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

Volumn 6, Issue 4, 2011, Pages

  Hartigan, Ashlie ^a   Fiala, Ivan ^b   Dyková, Iva ^b   Jirků, Miloslav ^b   Okimoto, Ben ^c   Rose, Karrie ^d   Phalen, David N ^a   Šlapeta, Jan ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b INSTITUTE OF PARASITOLOGY   (Czech Republic)

^c Honolulu Zoo   (United States)

^d TARONGA CONSERVATION SOCIETY AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

INTERNAL TRANSCRIBED SPACER 1; RIBOSOME DNA;

ANIMAL TISSUE; ARTICLE; BRAIN; BRAZIL; CONTROLLED STUDY; FROG; GENE SEQUENCE; GENOTYPE; LIVER; MYELINATED NERVE; MYXOZOA; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE IDENTIFICATION; PARASITE LOCALIZATION; PARASITOSIS; PHENOTYPE; PHYLOGENY; TOAD; UNITED STATES; ANIMAL; ANIMAL PARASITOSIS; AUSTRALIA; CYTOLOGY; ENDANGERED SPECIES; FROGS AND TOADS; GENETICS; GEOGRAPHY; GROWTH, DEVELOPMENT AND AGING; INTRODUCED SPECIES; LARVA; LIFE CYCLE; MOLECULAR GENETICS; MYELIN SHEATH; NERVE FIBER; PARASITE; PARASITOLOGY; PATHOLOGY; PHYSIOLOGY; ULTRASTRUCTURE;

AMPHIBIA; ANURA; BUFO MARINUS; LITORIA AUREA; LITORIA RANIFORMIS; MYXIDIUM; MYXOSPOREA; MYXOZOA;

ANIMALS; ANURA; AUSTRALIA; AXONS; BRAIN; BRAZIL; DNA, RIBOSOMAL; ENDANGERED SPECIES; GENOTYPE; GEOGRAPHY; HAWAII; INTRODUCED SPECIES; LARVA; LIFE CYCLE STAGES; LIVER; MOLECULAR SEQUENCE DATA; MYELIN SHEATH; MYXOZOA; PARASITES; PARASITIC DISEASES, ANIMAL; PHYLOGENY;

EID: 79955566064     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018871     Document Type: Article

References (69)

1. Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, et al. (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468: 647-652.
2. Smith KF, Sax DF, Lafferty KD, (2006) Evidence for the role of infectious disease in species extinction and endangerment. Conservation Biology 20: 1349-1357.
3. Blackburn DC, Evans BJ, Pessier AP, Vredenburg VT, (2010) An enigmatic mortality event in the only population of the Critically Endangered Cameroonian frog Xenopus longipes. African Journal of Herpetology 59: 111-122.
4. Briggs CJ, Knapp RA, Vredenburg VT, (2010) Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proceedings of the National Academy of Sciences of the United States of America 107: 9695-9700.
5. Teacher AGF, Cunningham AA, Garner TWJ, (2010) Assessing the long-term impact of Ranavirus infection in wild common frog populations. Animal Conservation 13: 514-522.
6. Green DE, Gray MJ, Miller DL, (2009) Disease monitoring and biosecurity. In: Dodd CK, editors. Amphibian Ecology and Conservation: A Handbook of Techniques Oxford Oxford Press pp. 481-505.
7. Sitjà-Bobadilla A, (2009) Can Myxosporean parasites compromise fish and amphibian reproduction? Proceedings of the Royal Society B: Biological Sciences 276: 2861-2870.
8. Mutschmann F, (2004) Pathological changes in African hyperoliid frogs due to a myxosporidian infection with a new species of Hoferellus (Myxozoa). Diseases of Aquatic Organisms 60: 215-222.
9. Duncan AE, Garner MM, Bartholomew JL, Reichard TA, Nordhausen RW, (2004) Renal myxosporidiasis in Asian horned frogs (Megophrys nasuta). Journal of Zoo and Wildlife Medicine 35: 381-386.
10. Hedrick RP, Adkison MA, El-Matbouli M, MacConnell E, (1998) Whirling disease: re-emergence among wild trout. Immunological Reviews 166: 365-376.
11. Steinbach-Elwell LC, Eagle-Dtromberg K, Ryce EKN, Bartholomew JL, (2009) Whirling Disease in the United States: A Summary of Progress in Research and Management Bozeman, MO Whirling Disease Initiative, Montana Water Center, Montana State University.
12. Whipps CM, El-Matbouli M, Hedrick RP, Blazer V, Kent ML, (2004) Myxobolus cerebralis internal transcribed spacer 1 (ITS-1) sequences support recent spread of the parasite to North America and within Europe. Diseases of Aquatic Organisms 60: 105-108.
13. Hill BD, Green PE, Lucke HA, (1997) Hepatitis in the green tree frog (Litoria caerulea) associated with infection by a species of Myxidium. Australian Veterinary Journal 75: 910-911.
14. Delvinquier BLJ, (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.
15. Hartigan A, Phalen DN, Šlapeta J, (2010) Museum material reveals a frog parasite emergence after the invasion of the cane toad in Australia. Parasites & Vectors 3: 50.
16. Dubey S, Shine R, (2008) Origin of the parasites of an invading species, the Australian cane toad (Bufo marinus): are the lungworms Australian or American? Molecular Ecology 17: 4418-4424.
17. Mahony M, (1996) The decline of the Green and Golden Bell Frog Litoria aurea viewed in the context of declines and disappearances of other Australian frogs. Australian Zoologist 30: 237-246.
18. Wassens S, (2008) Review of the past distribution and decline of the southern bell frog Litoria raniformis in New South Wales. Australian Zoologist 34: 446-452.
19. Mahony M, (1999) Review of the declines and disappearances within the bell frog species group (Litoria aurea species group) in Australia. In: Campbell A, editors. Declines and disappearances of Australian frogs: Environment Australia, Canberra pp. 81-93.
20. White AW, Pyke GH, (2008) Green and Golden Bell frogs in New South Wales: current status and future prospects. Australian Zoologist 34: 319-333.
21. Berger L, Speare R, Daszak P, Green DE, Cunningham AA, et al. (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proceedings of the National Academy of Sciences of the United States of America 95: 9031-9036.
22. McFadden M, Duffy S, Harlow P, Hobcroft D, Webb C, et al. (2008) A review of the green and golden bell frog Litoria aurea breeding program at Taronga Zoo. Australia Zoologist 34: 291-296.
23. Lom J, Dyková I, (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica 53: 1-36.
24. Lom J, Feist SW, Dyková I, Kepr T, (1989) Brain myxoboliasis of bullhead, Cottus gobio L., due to Myxobolus jiroveci sp. nov.: light and electron microscope observations. Journal of Fish Diseases 12: 15-27.
25. Dyková I, Lom J, (2007) Histopathology of Protistan and Myxozoan Infections in Fishes. An Atlas Praha Academia.
26. Stensaas LJ, Stensaas SS, Sotelo JR, (1967) An intra-axonal protozoon in the spinal cord of the toad Bufo arenarum (Hensel). Journal of Protozoology 14: 585-595.
27. Alencar AA, (1957) Toxoplasmose espontanea e inaparente em amfibios dos generos Leptodactylus e Bufo. Jornal Brasileiro de Neurologia 9: 137-146.
28. Lom J, McGeorge J, Feist SW, Morris D, Adams A, (1997) Guidelines for the uniform characterisation of the actinosporean stages of parasites of the phylum Myxozoa. Diseases of Aquatic Organisms 30: 1-9.
29. Jirků M, Bolek MG, Whipps CM, Janovy J, Kent ML, et al. (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.
30. Sutherst RW, Floyd RB, Maywald GF, (1996) The potential geographical distribution of the cane toad, Bufo marinus L in Australia. Conservation Biology 10: 294-299.
31. Phillips BL, Brown GP, Webb JK, Shine R, (2006) Invasion and the evolution of speed in toads. Nature 439: 803-803.
32. Urban MC, Phillips BL, Skelly DK, Shine R, (2007) The cane toad's (Chaunus [Bufo] marinus) increasing ability to invade Australia is revealed by a dynamically updated range model. Proceedings of the Royal Society B: Biological Sciences 274: 1413-1419.
33. Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, et al. (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution 22: 148-155.
34. Easteal S, (1981) The history of introductions of Bufo marinus (Amphibia: Anura)- a natural experiment in evolution. Biological Journal of the Linnean Society 16: 93-113.
35. Kudo R, 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 y Parasitología, Bacteriología, Clinica y Laboratoria 6: 65-73.
36. O'Donoghue PJ, Adlard RD, (2000) Catalogue of protozoan parasites recorded in Australia. Memoirs of the Queensland Museum 45: 1-163.
37. Hebert PDN, Stoeckle MY, Zemlak TS, Francis CM, (2004) Identification of birds through DNA barcodes. Plos Biology 2: 1657-1663.
38. Waugh J, (2007) DNA barcoding in animal species: progress, potential and pitfalls. Bioessays 29: 188-197.
39. Hemmerter S, Šlapeta J, van den Hurk A, Cooper R, Whelan P, et al. (2007) A curious coincidence: mosquito biodiversity and the limits of the Japanese encephalitis virus in Australasia. BMC Evolutionary Biology 7: 100.
40. Whipps CM, Kent ML, (2006) Phylogeography of the cosmopolitan marine parasite Kudoa thyrsites (Myxozoa: Myxosporea). Journal of Eukaryotic Microbiology 53: 364-373.
41. Henderson M, Okamura B, (2004) The phylogeography of salmonid proliferative kidney disease in Europe and North America. Proceedings of the Royal Society of London Series B: Biological Sciences 271: 1729-1736.
42. Gunter NL, Whipps CM, Adlard RD, (2009) Ceratomyxa (Myxozoa: Bivalvulida): Robust taxon or genus of convenience? International Journal for Parasitology 39: 1395-1405.
43. Fiala I, (2006) The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. International Journal for Parasitology 36: 1521-1534.
44. Kent ML, Andree KB, Bartholomew JL, El-Matbouli M, Desser SS, et al. (2001) Recent advances in our knowledge of the Myxozoa. Journal of Eukaryotic Microbiology 48: 395-413.
45. Holzer AS, Sommerville C, Wootten R, (2004) Molecular relationships and phylogeny in a community of myxosporeans and actinosporeans based on their 18S rDNA sequences. International Journal for Parasitology 34: 1099-1111.
46. Hufbauer RA, Torchin ME, (2008) Integrating ecological and evolutionary theory of biological invasion. In: Nentwig W, editors. Biological Invasions Heidelberg Springer pp. 79-96.
47. Tompkins DM, Poulin R, (2006) Parasites and biological invasion. In: Allen RB, Lee WG, editors. Biological Invasions in New Zealand Heidelberg Springer pp. 67-84.
48. Carlton JT, (1996) Biological invasions and cryptogenic species. Ecology 77: 1653-1655.
49. Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM, (2003) Introduced species and their missing parasites. Nature 421: 628-630.
50. Marr SR, Mautz WJ, Hara AH, (2008) Parasite loss and introduced species: a comparison of the parasites of the Puerto Rican tree frog, (Eleutherodactylus coqui), in its native and introduced ranges. Biological Invasions 10: 1289-1298.
51. Dunn AM, (2009) Parasites and biological invasions. Advances in Parasitology 68: 161-184.
52. Prenter J, MacNeil C, Dick JTA, Dunn AM, (2004) Roles of parasites in animal invasions. Trends in Ecology and Evolution 19: 385-390.
53. Daszak P, Cunningham AA, Hyatt AD, (2000) Emerging infectious diseases of wildlife- Threats to biodiversity and human health. Science 287: 443-449.
54. Power AG, Mitchell CE, (2004) Pathogen spillover in disease epidemics. American Naturalist 164: S79-S89.
55. Kelly DW, Paterson RA, Townsend CR, Poulin R, Tompkins DM, (2009) Parasite spillback: A neglected concept in invasion ecology? Ecology 90: 2047-2056.
56. Hershberger P, van der Leeuw B, Gregg J, Grady C, Lujan K, et al. (2010) Amplification and transport of an endemic fish disease by an introduced species. Biological Invasions 12: 3665-3675.
57. Telfer S, Bown KJ, Sekules R, Begon I, Hayden T, et al. (2005) Disruption of a host-parasite system following the introduction of an exotic host species. Parasitology 130: 661-668.
58. Rose K, (2005) Wildlife Health Investigation Manual: The Australian Registry of Wildlife Health.
59. Cameron AR, Baldock FC, (1998) A new probability formula for surveys to substantiate freedom from disease. Preventive Veterinary Medicine 34: 1-17.
60. Coleman AW, Vacquier VD, (2002) Exploring the phylogenetic utility of ITS sequences for animals: A test case for abalone (Haliotis). Journal of Molecular Evolution 54: 246-257.
61. Bartošová P, Fiala I, 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.
62. Wheeler DL, Barrett T, Benson DA, Bryant SH, Canese K, et al. (2008) Database resources of the national center for biotechnology information. Nucleic Acids Research 36: D13-D21.
63. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596-1599.
64. Canning EU, Tops S, Curry A, Wood TS, Okamura B, (2002) Ecology, development and pathogenicity of Buddenbrockia plumatellae Schroder, 1910 (Myxozoa, Malacosporea) (syn. Tetracapsula bryozoides) and establishment of Tetracapsuloides n. gen. for Tetracapsula bryosalmonae. Journal of Eukaryotic Microbiology 49: 280-295.
65. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG, (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25: 4876-4882.
66. Talavera G, Castresana J, (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56: 564-577.
67. Guindon S, Gascuel O, (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52: 696-704.
68. Ronquist F, Huelsenbeck JP, (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
69. Posada D, Crandall KA, (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14: 817-818.