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Widespread infection of the Eastern red-spotted newt (Notophthalmus viridescens) by a new species of Amphibiocystidium, a genus of fungus-like mesomycetozoan parasites not previously reported in North America

Published online by Cambridge University Press:  12 October 2007

T. R. RAFFEL ,
T. BOMMARITO ,
D. S. BARRY ,
S. M. WITIAK  and
L. A. SHACKELTON
T. R. RAFFEL*
Affiliation:
Center for Infectious Disease Dynamics, Biology Department, Penn State University, University Park, PA 16802, USA Department of Biology, University of South Florida, Tampa, FL 33620, USA
T. BOMMARITO
Affiliation:
Cooperative Wildlife Research Lab, Department of Zoology, Southern Illinois University, Carbondale, IL 62901, USA
D. S. BARRY
Affiliation:
Department of Biological Sciences, Marshall University, Huntington, WV 25755, USA
S. M. WITIAK
Affiliation:
Department of Plant Pathology, Penn State University, University Park, PA 16802, USA
L. A. SHACKELTON
Affiliation:
Center for Infectious Disease Dynamics, Biology Department, Penn State University, University Park, PA 16802, USA
*
*Corresponding author: 4202 E. Fowler Avenue, SCA 110, Tampa, Florida33620, USA. Tel: +813 974 6210. Fax: +813 974 3263. E-mail: traffel@cas.usf.edu
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Summary

Given the worldwide decline of amphibian populations due to emerging infectious diseases, it is imperative that we identify and address the causative agents. Many of the pathogens recently implicated in amphibian mortality and morbidity have been fungal or members of a poorly understood group of fungus-like protists, the mesomycetozoans. One mesomycetozoan, Amphibiocystidium ranae, is known to infect several European amphibian species and was associated with a recent decline of frogs in Italy. Here we present the first report of an Amphibiocystidium sp. in a North American amphibian, the Eastern red-spotted newt (Notophthalmus viridescens), and characterize it as the new species A. viridescens in the order Dermocystida based on morphological, geographical and phylogenetic evidence. We also describe the widespread and seasonal distribution of this parasite in red-spotted newt populations and provide evidence of mortality due to infection.

Keywords

DermocystidaDermocystidiumAmphibiothecumamphibian declinesalamanderfungal infection
Type
Research Article
Information
Parasitology , Volume 135 , Issue 2 , February 2008 , pp. 203 - 215
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

ASTM. (1988). Standard Practice for Conducting Acute Toxicity Tests with Fishes, Macroinvertebrates, and Amphibians. ASTM, West Conshohocken, PA, USA.Google Scholar
Berger, L., Speare, R., Hines, H. B., Marantelli, G., Hyatt, A. D., McDonald, K. R., Skerratt, L. F., Olsen, V., Clarke, J. M., Gillespie, G., Mahony, M., Sheppard, N., Williams, C. and Tyler, M. J. (2004). Effect of season and temperature on mortality in amphibians due to chytridiomycosis. Australian Veterinary Journal 82, 434–439.Google Scholar
Bly, J. E., Lawson, L. A., Szalai, A. J. and Clem, L. W. (1993). Environmental factors affecting outbreaks of winter saprolegniosis in Channel catfish, Ictalurus Punctatus (Rafinesque). Journal of Fish Diseases 16, 541–549.CrossRefGoogle Scholar
Bower, S. M., Carnegie, R. B., Goh, B., Jones, S. R. M., Lowe, G. J. and Mak, M. W. S. (2004). Preferential PCR amplification of parasitic protistan small subunit rDNA from metazoan tissues. Journal of Eukaryotic Microbiology 51, 325–332.Google Scholar
Branscomb, R. (2002). Rhinosporidiosis update. Laboratory Medicine 33, 631–633.CrossRefGoogle Scholar
Broz, O. (1944). Die Herkunft der Zystenmembran von Dermocystidium ranae. Vestnik Ceskoslovenske Spolecnosti Zoologicke 9, 16–25.Google Scholar
Broz, O. and Privora, M. (1951). Two skin parasites of Rana temporaria: Dermocystidium ranae Guyenot & Naville and Dermosporidium granulosom n. sp. Parasitology 42, 65–69.CrossRefGoogle Scholar
Carini, A. (1940). Sobre um parasito semelhante ao “Rhinosporidium” encontrado em quistos da pelede uma “Hyla”. Arquivos do Institutos Biologico 11, 93–98.Google Scholar
Chinchar, V. G. (2002). Ranaviruses (family Iridoviridae): emerging cold-blooded killers. Archives of Virology 147, 447–470.Google Scholar
Daszak, P., Cunningham, A. A. and Hyatt, A. D. (2001). Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Tropica 78, 103–116.Google Scholar
Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 1792–1797.CrossRefGoogle ScholarPubMed
Feldman, S. H., Wimsatt, J. H. and Green, D. E. (2005). Phylogenetic classification of the frog pathogen Amphibiothecum (Dermosporidium) penneri based on small ribosomal subunit sequencing. Journal of Wildlife Diseases 41, 701–706.CrossRefGoogle ScholarPubMed
Gambier, H. (1924). Sur un Protiste parasite et pathogene des Tritons: Hepatosphera molgarum n. g., n. sp. Comptes Rendus des Séances de la Societe de Biologie et de des Filiales 90, 439–441.Google Scholar
Gill, D. E. (1979). Density dependence and homing behavior in adult red-spotted newts, Notophthalmus viridescens (Rafinesque). Ecology 60, 800–813.Google Scholar
Goodchild, C. G. (1953). A subcutaneous, cyst-parasite of Bullfrogs: Histocystidium ranae, n. g., n. sp. Journal of Parasitology 39, 395–405.Google Scholar
Green, D. E., Converse, K. A. and Schrader, A. K. (2002). Epizootiology of sixty-four amphibian morbidity and mortality events in the USA, 1996–2001. Annals of the New York Academy of Sciences 969, 323–339.Google Scholar
Green, D. E., Feldman, S. H. and Wimsatt, J. H. (2003). Emergence of a Perkinsus-like agent in anuran liver during die-offs of local populations: PCR detection. American Association of Zoo Veterinarians Conference Proceedings, Milwaukee, Wisconsin, 120–121.Google Scholar
Green, D. E. and Sherman, C. K. (2001). Diagnostic histological findings in Yosemite toads (Bufo canorus) from a die-off in the 1970s. Journal of Herpetology 35, 92–103.CrossRefGoogle Scholar
Guyenot, E. and Naville, A. (1922). Un nouveau protiste du genre Dermocystidium parasite de la Grenouille Dermocystidium ranae nov. spec. Revue Suisse de Zoologie 29, 133–145.Google Scholar
Holl, F. J. (1932). The ecology of certain fishes and amphibians with special reference to their helminth and linguatulid parasites. Ecological Monographs 2, 83–107.Google Scholar
Hopkins, S. H. (1933). Note on the life history of Clinostomum marginatum (Trematoda). Transactions of the American Microscopical Society 52, 147–149.CrossRefGoogle Scholar
Jancovich, J. K., Davidson, E. W., Parameswaran, N., Mao, J., Chinchar, V. G., Collins, J. P., Jacobs, B. L. and Storfer, A. (2005). Evidence for emergence of an amphibian iridoviral disease because of human-enhanced spread. Molecular Ecology 14, 213–224.CrossRefGoogle ScholarPubMed
Jay, J. M. and Pohley, W. J. (1981). Dermosporidium penneri sp n from the skin of the American toad, Bufo americanus (Amphibia, Bufonidae). Journal of Parasitology 67, 108–110.CrossRefGoogle Scholar
Johnson, P. T. and Lunde, K. B. (2005). Parasite infection and limb malformations: A growing problem in amphibian conservation. In Amphibian Declines: the Conservation Status of United States Species (ed. Lannoo, M. J.). pp. 124–138. University of California Press, Berkeley, USA.Google Scholar
Johnson, P. T. J. and Chase, J. M. (2004). Parasites in the food web: linking amphibian malformations and aquatic eutrophication. Ecology Letters 7, 521–526.Google Scholar
Johnson, P. T. J., Lunde, K. B., Zelmer, D. A. and Werner, J. K. (2003). Limb deformities as an emerging parasitic disease in amphibians: Evidence from museum specimens and resurvey data. Conservation Biology 17, 1724–1737.Google Scholar
Kurzava, L. M. and Morin, P. J. (1998). Tests of functional equivalence: Complementary roles of salamanders and fish in community organization. Ecology 79, 477–489.CrossRefGoogle Scholar
Lips, K. R., Brem, F., Brenes, R., Reeve, J. D., Alford, R. A., Voyles, J., Carey, C., Livo, L., Pessier, A. P. and Collins, J. P. (2006). Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proceedings of the National Academy of Sciences, USA 103, 3165–3170.CrossRefGoogle Scholar
Moral, H. (1913). Über das Auftreten von Dermocystidium pusula (Pérez), einem einzelligen Parasiten der Haut des Molches bei Triton cristatus. Archiv für mikroskopische Anatomie 81, 381–393.Google Scholar
Muzzall, P. M., Peterson, J. D. and Gillilland, M. G. (2003). Helminths of Notophthalmus viridescens (Caudata: salamandridae) from 118th Pond, Michigan, USA. Comparative Parasitology 70, 214–217.CrossRefGoogle Scholar
Olson, R. E., Dungan, C. F. and Holt, R. A. (1991). Water borne transmission of Dermocystidium salmonis in the laboratory. Diseases of Aquatic Organisms 12, 41–48.Google Scholar
Padgett-Flohr, G. E., Bommarito, T. and Sparling, D. (2007). Amphibian chytridiomycosis: Implications regarding amphibian research. Herpetological Review (in the Press).Google Scholar
Page, R. D. M. (1996). TREEVIEW: An application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12, 357–358.Google Scholar
Pascolini, R., Daszak, P., Cunningham, A. A., Tei, S., Vagnetti, D., Bucci, S., Fagotti, A. and Di Rosa, I. (2003). Parasitism by Dermocystidium ranae in a population of Rana esculenta complex in central Italy and description of Amphibiocystidium n. gen. Diseases of Aquatic Organisms 56, 65–74.Google Scholar
Pereira, C. N., Di Rosa, I., Fagotti, A., Simoncelli, F., Pascolin, R. and Mendoza, L. (2005). The pathogen of frogs Amphibiocystidium ranae is a member of the order Dermocystida in the class Mesomycetozoea. Journal of Clinical Microbiology 43, 192–198.CrossRefGoogle ScholarPubMed
Pérez, C. (1907). Dermocystis pusula organisme nouveau parasite de la peau des Tritons. Comtes Rendus de la Société de Biologie 63, 445–447.Google Scholar
Pérez, C. (1913). Dermocystidium pusula: Parasite de la peau des Tritons. Archives de Zoologie Expérimentale et Générale 52, 343–357.Google Scholar
Poisson, C. (1937). Sur une nouvelle espèce du genre Dermomycoides Granata 1919: Dermomycoides armoriacus Poisson 1936 parasite cutané de Triturus palmatus (Schneider). Genèse et structure de la zoospore. Bulletin Biologique de la France et de la Belgique 71, 91–116.Google Scholar
Posada, D. and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.Google Scholar
Raffel, T. R. (2006). Drivers of seasonal infection dynamics in the parasite community of red-spotted newts (Notophthalmus viridescens). Ph. D. thesis. The Pennsylvania State University, University Park, USA.Google Scholar
Raffel, T. R., Dillard, J. R. and Hudson, P. J. (2007). Field evidence for leech-borne transmission of amphibian Ichthyophonus. Journal of Parasitology 92, 1256–1264.Google Scholar
Raffel, T. R., Rohr, J. R., Kiesecker, J. M. and Hudson, P. J. (2006). Negative effects of changing temperature on amphibian immunity under field conditions. Functional Ecology 20, 819–828.Google Scholar
Remy, P. (1931). Presence de Dermocystidium ranae (Guyenot et Naville) chez une Rana esculenta L. de Lorraine. Annales de Parasitologie Humaine et Comparee 9, 1–3.Google Scholar
Rohr, J. R., Madison, D. M. and Sullivan, A. M. (2002). Sex differences and seasonal trade-offs in response to injured and non-injured conspecifics in red-spotted newts, Notophthalmus viridescens. Behavioral Ecology and Sociobiology 52, 385–393.Google Scholar
Russell, C. M. (1951). Survey of the intestinal helminths of Triturus v. viridescens in the vicinity of Charlottesville, Virginia. Virginia Journal of Science 2, 215–219.Google Scholar
Sever, D. M. (2002). Female sperm storage in amphibians. Journal of Experimental Zoology 292, 165–179.CrossRefGoogle ScholarPubMed
Shaw, D. J. and Dobson, A. P. (1995). Patterns of macroparasite abundance and aggregation in wildlife populations: A quantitative review. Parasitology 111 (Suppl.), S111–S133.CrossRefGoogle ScholarPubMed
Shaw, D. J., Grenfell, B. T. and Dobson, A. P. (1998). Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117, 597–610.CrossRefGoogle ScholarPubMed
Shimodaira, H. and Hasegawa, M. (1999). Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16, 1114–1116.CrossRefGoogle Scholar
Swofford, D. L. (2003). PAUP*: Phylogenetic Analysis using Parsimony (and other Methods). Version 4.0. Sinauer Associates, Sunderland, MA, USA.Google Scholar
Weldon, C., du Preez, L. H., Hyatt, A. D., Muller, R. and Speare, R. (2004). Origin of the amphibian chytrid fungus. Emerging Infectious Diseases 10, 2100–2105.Google Scholar