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New species of Myxosporea from frogs and resurrection of the genus Cystodiscus Lutz, 1889 for species with myxospores in gallbladders of amphibians

Published online by Cambridge University Press:  19 January 2012

ASHLIE HARTIGAN ,
IVAN FIALA ,
IVA DYKOVÁ ,
KARRIE ROSE ,
DAVID N. PHALEN  and
JAN ŠLAPETA
ASHLIE HARTIGAN
Affiliation:
Faculty of Veterinary Science, University of Sydney, New South Wales 2006, Australia
IVAN FIALA
Affiliation:
Institute of Parasitology, Biology Centre, Academy of Sciences of the Czech Republic, České Budějovice, Czech Republic
IVA DYKOVÁ
Affiliation:
Institute of Parasitology, Biology Centre, Academy of Sciences of the Czech Republic, České Budějovice, Czech Republic
KARRIE ROSE
Affiliation:
Australian Registry of Wildlife Health, Taronga Conservation Society Australia, Mosman, New South Wales, Australia
DAVID N. PHALEN
Affiliation:
Faculty of Veterinary Science, University of Sydney, New South Wales 2006, Australia
JAN ŠLAPETA*
Affiliation:
Faculty of Veterinary Science, University of Sydney, New South Wales 2006, Australia
*
*Corresponding author: McMaster Building B14, Faculty of Veterinary Science, University of Sydney, New South Wales 2006, Australia. Tel: +61 2 9251 2025. Fax: +61 2 935 17348. E-mail: jan.slapeta@sydney.edu.au
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Summary

Two new myxosporean species in the gallbladders of frogs have recently spread across eastern Australia and cause disease. Cystodiscus axonis sp. n. and Cystodiscus australis sp. n. are species of Myxosporea (Myxozoa) identified from a range of Australian frogs and tadpoles including the introduced Cane toad (Rhinella marina). The new species are defined by their distinct genetic lineage, myxospore morphology and ultrastructure of the pre-sporogonic development. Spores of both species are produced in the gallbladder. Spores of C. axonis sp. n. possess distinct filiform polar appendages (FPA). The pre-sporogonic development of C. axonis sp. n. is within myelinated axons in the central nervous system of hosts, as well as bile ducts of tadpoles. Pre-sporogonic and sporogonic development of C. australis sp. n. is confined to tadpole bile ducts and myxospores of C. australis sp. n. are devoid of FPA. The genus Cystodiscus Lutz, 1889 introduced for Cystodiscus immersus Lutz, 1889 is emended to accompany myxosporean parasites affecting amphibians previously classified in the genus Myxidium sensu lato. A synopsis of described species within Cystodiscus is provided.

Keywords

Cystodiscus axonisCystodiscus australisnew speciesMyxidiumMyxosporeaamphibiansfrogstadpolesbrainliverdiseasephylogeny
Type
Research Article
Information
Parasitology , Volume 139 , Issue 4 , April 2012 , pp. 478 - 496
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Azevedo, C. and Matos, E. (1996). Light and electron microscopic study of a myxosporean, Tetrauronema desaequalis sp. n. (Family Tetrauronematidae), from an Amazonian fish. Journal of Parasitology 82, 288–291. doi: 10.2307/3284162.CrossRefGoogle Scholar
Bartošová, P., Fiala, I. and Hypša, V. (2009). Concatenated SSU and LSU rDNA data confirm the main evolutionary trends within myxosporeans (Myxozoa: Myxosporea) and provide an effective tool for their molecular phylogenetics. Molecular Phylogenetics and Evolution 53, 81–93. doi: 10.1016/j.ympev.2009.05.018.Google Scholar
Carini, A. (1932). Myxidium lindoyense n. sp., parasita da vesicula biliar de batrachios do Brasil. Revista de Biologia e Hygiene Sao Paolo 3, 83–84.Google Scholar
Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540–552.Google Scholar
Clark, J. G. (1982). Studies on the biology of Myxidium serotinum Kudo and Sprague, 1940 (Myxozoa), a parasite of amphibian invertebrates, Ph.D. thesis. Department of Biological Sciences, College of Arts and Sciences, University of Cincinnati, Cincinnati, USA.Google Scholar
Clark, J. G. and Shoemaker, J. (1973). Eurycea bislineata (Green) Two-lined salamander, a new host of Myxidium serotinum Kudo and Sprague 1940 (Myxosporidea, Myxidiidae). Journal of Protozoology 20, 365–366. doi: 10.1111/j.1550-7408.1973.tb00902.x.Google Scholar
Cordero, E. H. (1919). Nota sobre ‘Opalina antilliensis’ Metcalf, ciliado parasito de los batracios del Uruguay. Physis Seccion A los Oceanos y sus Organismos 4, 531–535.Google Scholar
de Leon, G. P. P. and Nadler, S. A. (2010). What we don't recognize can hurt us: a plea for awareness about cryptic species. Journal of Parasitology 96, 453–464. doi: 10.1645/Ge-2260.1.Google Scholar
Delvinquier, B. L. J. (1986). Myxidium immersum (Protozoa, Myxosporea) of the cane toad, Bufo marinus, in Australian anura, with a synopsis of the genus in amphibians. Australian Journal of Zoology 34, 843–853. doi: 10.1071/ZO9860843.Google Scholar
Delvinquier, B. L. J., Markus, M. B. and Passmore, N. I. (1992). Myxidium lesminteri sp. n. (Myxosporea, Myxidiidae) from the gallbladder of 3 Southern African anura. Systematic Parasitology 23, 25–30. doi: 10.1007/BF00008005.Google Scholar
Faivovich, J., Haddad, C. F. B., Garcia, P. C. A., Frost, D. R., Campbell, J. A. and Wheeler, W. C. (2005). Systematic review of the frog family hylidae, with special reference to hylinae: phylogenetic analysis and taxonomic revision. Bulletin of the American Museum of Natural History 294, 1–240. doi: 10.1206/0003-0090(2005)294[0001:SROTFF]2.0.CO;2.CrossRefGoogle Scholar
Fiala, I. (2006). The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. International Journal for Parasitology 36, 1521–1534. doi: 10.1016/j.ijpara.2006.06.016.CrossRefGoogle ScholarPubMed
Fiala, I. and Bartošová, P. (2010). History of myxozoan character evolution on the basis of rDNA and EF-2 data. Bmc Evolutionary Biology 10. doi: 22810.1186/1471-2148-10-228.CrossRefGoogle ScholarPubMed
Frost, D. R. (2011). Amphibian Species of the World: an Online Reference. Version 5.5 (31 January, 2011). Electronic Database accessible athttp://research.amnh.org/vz/herpetology/amphibia/, American Museum of Natural History, New York, USA.Google Scholar
Gray, M. E. (1993). A new species of Myxidium (Myxozoa: Myxidiidae) from the gall bladders of anuran amphibians from Peru. Transactions of the Kansas Academy of Science 96, 152–157. doi: 10.2307/3628327.CrossRefGoogle Scholar
Griffin, M. J., Wise, D. J. and Pote, L. M. (2009). Morphology and small-subunit ribosomal DNA sequence of Henneguya adiposa (Myxosporea) from Ictalurus punctatus (Siluriformes). Journal of Parasitology 95, 1076–1085. doi: 10.1645/ge-2012.1.Google Scholar
Hartigan, A., Fiala, I., Dyková, I., Jirků, M., Okimoto, B., Rose, K., Phalen, D. N. and Šlapeta, J. (2011). A suspected parasite spill-back of two novel Myxidium spp. (Myxosporea) causing disease in Australian endemic frogs found in the invasive Cane Toad. PloS ONE 6, e18871. doi: 10.1371/journal.pone.0018871.CrossRefGoogle ScholarPubMed
Hartigan, A., Phalen, D. N. and Šlapeta, J. (2010). Museum material reveals a frog parasite emergence after the invasion of the cane toad in Australia. Parasites & Vectors 3. doi: 10.1186/1756-3305-3-50.CrossRefGoogle ScholarPubMed
Jirků, M., Bolek, M. G., Whipps, C. M., Janovy, J., Kent, M. L. and Modrý, D. (2006). A new species of Myxidium (Myxosporea: Myxidiidae), from the western chorus frog, Pseudacris triseriata triseriata, and Blanchard's cricket frog, Acris crepitans blanchardi (Hylidae), from Eastern Nebraska: Morphology, phylogeny, and critical comments on amphibian Myxidium taxonomy. Journal of Parasitology 92, 611–619. doi: 10.1645/GE-728R.1.Google Scholar
Katoh, K., Kuma, K., Toh, H. and Miyata, T. (2005). MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research 33, 511–518. doi: 10.1093/nar/gki198.Google Scholar
Kudo, R. R. (1943). Further observations on the protozoan, Myxidium serotinum, inhabiting the gall bladder of North American Salientia. Journal of Morphology 72, 263–277.Google Scholar
Kudo, R. R. and Sprague, V. (1940). On Myxidium immersum Lutz and M. serotinum n. sp., two Myxosporidian parasites of Salientia of South and North America. Revista de Medicina Tropical Habana 6, 65–73.Google Scholar
Lom, J. (1987). Myxosporea a new look at long known parasites of fish. Parasitology Today 3, 327–332. doi: 10.1016/0169-4758(87)90115-3.Google Scholar
Lom, J. and Arthur, J. R. (1989). A guideline for the preparation of species descriptions in Myxosporea. Journal of Fish Diseases 12, 151–156.CrossRefGoogle Scholar
Lom, J. and Dyková, I. (1992). Protozoan Parasites of Fishes, Elsevier, New York, USA.Google Scholar
Lom, J. and Dyková, I. (2006). Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica 53, 1–36.Google Scholar
Lom, J., Feist, S. W., Dyková, I. and Kepr, T. (1989). Brain myxoboliasis of bullhead, Cottus gobio L., due to Myxobolus jiroveci sp. nov.: light and electronmicroscope observations. Journal of Fish Diseases 12, 15–27. doi: 10.1111/j.1365-2761.1989.tb01235.x.Google Scholar
Lom, J., Pavlásková, M. and Dyková, I. (1985). Notes on kidney-infecting species of the genus Sphaerospora Thélohan (Myxosporea), including a new species of Sphaerospora gobionis sp. nov., and on Myxosporean life cycle stages in the blood of some freshwater fish. Journal of Fish Diseases 8, 221–232. doi: 10.1111/j.1365-2761.1985.tb01217.x.Google Scholar
Lühe, M. (1899). Cystodiscus immersus Lutz. Verhandlungen der Deutschen Zoologischen Gesellschaft 9, 291–293.Google Scholar
Lutz, A. (1889). Üeber ein Myxosporidium aus der Gallenblase brasilianischer Batrachier. Centralblatt für Bakteriologie und Parasitenkunde 5, 84–88.Google Scholar
Mann, R. M., Hyne, R. V. and Choung, C. B. (2010). Hormonal induction of spermiation, courting behavior and spawning in the Southern bell frog, Litoria raniformis. Zoo Biology 29, 774–782. doi: 10.1002/zoo.20331.Google Scholar
Marquet, E. and Sobel, H. (1970). A protozoon in central nervous system of lungfish Polypterus enlicheri. Journal of Protozoology 17, 71. doi: 10.1111/j.1550-7408.1970.tb05160.x.CrossRefGoogle Scholar
McAllister, C. T. and Bursey, C. R. (2005). Endoparasites of the eastern narrowmouth toad, Gastrophryne carolinensis (Anura: Microhylidae), from northwestern Louisiana and northeastern Texas, USA. Comparative Parasitology 72, 124–128. doi: 10.1654/4149.CrossRefGoogle Scholar
McAllister, C. T., Bursey, C. R. and Trauth, S. E. (2008). New host and geographic distribution records for some endoparasites (Myxosporea, Trematoda, Cestoidea, Nematoda) of amphibians and reptiles from Arkansas and Texas, USA. Comparative Parasitology 75, 241–254. doi: 10.1654/4329.1.CrossRefGoogle Scholar
McAllister, C. T., Crawford, J. A. and Kuhns, A. R. (2009). Myxidium serotinum (Protista: Myxozoa) from a Jefferson salamander Ambystoma jeffersonianum, in Illinois. Texas Journal of Science 61, 61–64.Google Scholar
McAllister, C. T. and Freed, P. S. (1996). A new host and geographic record for Myxidium lesminteri (Protozoa: Myxosporea) from Tomopterna cryptotis (Amphibia: Ranidae), in Namibia, South-West Africa. Journal of the Helminthological Society of Washington 63, 123–124.Google Scholar
McAllister, C. T. and Trauth, S. E. (1995). New host records for Myxidium serotinum (Protozoa, Myxosporea) from North American amphibians. Journal of Parasitology 81, 485–488.Google Scholar
Sarkar, N. K. (1982). Myxosporidan Myxidium haldari sp. n. (Myxozoa, Myxidiidae) from Indian tree frog Hyla arborea. Acta Protozoologica 21, 197–199.Google Scholar
Schlick-Steiner, B. C., Seifert, B., Stauffer, C., Christian, E., Crozier, R. H. and Steiner, F. M. (2007). Without morphology, cryptic species stay in taxonomic crypsis following discovery. Trends in Ecology & Evolution 22, 391–392. doi: 10.1016/j.tree.2007.05.004.Google Scholar
Stamatakis, A. (2006). RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690. doi: 10.1093/bioinformatics/btl446.Google Scholar
Stensaas, L. J., Stensaas, S. S. and Sotelo, J. R. (1967). An intra-axonal protozoon in spinal cord of toad Bufo arenarum (Hensel). Journal of Protozoology 14, 585. doi: 10.1111/j.1550-7408.1967.tb02045.x.Google Scholar
Swofford, D. L., Waddell, P. J., Huelsenbeck, J. P., Foster, P. G., Lewis, P. O. and Rogers, J. S. (2001). Bias in phylogenetic estimation and its relevance to the choice between parsimony and likelihood methods. Systematic Biology 50, 525–539. doi: 10.1080/106351501750435086.Google Scholar
Supplementary material: Image

Hartigan Supplementary Figure

Hartigan Supplementary Figure

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Hartigan Supplementary Table

Supplementary Table 1. Myxosporean species DNA used for specificity test of Cystodiscus spp. with species specific multiplex PCR

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