Physalopterine nematodes in Australian reptiles: interactions and patterns of infection
Hugh I. Jones
+ Author Affiliations
- Author Affiliations
Microbiology and Immunology, M502, School of Pathology and Laboratory Medicine, University of Western Australia, Nedlands, WA 6009, Australia. Email: hugh.jones@uwa.edu.au
Australian Journal of Zoology 62(2) 180-194 https://doi.org/10.1071/ZO13033
Submitted: 27 April 2013 Accepted: 31 March 2014 Published: 21 May 2014
Abstract
Spirurid nematodes (family Physalopteridae) are widespread as adults or as encysted larvae in many species of Australian reptiles. Fifteen species of physalopterine nematodes (subfamily Physalopterinae) in the genera Kreisiella, Abbreviata and Skrjabinoptera infect more than 40 species of reptile in the five families Agamidae, Varanidae, Gekkonidae, Scincidae and Elapidae. Four species of nematode are host-species specific, six are host-family specific to varanid lizards, and three to agamid lizards. Larger species of reptile support a higher prevalence and abundance of nematodes, and often support multiple infections with more than one species, with the potential for interspecific competition. Geographic distribution of nematodes is partially limited by host distribution, and by climatic factors, mainly precipitation and temperature. There are strong positive and negative associations between several pairs of nematodes. Two species of nematode with the most pronounced muscular development at the anterior end, Abbreviata tumidocapitis and Abbreviata glebopalmae, only occur concurrently, and in low numbers, with species of nematode without these morphological features, suggesting differences in feeding in the hosts’ stomachs. A combination of host specificity, geographic distribution and habitat, climatic factors and feeding organ morphology are factors that probably reduce the potential for interspecific competition. There is no evidence that concurrent infections affect either prevalence or abundance of nematodes, or cause discernible pathological changes to their hosts.
References
Aho, J. M. (1990). Helminth communities of amphibians and reptiles: comparative approaches to understanding patterns and processes. In ‘Parasite Communities: Patterns and Processes’. (Eds G. Esch, A Bush and J. Aho.) pp. 157–195. (Chapman and Hall: London and New York.)Anderson, R. C. (2000). ‘Nematode Parasites of Vertebrates.’ 2nd edn. (CABI Publishing: Wallingford, UK.)
Ast, J. C. (2001). Mitochondrial DNA evidence and evolution in Varanoidea (Squamata). Cladistics 17, 211–226.
| Mitochondrial DNA evidence and evolution in Varanoidea (Squamata).Crossref | GoogleScholarGoogle Scholar |
Baverstock, P. R., King, D., King, M., Birrell, J., and Krieg, M. (1993). The evolution of species of the Varanidae: microcomplement fixation analysis of serum albumins. Australian Journal of Zoology 41, 621–638.
| The evolution of species of the Varanidae: microcomplement fixation analysis of serum albumins.Crossref | GoogleScholarGoogle Scholar |
Baylis, H. A. (1924). A new species of Physaloptera (Nematoda) from an Australian lizard. Annals & Magazine of Natural History 13, 309–311.
Bush, A. O., Lafferty, K. D., and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.
| Parasitology meets ecology on its own terms: Margolis et al. revisited.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2svht1OmsA%3D%3D&md5=db67b8832bb604e6e07d120c25b39539CAS | 9267395PubMed |
Chabaud, A. G. (1956). Essai de révision des physaloptères parasites de reptiles. Annales de Parasitologie Humaine et Comparee 31, 29–52.
| 1:STN:280:DyaG28%2FptlWgsA%3D%3D&md5=519290d08bcca5935243fd99def31136CAS | 13340427PubMed |
Chabaud, A. G. (1975). ‘CIH Keys to the nematode parasites of vertebrates. No. 3. Keys to the order Spirurida. Part 1. Camallanoidea, Dracunculoidea, Gnathostomatoidea, Physalopteroidea, Rictularioidea and Thelazioidea.’ (Eds R. C. Anderson, A. G. Chabaud and S. Willmott.) (Commonwealth Agricultural Bureaux, Farnham Royal: Buckinghamshire, UK.)
Christian, K. A., and Green, B. (1994). Seasonal energetic and water turnover of the frillneck lizard, Chlamydosaurus kingii, in the wet–dry tropics of Australia. Herpetologica 50, 274–281.
Christian, K. A., Griffiths, A. D., and Bedford, G. (1995). Physiological ecology of frill-neck lizards in a seasonal tropical environment. Oecologia 106, 49–56.
Cogger, H. G. (2014). ‘Reptiles and Amphibians of Australia.’ 7th edn. (CSIRO Publishing: Melbourne.)
Dewi, K., Jones, H. I., and Hamidy, A. (2008). The status of Tanqua anomala (von Linstow, 1904) (Nematoda: Gnathostomatoidea). Transactions of the Royal Society of South Australia 132, 7–13.
Fitch, A. J., Goodman, A. E., and Donnellan, S. C. (2006). A molecular phylogeny of the Australian monitor lizards (Squamata: Varanidae) inferred from mitochondrial DNA sequences. Australian Journal of Zoology 54, 253–269.
| A molecular phylogeny of the Australian monitor lizards (Squamata: Varanidae) inferred from mitochondrial DNA sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotV2ru7Y%3D&md5=42071d55225d331747eaf50d6af5853dCAS |
Gems, D. (2000). Longevity and ageing in parasitic and free-living nematodes. Biogerontology 1, 289–307.
| Longevity and ageing in parasitic and free-living nematodes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3Mnmt1yhsw%3D%3D&md5=e471609cfaeeeda057a0c88db8e77305CAS | 11708211PubMed |
Goldberg, S. R., and Bursey, C. R. (2012). Intestinal helminths in nine species of endemic Australian lizards, Lophognathus longirostris (Agamidae), Heteronotia binoei and Lucasium stenodactylum (Gekkonidae), Ctenotus grandis, Ctenotus helenae, Cyclodomorphus branchialis, Egernia depressa, Eremiascincus richardsonii, Morethia butleri and Morethia lineoocellata (Scincidae), with a review of Australian lizard helminths. Comparative Parasitology 79, 247–268.
| Intestinal helminths in nine species of endemic Australian lizards, Lophognathus longirostris (Agamidae), Heteronotia binoei and Lucasium stenodactylum (Gekkonidae), Ctenotus grandis, Ctenotus helenae, Cyclodomorphus branchialis, Egernia depressa, Eremiascincus richardsonii, Morethia butleri and Morethia lineoocellata (Scincidae), with a review of Australian lizard helminths.Crossref | GoogleScholarGoogle Scholar |
Hatcher, M. J., and Dunn, A. M. (2011). ‘Parasites in Ecological Communities.’ (Cambridge University Press: Cambridge.)
Hay, M. (1972). The breeding of Physignathus lesueurii L. in captivity. Herpetofauna 5, 2–3.
Holmes, R., and Light, A. (1983). A serendipitous age estimation of a lizard, Tiliqua rugosa (Lacertilia: Scincidae). Western Australian Naturalist 15, 159–160.
Hugall, A. F., Foster, R., Hutchinson, M., and Lee, M. S. (2008). Phylogeny of Australasian agamid lizards based on nuclear and mitochondrial genes: implications for morphological evolution and biogeography. Biological Journal of the Linnean Society 93, 343–358.
| Phylogeny of Australasian agamid lizards based on nuclear and mitochondrial genes: implications for morphological evolution and biogeography.Crossref | GoogleScholarGoogle Scholar |
Irwin-Smith, V. (1922). Notes on nematodes in the genus Physaloptera. Part III. The Physaloptera of Australian lizards. Proceedings of the Linnean Society of New South Wales 46, 232–244.
James, C. D., Losos, J. B., and King, D. R. (1992). Reproductive biology and diets of goannas (Reptilia: Varanidae) from Australia. Journal of Herpetology 26, 128–136.
| Reproductive biology and diets of goannas (Reptilia: Varanidae) from Australia.Crossref | GoogleScholarGoogle Scholar |
Johnston, T. H., and Mawson, P. M. (1941). Some parasitic nematodes in the collection of the Australian Museum. Records of the Australian Museum 21, 9–16.
| Some parasitic nematodes in the collection of the Australian Museum.Crossref | GoogleScholarGoogle Scholar |
Johnston, T. H., and Mawson, P. M. (1942a). The Gallard collection of parasitic nematodes in the Australian Museum. Records of the Australian Museum 21, 110–115.
| The Gallard collection of parasitic nematodes in the Australian Museum.Crossref | GoogleScholarGoogle Scholar |
Johnston, T. H., and Mawson, P. M. (1942b). Some new and known Australian parasitic nematodes. Proceedings of the Linnean Society of New South Wales 67, 90–94.
Johnston, T. H., and Mawson, P. M. (1947). Some nematodes from Australian lizards. Transactions of the Royal Society of South Australia 71, 22–27.
Johnston, T. H., and Mawson, P. M. (1948). Some new records of nematodes from Australian snakes. Records of the South Australian Museum 9, 101–106.
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 |
Jones, H. I. (1978a). Abbreviata (Nematoda: Physalopteroidea) from Western Australian snakes. Australian Journal of Zoology 26, 789–807.
| Abbreviata (Nematoda: Physalopteroidea) from Western Australian snakes.Crossref | GoogleScholarGoogle Scholar |
Jones, H. I. (1978b). Gastrointestinal nematodes from aquatic Australian snakes. Memoirs of the Queensland Museum 118, 243–254.
Jones, H. I. (1979). Gastrointestinal nematodes, including three new species, from Australian and Papua New Guinean pythons. Proceedings of the Helminthological Society of Washington 46, 1–14.
Jones, H. I. (1980). Observations on nematodes from west and central Australian snakes. Australian Journal of Zoology 28, 423–433.
| Observations on nematodes from west and central Australian snakes.Crossref | GoogleScholarGoogle Scholar |
Jones, H. I. (1983a). Prevalence and intensity of Abbreviata Travassos (Nematoda: Physalopteridae) in the ridge-tailed monitor Varanus acanthurus Boulenger in northern Australia. Records of the Western Australian Museum 11, 1–9.
Jones, H. I. (1983b). Abbreviata (Nematoda: Physalopteridae) in lizards of the Varanus gouldii complex (Varanidae) in Western Australia. Australian Journal of Zoology 31, 285–298.
| Abbreviata (Nematoda: Physalopteridae) in lizards of the Varanus gouldii complex (Varanidae) in Western Australia.Crossref | GoogleScholarGoogle Scholar |
Jones, H. I. (1985a). Two new species of nematode (Spirurida: Physalopteridae) from Australian lizards (Reptilia: Scincidae: Gekkonidae). Journal of Natural History 19, 1231–1237.
| Two new species of nematode (Spirurida: Physalopteridae) from Australian lizards (Reptilia: Scincidae: Gekkonidae).Crossref | GoogleScholarGoogle Scholar |
Jones, H. I. (1985b). Gastrointestinal nematodes of the perentie, Varanus giganteus (Grey), in Western Australia, with description of a new species of Abbreviata Travassos (Nematoda: Physalopteridae). Records of the Western Australian Museum 12, 379–387.
Jones, H. I. (1986). Gastrointestinal nematodes in the lizard genus Pogona Storr, 1982 (Agamidae) in Western Australia. Australian Journal of Zoology 34, 689–705.
| Gastrointestinal nematodes in the lizard genus Pogona Storr, 1982 (Agamidae) in Western Australia.Crossref | GoogleScholarGoogle Scholar |
Jones, H. I. (1988). Nematodes from nine species of Varanus (Reptilia) from tropical Northern Australia, with particular reference to the genus Abbreviata (Physalopteridae). Australian Journal of Zoology 36, 691–708.
| Nematodes from nine species of Varanus (Reptilia) from tropical Northern Australia, with particular reference to the genus Abbreviata (Physalopteridae).Crossref | GoogleScholarGoogle Scholar |
Jones, H. I. (1992a). Gastrointestinal nematodes in the lizard genera Tiliqua and Cyclodomorphus (Scincidae) in Western Australia. Australian Journal of Zoology 40, 115–126.
| Gastrointestinal nematodes in the lizard genera Tiliqua and Cyclodomorphus (Scincidae) in Western Australia.Crossref | GoogleScholarGoogle Scholar |
Jones, H. I. (1992b). Gastrointestinal nematodes of Varanus caudolineatus (Reptilia: Varanidae) in Western Australia. Records of the Western Australian Museum 16, 109–112.
Jones, H. I. (1994). Gastrointestinal nematodes of the frillneck lizard, Chlamydosaurus kingii (Agamidae) with particular reference to Skrjabinoptera goldmanae (Spirurida: Physalopteridae). Australian Journal of Zoology 42, 371–377.
| Gastrointestinal nematodes of the frillneck lizard, Chlamydosaurus kingii (Agamidae) with particular reference to Skrjabinoptera goldmanae (Spirurida: Physalopteridae).Crossref | GoogleScholarGoogle Scholar |
Jones, H. I. (1995a). The functional anatomy of the anterior end of Skrjabinoptera goldmanae from Australian agamid lizards. Journal of Helminthology 69, 33–37.
| The functional anatomy of the anterior end of Skrjabinoptera goldmanae from Australian agamid lizards.Crossref | GoogleScholarGoogle Scholar |
Jones, H. I. (1995b). Gastric nematode communities in lizards from the Great Victoria Desert, and an hypothesis for their evolution. Australian Journal of Zoology 43, 141–164.
| Gastric nematode communities in lizards from the Great Victoria Desert, and an hypothesis for their evolution.Crossref | GoogleScholarGoogle Scholar |
Jones, H. I. (1995c). Pathology associated with physalopterid larvae (Nematoda: Spirurida) in the gastric tissues of Australian reptiles. Journal of Wildlife Diseases 31, 299–306.
| Pathology associated with physalopterid larvae (Nematoda: Spirurida) in the gastric tissues of Australian reptiles.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK287ntlGguw%3D%3D&md5=b83a002797fc17bf4c4144927434cfddCAS | 8592348PubMed |
Jones, H. I. (2003). Parasitic worms of reptiles from Tasmania and the islands of Bass Strait. Papers and Proceedings of the Royal Society of Tasmania 137, 7–12.
Jones, H. I. (2004). Gastric nematodes, including a new species of Abbreviata (Spirurida: Physalopteridae) from the mangrove monitor, Varanus indicus (Reptilia: Varanidae). Transactions of the Royal Society of South Australia 128, 53–59.
Jones, H. I. (2005). The gastrointestinal nematodes of Varanus rosenbergi (Reptilia: Varanidae) and the effects of habitat change in southern Australia, with particular reference to the genus Abbreviata (Physalopteroidea). Records of the Western Australian Museum 22, 259–263.
Jones, H. I. (2007a). Nematodes of the water dragon, Physignathus lesueurii (Reptilia: Agamidae) in Australia, with a description of Spinicauda fluviatica sp. nov. (Nematoda: Heterakoidea). Australian Journal of Zoology 55, 161–168.
| Nematodes of the water dragon, Physignathus lesueurii (Reptilia: Agamidae) in Australia, with a description of Spinicauda fluviatica sp. nov. (Nematoda: Heterakoidea).Crossref | GoogleScholarGoogle Scholar |
Jones, H. I. (2007b). Helminth parasites of the lace monitor, Varanus varius (Reptilia: Varanidae) in eastern Australia. Transactions of the Royal Society of South Australia 131, 162–168.
Jones, H. I. (2010). Dwarf monitor lizards (Varanidae: Varanus, Odatria s. gen) as definitive and paratenic hosts for physalopteran nematodes. Australian Journal of Zoology 58, 69–75.
| Dwarf monitor lizards (Varanidae: Varanus, Odatria s. gen) as definitive and paratenic hosts for physalopteran nematodes.Crossref | GoogleScholarGoogle Scholar |
Jones, H. I. (2013a). Gastrointestinal nematodes from three species of Australian leaf-tailed gecko (Reptilia: Saltuarius spp), with descriptions of new species of Skrjabinodon (Oxyuroidea: Pharyngodonidae) and Hedruris (Habronematoidea: Hedruridae). Comparative Parasitology 80, 47–59.
| Gastrointestinal nematodes from three species of Australian leaf-tailed gecko (Reptilia: Saltuarius spp), with descriptions of new species of Skrjabinodon (Oxyuroidea: Pharyngodonidae) and Hedruris (Habronematoidea: Hedruridae).Crossref | GoogleScholarGoogle Scholar |
Jones, H. I. (2013b). Gastrointestinal nematodes of the Australian leaf-tailed gecko Phyllurus platurus (Reptilia: Gekkonidae), with a redescription of Abbreviata bancrofti (Irwin-Smith, 1922), and observations on physalopterid larvae. Comparative Parasitology 80, 217–224.
| Gastrointestinal nematodes of the Australian leaf-tailed gecko Phyllurus platurus (Reptilia: Gekkonidae), with a redescription of Abbreviata bancrofti (Irwin-Smith, 1922), and observations on physalopterid larvae.Crossref | GoogleScholarGoogle Scholar |
Jones, H. I. (2013c). Gastric nematodes from the plains goanna, Varanus spenceri (Reptilia: Varanidae), from central Queensland. Memoirs of the Queensland Museum 56, 457–460.
Jones, H. I., and Watharow, S. (2010). Gastrointestinal helminths in two allopatric sibling species of swamp skink, Lissolepis coventryi and Lissolepis luctuosus (Reptilia: Scincidae), from south-eastern and south-western Australia, with descriptions of three new species of nematode. Comparative Parasitology 77, 37–51.
| Gastrointestinal helminths in two allopatric sibling species of swamp skink, Lissolepis coventryi and Lissolepis luctuosus (Reptilia: Scincidae), from south-eastern and south-western Australia, with descriptions of three new species of nematode.Crossref | GoogleScholarGoogle Scholar |
King, D. (2004). Varanus pilbarensis. In ‘Varanoid Lizards of the World’. (Eds E. R. Pianka, D. R. King and R. A. King.) pp. 430–433. (Indiana University Press: Bloomington and Indianapolis.)
King, D., and Green, B. (1999). ‘Goannas. The Biology of Varanid Lizards.’ (University of New South Wales Press: Sydney.)
King, C., Jones, H. I., and Tay, A. (2013). Arthropod intermediate hosts of Abbreviata antarctica (Nematoda: Physalopteridae) in Australia. The Journal of Parasitology 99, 708–711.
| Arthropod intermediate hosts of Abbreviata antarctica (Nematoda: Physalopteridae) in Australia.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3szjsV2gtg%3D%3D&md5=03b869714c9db5aac85d00366029b8e6CAS | 23360383PubMed |
Kreis, H. A. (1940). Beiträge zur Kenntnis parasitischer Nematoden. IX. Parasitische nematoden aus dem Naturhistorischen Museum Basel. Zentralblatt für Bakteriologie. Abt.1. Originale 145, 163–208.
Lant, B., and Storey, K. B. (2010). An overview of stress response and hypometabolic strategies in Caenorhabditis elegans. Conserved and contrasting signals with the mammalian system. International Journal of Biological Sciences 6, 9–50.
| An overview of stress response and hypometabolic strategies in Caenorhabditis elegans. Conserved and contrasting signals with the mammalian system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXntV2jtA%3D%3D&md5=d2e61c675fcd3218100ac0a5378052d0CAS | 20087441PubMed |
Mawson, P. M. (1970). Skrjabinoptera goldmanae n. sp. (Nematoda: Physalopteridae) from an Australian agamid lizard. Transactions of the Royal Society of South Australia 94, 223–225.
Paterson, S., and Viney, M. E. (2002). Host immune responses are necessary for density dependence in nematode infections. Parasitology 125, 283–292.
| Host immune responses are necessary for density dependence in nematode infections.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38vpslSktg%3D%3D&md5=4885ffe388fa3d58677ce3d58a60bfe4CAS | 12358425PubMed |
Pianka, E. R. (1970). Notes on the biology of Varanus gouldii. Western Australian Naturalist 11, 141–144.
Pianka, E. R. (1971). Notes on the biology of Varanus tristis. Western Australian Naturalist 11, 180–183.
Pianka, E. R. (1986). ‘Ecology and Natural History of Desert Lizards.’ (Princeton University Press: New Jersey.)
Pianka, E. R. (1994). Comparative ecology of Varanus in the Great Victoria Desert. Australian Journal of Ecology 19, 395–408.
| Comparative ecology of Varanus in the Great Victoria Desert.Crossref | GoogleScholarGoogle Scholar |
Pianka, E. R., and King, D. R. (2004). Introduction. In ‘Varanoid Lizards of the World’. (Eds E. R. Pianka, D. R. King, and R. A. King.) pp. 1–8. (Indiana University Press: Bloomington and Indianapolis.)
Quinnell, R. J., Medley, G. F., and Keymer, A. E. (1990). The regulation of gastrointestinal helminth populations. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 330, 191–201.
| The regulation of gastrointestinal helminth populations.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M7msVCjsA%3D%3D&md5=8ca369e6d4b39fe8d66bd66be2efb6a6CAS |
Shine, R. (1986). Food habits, habitats and reproductive biology of four sympatric species of varanid lizards in tropical Australia. Herpetologica 42, 346–360.
Shine, R., and Lambeck, R. (1989). Ecology of frillneck lizards, Chlamydosaurus kingii (Agamidae), in tropical Australia. Australian Wildlife Research 16, 491–500.
| Ecology of frillneck lizards, Chlamydosaurus kingii (Agamidae), in tropical Australia.Crossref | GoogleScholarGoogle Scholar |
Sprent, J. F. A. (1988). Ascaridoid nematodes of amphibians and reptiles: Ophidascaris Baylis, 1920. Systematic Parasitology 11, 165–213.
| Ascaridoid nematodes of amphibians and reptiles: Ophidascaris Baylis, 1920.Crossref | GoogleScholarGoogle Scholar |
Thomas, P. M. (1959). Some nematode parasites from Australian hosts. Transactions of the Royal Society of South Australia 82, 151–162.
Viney, M. E., Steer, M. D., and Wilkes, C. P. (2006). The reversibility of constraints on size and fecundity in the parasitic nematode Strongyloides ratti. Parasitology 133, 477–483.
| The reversibility of constraints on size and fecundity in the parasitic nematode Strongyloides ratti.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28rjsFGltA%3D%3D&md5=c183ba2b438705a6a00546e2751b94fdCAS | 16817996PubMed |
Watharow, S., and Jones, H. I. (2009). Gastric nematodes of snakes and lizards from the Victorian mallee. Herpetofauna 39, 21–27.
