A Model for Taxonomic Work on Homoxenous Coccidia: Redescription, Host Specificity, and Molecular Phylogeny of Eimeria ranae Dobell, 1909, with a Review of Anuran‐Host Eimeria (Apicomplexa: Eimeriorina)

ABSTRACT. We attempt to extend knowledge of anuran Eimeria, and to provide a model for a complex approach to studies on coccidia. New host and geographic records of coccidia in European Anura are provided. In the second part, Eimeria ranae Dobell, 1909 is redescribed from European terrestrial frogs of the genus Rana based on light microscopic and ultrastructural data on both exogenous and endogenous developmental stages, host specificity, and molecular phylogenetic data. Results of experimental transmissions show for the first time that the host specificity of E. ranae is restricted to the genus Rana and that isolates from tadpoles and adults are conspecific. Disappearance of infection during metamorphosis was confirmed experimentally, suggesting that infections in adults result from reinfections. Poikilotherm‐host Eimeria species possessing a Stieda body (SB) are for the first time included in a molecular phylogenetic analysis. Eimeria ranae and Eimeria arnyi from a colubrid snake form together a well‐supported clade, basal to other SB‐bearing coccidia. The other analysed reptile–host eimerians, Eimeria tropidura and Choleoeimeria sp., which possess bivalved sporocysts and lack a SB, represent a distinct basal lineage of the eimeriid clade. The third part of the article reviews anuran‐host Eimeria. Three distinct oocyst morphotypes, apparently correlating with the character of endogenous development, are recognized and characterized among anuran eimeriids.

[1]  I. Paperna.  Ultrastructural and developmental affinities of piscine coccidia , 1995 .

[2]  C. Dobell.  Researches on the Intestinal Protozoa of Frogs and Toads , 1909 .

[3]  M. Sogin,et al.  The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. , 1988, Gene.

[4]  D. Duszynski,et al.  A guideline for the preparation of species descriptions in the Eimeriidae. , 1997, The Journal of parasitology.

[5]  R. Lainson,et al.  Life history and ultrastructure of Eimeria bufomarini n.sp. (Apicomplexa: Eimeriidae) of the giant toad, Bufo marinus (Amphibia: Anura) from Amazonian Brazil , 1995 .

[6]  David Posada,et al.  MODELTEST: testing the model of DNA substitution , 1998, Bioinform..

[7]  R. Wassersug,et al.  Metamorphic shortening of the alimentary tract in anuran larvae (Rana catesbeiana) , 1995, The Anatomical record.

[8]  J. Lukeš,et al.  Phylogeny of trypanosomes as inferred from the small and large subunit rRNAs: implications for the evolution of parasitism in the trypanosomatid protozoa. , 1996, Molecular and biochemical parasitology.

[9]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[10]  D. Modrý,et al.  Extra-intestinal localization of Goussia sp. (Apicomplexa) oocysts in Rana dalmatina (Anura: Ranidae), and the fate of infection after metamorphosis. , 2006, Diseases of aquatic organisms.

[11]  O. Gascuel,et al.  A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. , 2003, Systematic biology.

[12]  D. Morrison,et al.  The current status of the small subunit rRNA phylogeny of the coccidia (Sporozoa). , 2004, International journal for parasitology.

[13]  J. Lukeš,et al.  The phylogeny of Goussia and Choleoeimeria (Apicomplexa; Eimeriorina) and the evolution of excystation structures in coccidia. , 2002, Protist.

[14]  D. Modrý,et al.  Eimeria fragilis and E. wambaensis, two new species of Eimeria Schneider [Apicomplexa: Eimeriidae] from African anurans , 2005 .

[15]  J. Janovy,et al.  OBSERVATIONS ON THE LIFE HISTORY AND DESCRIPTIONS OF COCCIDIA (APICOMPLEXA) FROM THE WESTERN CHORUS FROG, PSEUDACRIS TRISERIATA TRISERIATA, FROM EASTERN NEBRASKA , 2003, The Journal of parasitology.

[16]  C. McAllister,et al.  The Coccidia (Apicomplexa: Eimeriidae) of Anura, with descriptions of four new species , 1988 .

[17]  J. Lukeš,et al.  Phylogenetic analysis of coccidian parasites from invertebrates: search for missing links. , 2006, Protist.

[18]  M. Vences,et al.  Climatic oscillations triggered post-Messinian speciation of Western Palearctic brown frogs (Amphibia, Ranidae). , 2003, Molecular phylogenetics and evolution.

[19]  E. Stanley,et al.  Parasite s of Wood Frogs, Rana sylvatica (Ranidae), from Arkansas, with a Description of a New Species of Eimeria (Apicomplexa: Eimeriidae) , 1995 .

[20]  N. D. Levine,et al.  Cross-transmission of Eimeria spp. (Protozoa, Apicomplexa) of rodents--a review. , 1988, The Journal of protozoology.

[21]  L. Trueb,et al.  Biology of Amphibians , 1986 .

[22]  D. Morrison,et al.  The conceptual basis for a new classification of the coccidia. , 2002, International journal for parasitology.

[23]  P. L. Long,et al.  Problems in the identification of species of Eimeria. , 1984, The Journal of protozoology.

[24]  D. Duszynski,et al.  Cross-transmission studies with Eimeria arizonensis, E. arizonensis-like oocysts and Eimeria langebarteli: host specificity at the genus and species level within the Muridae. , 1999, The Journal of parasitology.

[25]  I. Paperna,et al.  Goussia hyperolisi n. sp. : a coccidian infection in reed frog Hyperolis viridiflavus tadpoles which expires towards metamorphosis , 1997 .

[26]  John J. Lee,et al.  An illustrated guide to the protozoa , 1985 .

[27]  D. Duszynski,et al.  Seven new species of Eimeria Schneider, 1875 (Apicomplexa: Eimeriidae) from colubrid snakes of Guatemala and a discussion of what to call ellipsoid tetrasporocystic, dizoic coccidia of reptiles , 2006, Systematic Parasitology.

[28]  I. Paperna,et al.  Description and taxonomic discussion of eimerian coccidia from African and Levantine geckoes , 1989 .

[29]  W. L. Gannon,et al.  Designation and curatorial management of type host specimens (Symbiotypes) for new parasite species , 1992 .

[30]  S. Desser,et al.  The Coccidia (Apicomplexa: Eimeriidae) of frogs from Algonquin Park, with descriptions of two new species , 1989 .

[31]  S. J. Upton,et al.  Coccidia (Apicomplexa: Eimeriidae) of amphibians of the world , 2007 .

[32]  J. Thompson,et al.  The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. , 1997, Nucleic acids research.

[33]  S. Ueda,et al.  Apoptosis and cell proliferation in the Xenopus small intestine during metamorphosis , 1996, Cell and Tissue Research.

[34]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .