouvel essai de classification. Annales de Parasitologie humaine et comparée 51, 365–397.
Chilton, N.B., Gasser, R.B. & 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.
Chilton, N.B., Andrews, R.H. & Beveridge, I. (1996) Genetic evidence for a complex of species within Rugopharynx australis (Mönnig, 1926) (Nematoda: Strongyloidea) from macropodid marsupials. Systematic Parasitology 34, 125–133.
Chilton, N.N., Huby-Chilton, F., Johnson, P.M., Beveridge, I. & Gasser R.B. (2009) Genetic variation within species of the nematode genus Cloacina (Stongyloidea: Cloacininae) parasitic in the stomachs of rock wallabies, Petrogale spp. (Marsupialia: Macropodidae) in Queensland. Australian Journal of Zoology 57, 1–10.
Chowattukunnel, J.T. & Esslinger, J.H. (1979) A new species of Breinlia (Breinlia) (Nematoda: Filarioidea) from the south Indian flying squirrel, Petaurista philippensis (Eliot). Journal of Parasitology 65, 375–378.
Eberhard, M.L. (1980) Dipetalonema (Cercopithifilaria) kenyensis subgen. et sp. n. (Nematoda: Filarioidea) from African Baboons, Papio anubis. Journal of Parasitology 66, 551–554.
Eisig, H. (1869) Beschreibung einer Filaria aus Halmaturus. Zeitschrift für wissenschaftliche Zoologie 20, 99–102.
Flannery, T. (1995) Mammals of New Guinea. Reed Books: Sydney, 439 pp.
Godthelp, H. (2001) The Australian rodent fauna, flotillas, flotsam or just fleet footed? In: Metcalfe, I., Smith, J.B.M., Morwood, M. & Davidson, I. (Eds.), Faunal and Floral Migrations and Evolution in SE Asia–Australasia. A.A. Balkema Publishers, Lisse, pp. 319–322.
Hall, R. (1998) The plate tectonics of SE Asia and the distribution of land and sea. In: Hall, R. & Holloway, J.D. (Eds.) Biogeography and Geological Evolution of SE Asia, Leiden: Backhuys, pp. 99–131,.
Ho, B.C., Singh, M. & Lim, B.L. (1973) Observations on the development of a new filaria (Breinlia booliati, Singh and Ho, 1973) of a rat Rattus sabanus in the mosquito Aedes togoi. Journal of Helminthology 47, 135–140.
Johnston, T.H. (1909) The Entozoa of Monotremata and Australian Marsupialia. No. i. Proceedings of the Linnean Society of New South Wales, 34, 514–523.
Johnston, T.H. & Mawson, P.M. (1938a) An account of some filarial parasites of Australian marsupials. Transactions of the Royal Society of South Australia, 62, 107–121.
Johnston, T.H. & Mawson, P.M. (1938b) Some nematodes from Australian marsupials. Records of the South Australian Museum, 6, 187–199.
Johnston, T.H. & Mawson, P.M. (1939a) Strongyle nematodes from Queensland marsupials. Transactions of the Royal Society of South Australia, 63, 121–148.
Johnston, T.H. & Mawson, P.M. (1939b) Sundry nematodes from eastern Australian marsupials. Transactions of the Royal Society of South Australia 63, 204–209.
Johnston, T.H. & Mawson, P.M. (1940) New and known nematodes from Australian marsupials. Transactions of the Royal Society of South Australia 65, 468–476.
Jones, A. & Anderson, T.J.C. (1990) Helminths of rodents and marsupials from Papua New Guinea, with the description of two new species, Echinostoma echymiperae n. sp. (Digenea: Echinostomatidae) and Vampirolepis peroryctis n. sp. (Cestoda: Hymenolepididae). Systematic Parasitology 15, 223–237.
Jones, A. & Anderson, T.J.C. (1996) Raillietina melomyos n. sp. (Cestoda, Davaineidae) from mosaic–tailed rats in Papua New Guinea. Systematic Parasitology 33, 73–76.
Kennett, J.P., Kellerr, G. & Srinivasan, M.S. (1985) Miocene planktonic foraminiferal biogeography and paleogeographic development of the Indo–Pacific region. Geological Society of America Memoir 163, 197–236.
Kerle, J.A. (1995) Grassland melomys Melomys burtoni (Ramsay, 1887). In: R. Strahan (Ed.). The Mammals of Australia. Reed Books, Sydney, pp. 632–634.
Knight, D.H. (1977) Heartworm heart disease. Advances in Veterinary Science and Comparative Medicine, 21, 107–149.
Ko, R.C. (1972) The transmission of Ackertia marmotae Webster, 1967 (Nematoda: Onchocercidae) of groundhogs (Marmota monax) by Ixodes cookei. Canadian Journal of Zoology 50, 437–450.
Leidy, J, (1875) On some parasitic worms. Proceedings of the Academy of Natural Sciences, Philadelphia 27, 17–18.
Lim, B.L., Mak, J.W. & Nalim, S. (1978) New hosts of Breinlia booliati with observations on its distribution in Southeast Asia. Southeast Asian Journal of Tropical Medicine and Public Health 9, 526–528.
Lim, B.L., Mak, J.W., Singh, M., Ho, B.C. & Yap, E.H. (1975) Distribution and ecological consideration of Breinlia booliati infecting wild rodents in Malaysia. Southeast Asian Journal of Tropical Medicine and Public Health 6, 241–246.
Lindenmayer, D.B., Dubach, J. & Viggers, K.L. (2002) Geographic dimorphism in the mountain brushtail possum (Trichosurus caninus) – the case for a new species. Australian Journal of Zoology 50, 369–393.
Linstow, O. von (1897) Zur Systematic der Nematoden nebst Beschreibung neuer Arten. Archiv für mikroskopische Anatomie und Entwicklungsmechanik 49, 608–622.
Linstow, O. von (1898) Nemathelminthen von Herrn Richard Semon in Australien gesammelt. Denkschriften der Medizinisch-naturwissen-schaftlichen Gesellschaft zu Jena 8, 467–472.
Linstow, O. von (1905) Helminthologische Beobachtungen. Archiv für mikroskopische Anatomie und Entwicklungsmechanik 66, 355–366.
Mackerras, M.J. (1954) Two new species of Dipetalonema (Nematoda: Filarioidea) from Australian marsupials. Proceedings of the Royal Society of Queensland 64, 51–57.
Mackerras, M.J. (1962) Filarial parasites (Nematoda: Filarioidea) of Australian animals. Australian Journal of Zoology 10, 400–457.
Mak, J.W. & Lim, B.L. (1974) New host of Breinlia booliati in wild rats from Sarawak with further observations on its morphology. Southeast Asian Journal of Tropical Medicine and Public Health 5, 22–30.
Miyata, A. & Tsukamoto, M. (1975) Blood parasites from small mammals in Palawan Islands, the Philippines. Tropical Medicine 16, 113–130.
Oakwood, M. & Spratt, D.M. (2000) Parasites of the northern quoll, Dasyurus hallucatus (Marsupialia: Dasyuridae) in tropical savanna, Northern Territory. Australian Journal of Zoology 48, 79–90.
Obendorf, D.L. (1979) The helminth parasites of Rattus fuscipes (Waterhouse) from Victoria, including description of two new nematode species. Australian Journal of Zoology, 27, 867–879.
Obendorf, D., Spratt, D., Beveridge, I., Presidente, P. & Coman, B. (1998) Parasites and diseases in Australian brushtail possums, Trichosurus spp. In: R. Lynch (Ed.) Biological Control of Possums. The Royal Society of New Zealand, Miscellaneous series 45, Wellington, pp. 6–9.
Petit, G., Bain, O., Carrat, C. & De Marval, F. (1988) Développement de la filaire Monanema martini dans l’épiderme des tiques Ixodidae. Annales de Parasitologie humaine et comparée 63, 54–63.
Petter, A.J. (1958) Filaria sergenti Mathis et Léger, 1909, parasite d’un nycticèbe (Nyticebus tardigradus Link), appartient au genre Breinlia Yorke et Maplestone, 1926. Bulletin de la Société Zoologique de France 83, 423–429.
Portas, T.J., Spratt, D.M. & Rose, K.A. (2005) Microfilaraemia associated with Pelecitus roemeri in a western grey kangaroo (Macropus fuliginosus). Australian Veterinary Journal 83, 353–354.
Presidente, P.J.A. (1984) Parasites and diseases of brushtail possums (Trichosurus spp.): occurrence and significance. In Smith, A.P. & Hume, I.D. (Eds.) Possums & Gliders, Australian Mammal Society, Sydney, pp. 171–190.
Presidente, P.J.A., Barnett, J.L., How, R.A. & Humphreys, W.F. (1982) Effects of habitat, host sex and age on the parasites of Trichosurus caninus (Marsupialia: Phalangeridae) in north–eastern New South Wales. Australian Journal of Zoology, 30, 33–47.
Purnomo, & Bangs, M.J. (1996) Breinlia tinjili sp. n. (Filarioidea: Onchocercidae), from the Malaysian field rat, Rattus tiomanicus, on Tinjil Island, West Java, Indonesia. Journal of Helminthology 63, 93–97.
Railliet, A. & Henry, A. (1910) Les onchocerques, nematodes parasites du tissue conjonctif. Comptes rendu de la Société de Biologie 68, 248–251.
Ramachandran, C.P. & Dunn, F.L. (1968) The development of Breinlia sergenti (Dipetalonematidae) in Aedes mosquitoes. Annals of Tropical Medicine and Parasitology , 62, 441–454.
Robins , J.H., McLenachan, P.A., Phillips, M.J., McComish, B.J., Matisoo-Smiths, E. & Ross, H.A. (2010) Evolutionary relationships and divergence times among the native rats of Australia. BMC Evolutionary Biology 10, 375–428.
Rowe, K.C., Reno, M.L., Richmond, D.M.,Adkins, R.M. & Steppan, S.J. (2008) Pliocene colonization and adaptive radiations in Australia and New Guinea (Sahul): Multilocus systematics of the old endemic rodents (Muroidea: Murinae). Molecular Phylogenetics and Evolution 47, 84–101.
Rowe, K.C., Aplin, K.P., Baverstock, P.R. & Mortiz, C. (2011) Recent and rapid speciation with limited morphological disparity in the genus Rattus. Systematic Biology DOI:10.1093/sysbio/syq092, Jan 14, 2011.
Singh, M. & Ho, B.C. (1973) Breinlia booliati sp. n. (Filarioidea: Onchocercidae), a filaria of the Malayan forest rat, Rattus sabanus (Thos.). Journal of Helminthology 47, 127–133.
Smales, L.R. (1997) A review of the helminth parasites of Australian rodents. Australian Journal of Zoology 45, 505–521.
Smales, L.R. (2005) Helminth parasites of the grassland melomys (Muridae: Hydromyinae) from Australia and Papua New Guinea. Australian Journal of Zoology 53, 369–374.
Smales, L.R. (2008) Three new species of Heligmonellidae (Nematoda: Trichostrongyloidea) from Melomys, Paramelomys and Uromys (Rodentia: Muridae) from Papua, Indonesia and Papua New Guinea. Comparative Parasitology 75, 52–60.
Smales, L.R. (2009) Helminths of Melomys rufescens and Melomys spp. (Muridae: Hydromyinae) from Papua New Guinea with the descriptions of a new genus and five new species in the Heligmonellidae (Nematoda: Trichostrongyloidea). The Raffles Bulletin of Zoology 57, 5–15.
Smales, L.R. & Spratt, D.M. (2008) Helminth assemblages of Uromys spp. (Muridae: Hydromyinae) from Australia, Papua New Guinea and Papua Indonesia, and comparison with assemblages in Melomys spp. in Australia. Australian Journal of Zoology 56, 85–94.
Smales, L.R., Heinrich, B. & McKillup, S.C. (2004) The helminth parasites of Melomys cervinipes (Rodentia: Muridae: Hydromyinae). Australian Journal of Zoology 52, 65–80.
Solomon, G.S. (1933) A note on a new species of Breinlia (Filariidae), from a tree kangaroo. Journal of Helminthology 11, 101–104
Spratt, D.M. (1972a) Aspects of the life history of Dirofilaria roemeri in naturally and experimentally infected kangaroos and wallabies. International Journal for Parasitology 2, 139–156.
Spratt, D.M. (1972b) Natural occurrence, histopathology and developmental stages of Dirofilaria roemeri in the intermediate host. International Journal for Parasitology 2, 201–208.
Spratt, D.M. (1974a) Distribution of third–stage Dirofilaria roemeri in the tissues of Tabanidae. International Journal for Parasitology 4, 477–480.
Spratt, D.M. (1974b) Comparative epidemiology of Dirofilaria roemeri infection in two regions of Queensland. International Journal for Parasitology 4, 481–488.
Spratt, D.M. (1975) Further studies of Dirofilaria roemeri (Nematoda: Filarioidea) in naturally and experimentally infected Macropodidae. International Journal for Parasitology 5, 561–564.
Spratt, D.M. (2008) Monanema australe sp. nov. (Nematoda: Onchocercidae) from the lungs and liver of native rodents in north Queensland. Transactions of the Royal Society of South Australia 132, 1–6.
Spratt, D.M. & Haycock, P. (1988) Aspects of the life history of Cercopithifilaria johnstoni (Nematoda: Filarioidea). International Journal for Parasitology 18, 1087–1092.
Spratt, D.M. & Hobbs, R.P. (2003) Breinlia (Breinlia) ventricola sp.. nov., a nematode parasite from the heart of the red kangaroo, Macropus rufus, in Western Australia. Transactions of the Royal Society of South Australia, 128, 67–71.
Spratt, D.M. & Varughese, G. (1975) A taxonomic revision of filarioid nematodes from Australian marsupials. Australian Journal of Zoology, Supplementary Series No. 35, 1–99.
Spratt, D.M., Beveridge I., & Walter, E.L. (1991) A catalogue of Australasian monotremes and marsupials and their recorded helminth parasites, Records of the the South Australian Museum Monograph Series No. 1: 1–105.
Tucker, M.S., Price, D.L., Kwa, B.H. & DeBaldo, A.C. (2003) Observations of Breinlia booliati in a new host, Rattus rattus jalorensis, from Kuantan, State of Pahang, Malaysia. Journal of Parasitology 89, 1220–1226.
Van Dyck, S. & Strahan, R. (2008) The mammals of Australia (third edition). Reed New Holland: Sydney, 886 pp.
Viggers, K.L. (1996) Assessment of health, condition and the effects of parasites in the mountain brushtail possum. PhD. Thesis, Australian National University.
Viggers, K.L. & Spratt, D.M. (1995) The parasites recorded from Trichosurus species (Marsupialia: Phalangeridae). Wildlife Research 22, 311–332.
Virboonchai, S., Guptavanij, P., Sucharit, S. & Harinasuta, C. (1974) Breinlia ratti in natural host (Rattus jalorensis) and experimental hosts. Southeast Asian Journal of tropical Medicine and public Health 45, 143.
Vuong, P.N., Spratt, D., Wanji, S., Aimard, L. & Bain, O. (1993). Onchocerca–like lesions induced by the filarioid nematode Cercopithifilaria johnstoni, in its natural hosts and in the laboratory rat. Annales de Parasitologie humaine et comparée, 68, 176–181.
Wahid, S. (1962) On a new species of Breinlia (Nematode: Filarioidea) from Macropus brachyurus. Journal of Helminthology 36, 207–210.
Walker, J.C. & McMillan, B. (1974) Breinlia mackerrasae n. sp. (Nematoda: Filarioidea) from the peramelid marsupial, Isoodon macrourus, with a note on Breinlia sp. from the “mumut” Peramelidae. Journal of Helminthology 48, 39–45.
Watts, C.H.S. & Aslin,. H.J. (1981) The Rodents of Australia. Angus & Robertson, Melbourne, 321 pp.
Watts, C.H.S. & Baverstock, P.R. (1994a) Evolution in New Guinean Muridae (Rodentia) assessed by microcompliment fixation of albumin. Australian Journal of Zoology 42, 295–306.
Watts, C.H.S. & Baverstock, P.R. (1994b) Evolution in some South–east Asian Murinae (Rodentia), as assessed my microcomplement fixation of albumin, and their relationship to Australian murines. Australian Journal of Zoology 42, 711–722.
Watts, C.H.S. & Baverstock, P.R. (1995) Evolution in the Murinae (Rodentia) assessed by microcomplement fixation of albumin. Australian Journal of Zoology 43, 105–118.
Watts, C.H.S., Bavertsock, P.A., Birrell, J. & Kreig, M. (1992) Phylogeny of the Australian rodents (Muridae): a molecular approach using microcomplement fixation of albumin. Australian Journal of Zoology 40, 81–90.
Yamaguti, S. “Systema Helminthum” Vol. III. The Nematodes of Vertebrates. Interscience Publishers, New York, 1261 pp.
Yeh, Liang-Sheng (1957) On a filarial parasite Deraiophoronema freitaslenti n. sp. from the giant anteater, Myrmecophagus tridactyla from British Guiana, and a proposed reclassification of Dipetalonema and related genera. Parasitology 196–205.
Yen, P.K.F. (1983) Filariasis in the Australian marsupial, Setonix brachyurus (quokka). PhD Thesis. Department of Microbiology, University of Western Australia, Nedlands.
Yorke, W. & Maplestone, P.A. (1926) The Nematode Parasites of Vertebrates. J. & A. Churchill Ltd. London, 536 pp.
Zaman, V. & Chellapah, W.T. (1968) Studies on vector susceptibility and larval morphology of a Filaria of the slow loris, Nycticebus coucang. Annals of Tropical Medicine and Parasitology 62, 450–454.