Coccidia (Eimeria and Isospora) of Anura

Compiled by
Donald W. Duszynski 1, Steve J. Upton 2, and Lee Couch 1

1 Department of Biology, University of New Mexico
2 Division of Biology, Kansas State University

Supported by NSF-PEET DEB 9521687

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Updated: 20 January 2008
Comments: eimeria@unm.edu (Duszynski), lcouch@unm.edu (Couch), or coccidia@ksu.edu (Upton)

    Family: Bufonidae

    Eimeria bufomarini Paperna and Lainson, 1995

    1. Host: Chaunus marinus (Cane toad)
    2. Reference: Paperna and Lainson 1995

    Eimeria himalayana Ray and Misra, 1941

    1. Synonym: Eimeria himalyanum Ray and Misra, 1941, lapsus
    2. Host: Duttaphyrnus himalayanus (Himalayan toad)
    3. References: Ray and Misra 1941, 1943

    Eimeria laminata Ray, 1935

    1. Synonym: Eimeria laminata (Ray, 1935) Paperna and Lainson 1995, lapsus
    2. Host: Duttaphrynus melanostictus (Black-spined toad)
    3. References: Ray 1935a, 1935b

    Eimeria mazzai Yakimoff and Gousseff, 1934

    1. Synonym: Eimeria transcaucasica Yakimoff and Gousseff, 1936
    2. Host: Bufo bufo (European common toad)
    3. References: Saxe 1955; Yakimoff and Gousseff 1934, 1936a; Walton 1964b

    Isospora brumpti Lavier, 1941

    1. Synonym: Diplospora brumpti (Lavier, 1941) Grasse, 1953
    2. Host: Pseudepidalea viridis (Green toad)
    3. References: Grasse 1953; Lavier 1941; Ovezmukhammedov 1973

    Isospora stomatici Chakravarty and Kar, 1944 emend. Levine, 1985

    1. Host: Bufo stomaticus (Marbled toad)
    2. Reference: Chakrvarty and Kar 1944, 1952

    Isospora wenyoni Ray and Das Gupta, 1935

    1. Host: Duttaphrynus melanostictus (Black-spined toad)
    2. Reference: Ray and Das Gupta 1935
    3. Chakravarty and Kar (1944) erroneously reported this eimerian from two Rana spp.

    Family: Dicroglossidae

    Eimeria cyanophlyctis Chakravarty and Kar, 1944

    1. Host: Euphlyctis cyanophlyctis
    2. Reference: Chakravarty and Kar 1944, 1952

    Eimeria terraepokotorum Jirku and Modry, 2006

    1. Host: Hoplobatrachus occipitalis (African tigrine frog)
    2. Reference: Jirky and Modry, 2006a

    Family: Hylidae

    Eimeria belawini Yakimoff, 1930

    1. Host: Hyla arborea (European tree frog)
    2. References: Levine and Becker 1933; Walton 1940, 1941, 1947; Yakimoff 1930a, 1930b

    Eimeria flexuosa Upton and McAllister, 1988

    1. Host: Pseudacris streckeri (Stecker's chorus frog)
    2. Reference: Upton and McAllister 1988

    Eimeria streckeri Upton and McAllister, 1988

    1. Host: Pseudacris streckeri (Strecker's chorus frog), Pseudacris triseriata (Western chorus frog
    2. Reference: Upton and McAllister 1988

    Isospora cogginsi Bolek, Janovy, and Irizarry-Rovira, 2003

    1. Host: Pseudacris triseriata (Western chorus frog)
    2. Reference: Bolek, Janovy, and Irizarry-Rovira, 2003

    Isospora cruzi Pinto and Vallim, 1926

    1. Hosts: Scinax crospedospilus (=Hyla crospedospila) (Campo Belo snouted treefrog), Scinax fuscovarius (=H. fuscoraria) (Snouted treefrog), Scinax nasicus (=H. nasica (lesser snouted treefrog), Scinax ruber (=H. rubra) (Red snouted treefrog)
    2. References: Pinto and Vallim 1926; Walton 1947

    Isospora delicatus Upton and McAllister, 1988

    1. Host: Pseudacris streckeri (Strecker's chorus frog)
    2. References: McAllister 1989; Upton and McAllister 1988

    Isospora wladimirovi Yakimoff, 1930

    1. Host: Hyla arborea (European tree frog)
    2. References: Yakimoff 1930a, 193b

    Family: Hyperolidae

    Eimeria wambaensis Jirku and Modry, 2005

    1. Host: Hyperolius viridiflavus (Common reed frog)
    2. Reference: Jirku and Modry, 2005

    Goussia hyperolisi Paperna, Ogara, and Schein, 1997

    1. Host: Tadpole of Hyperolis viridiflavus (Common reed frog)
    2. Reference: Paperna et al. 1997

    Family: Leptodacylidae

    Eimeria leptodactyli Carini, 1931

    1. Host: Leptodactylus ocellatus (Criolla frog)
    2. References: Carini 1931a, 1931b, 1931c; Walton 1945

    Family: Microhylidae

    Isospora fragosum Upton and McAllister, 1988

    1. Synonym: Isospora sp. of McAllister and Upton, 1987
    2. Host: Gastrophryne olivacea (Great Plains narrowmouth toad)
    3. References: McAllister 1989; McAllister and Upton 1987; Upton and McAllister 1988

    Family: Ranidae

    Eimeria algonquini Chen and Desser, 1988

    1. Hosts: Lithobates catesbeianus (American bullfrog), L. clamitans (Green frog), L. septentrionalis (Mink frog), L. sylvaticus (Wood frog)
    2. Reference: Chen and Desser 1988

    Eimeria fitchi McAllister, Upton, Trauth, and Bursey, 1995

    1. Host: Lithobates sylvaticus (Wood frog)
    2. Reference: McAllister et al. 1995

    Eimeria kermiti Chen and Desser, 1988

    1. Hosts: Lithobates catesbeianus (American bullfrog), L. clamitans (Green frog), L. septentrionalis (Mink frog),
    2. L. sylvaticus (Wood frog)
    3. Reference: Chen and Desser 1988

    Eimeria prevoti (Laveran and Mesnil, 1902) Doflein, 1909

    1. Synonym: Paracoccidium prevoti Laveran and Mesnil, 1902
    2. Synonym: Eimeria prevunti (Laveran and Mesnil, 1902) Yakimoff and Matikaschwili, 1933, lapsus
    3. Host: Pelophylax lessonae (Little water frog)
    4. References: Boulard 1975; Doflein 1909; Kazubski and Grabda-Kazubska 1974; Laveran and Mesnil 1902a; Noller 1913

    Eimeria ranae (Dobell, 1908) Dobell, 1909

    1. Synonym: Coccidium ranae Dobell, 1909
    2. Hosts: Rana temporaria (Grass frog), Pelophylax esculenta (Pool frog)
    3. References: Dobell 1908, 1909; Kazubski and Grabda-Kazubska 1974; Walton 1949b

    Eimeria ranarum (Labbe, 1894) Doflein, 1909

    1. Synonym: Acystis parasitica (Labbe, 1894, pro parte
    2. Synonym: Caryophagus ranarum Labbe, 1899
    3. Synonym: Coccidium ranarum (Labbe, 1894) Laveran and Mesnil, 1902
    4. Synonym: Karyophagus ranarum Labbe, 1894
    5. Hosts: Pelophylax esculenta(Pool frog), R. temporaria (Grass frog)
    6. References: Doflein 1909; Kazubski and Grabda-Kazubska 1974; Labbe 1894; Laveran and Mesnil 1902a; Rankin 1937; Walton 1941, 1949b, 1961
    7. Walton (1941, 1961) erroneously reports two Ambystoma spp. as hosts for this coccidian

    Goussia neglecta (Noller, 1920) Molnar, 1995

    1. Synonym: Eimeria neglecta Noller, 1920
    2. Hosts: Tadpoles of Pelophylax esculenta (Pool frog), possibly tadpoles of P. lessonae (Little water frog), possibly tadpoles of R. temporaria (Grass frog)
    3. References: Molnar 1995; Noller 1920; Walton 1949b

    Hyaloklossia lieberkuehni (Labbe, 1894) Laveran and Mesnil, 1902

    1. Synonym: Diplospora lieberkuhni (Labbe, 1894) Grasse, 1953; Hyaloklossia lieberkuhni (Labbe, 1894) Labbe, 1896; Klossia lieberkuhni Labbe, 1894; Isospora lieberkuhni (Labbe, 1894) Laveran and Mesnil, 1902
    2. Host: Pelophylax esculenta (Pool frog); Lithobates pipiens (Northern leopard frog); P. ridibunda (Marsh frog);
    3. R. temporaria (Grass frog); Bombina variegata (Yellowbelly toad).
    4. References: Golemansky and Bitseva 1975; Grasse 1953; Kazubski and Grabda-Kazubska 1974; Labbe 1894, 1896; Laveran and Mesnil 1902b; Levine and Nye 1977; Lieberkuhn 1854; Noller 1913, 1923; Vojtkova 1976; Walton 1941, 1949b

    Isospora neos Yakimoff and Gousseff, 1936

    1. Host: Rana arvalis (Peat-bog or Moor frog)
    2. References: Kazubski and Grabda-Kazubsa 1973, 1974; Yakimoff and Gousseff 1936b

    Family: Rhacophoridae

    Eimeria fragilis Jirku and Modry, 2005

    1. Host: Chiromantis petersii kelleri (Central foam-nest tree frog)
    2. References: Jirku and Modry, 2005


    Non-Valid Designations

    SPECIES INQUIRENDAE, INCERTAE SEDIS, AND NOMENA NUDA

    In this section, we place all those “coccidia” (Eimeriidae) about which too little is known from the published literature to decide whether they are real or not. Using definitions from the 4th edition of the International Code of Zoological Nomenclature (Ride et al. 2000), species inquirenda (pl. species inquirendae) refers to “a species of doubtful identity needing further investigation.” Implicit in our use of this term is that the taxonomic unit, or “species,” has been taxonomically named in some published document, but without existence of a type specimen of any kind (e.g. line drawing, photosyntype, stages in tissue sections, oocysts in preservative, etc.) and without sufficient qualitative and quantitative data on the most widely available stage in the lifecycle (i.e. the sporulated oocyst) to distinguish it from other, perhaps closely related, species.

    The term incertae sedis, defined by the Code, means “of uncertain taxonomic position.” Thus, this term applies to forms that are mentioned (e.g. as Eimeria sp. or Isospora sp.), but for which no mensural or qualitative data (e.g. number of sporocysts and sporozoites in the oocyst) were provided.

    Finally, sometimes authors, especially in the older literature, gave new names to organisms they saw, but failed to conform to Article 12 of the Code if published before 1931 or, if published after 1930, failed to conform to Article 13 (Ride et al. 2000). These names become nomen nudum (pl. nomena nuda), and, thus, become preoccupied and unavailable names. However, the same name may be made available later for the same or a different concept, but in such a case it would take authorship and date from that act of establishment, not from any earlier publication as a nomen nudum.

    SPECIES INQUIRENDAE

    "Coccidian" of Paperna and Lainson 1995, species inquirenda

    1. Host: Leptodactylus fuscus (Schneider 1799) (Rufous frog).
    2. In their paper describing the life history and ultrastructure of E. bufomarini, Paperna and Lainson (1995) mentioned finding another, as yet undescribed coccidium, in the Brazilian frog, Leptodactylus fuscus and said that this undescribed species also demonstrated endogenous sporogony in the epithelial cells of the intestine. Unfortunately, they never published this work.

    Goussia sp. of Jirku and Modrý 2006b, species inquirenda

    1. Host: Rana dalmatina Fitzinger In Bonaparte 1839 (Agile frog)
    2. Jirku and Modrý (2006b) reported on the extra-intestinal localization of Goussia sp. oocysts in R. dalmatina from the Czech Republic. Their sporocysts were remarkably similar to G. neglecta and overlapped in their dimensions. However, because G. neglecta is known to parasitize P. esculenta and P. ridibunda and recent findings that some Goussia spp. parasitizing fish have narrow host specificity (Molnár et al. 2005) these authors took a conservative approach and did not name their species of Goussia until experimental infections and molecular data can be obtained.

    Goussia-like coccidian” of Paperna et al. 1997, species inquirenda

    1. Host: Limnodynastes tasmaniensis Günther (1858) (Spotted marsh frog).
    2. Paperna et al. (1997) in their description paper on G. hyperolisi reported that L. Berger of the CSIRO Australian Animal Health Laboratory, Geelong, Victoria, Australia, presented them with a histological slide prepared from the intestine of a Limnodynastes tasmaniensis (=Lymnodynastes tasmanicus) tadpole heavily infected with sporulating Goussia-like oocysts. Unfortunately these authors never described the species, and nothing is known about it.

    Isospora lieberküehni (Labbé 1894) of Levine and Nye 1977, species inquirenda

    1. Synonym: Isospora lieberküehnk (Labbé 1894b) Laveran and Mesnil 1902b.
    2. Host: Lithobates pipiens (Schreber 1782) (Northern leopard frog).
    3. Levine and Nye (1977) reported the infection in 1 L. pipiens from Wisconsin, USA, as a new host and geographic record based solely on merozoites seen in the kidney tubule epithelial cells. It is difficult to tell what group of apicomplexans Levine and Nye (1977) were dealing with, however, because no oocysts were recovered and this species has been reported from European Pelophylax spp. It is doubtful that these authors were dealing with I. lieberküehni.

    Isospora hylae Mesnil 1907, species inquirenda

    1. Host: Hyla arborea (L. 1758) (European treefrog).
    2. Mesnil (1907) found oocysts in the digestive tract of H. arborea specimens from the outskirts of Paris. They were described as ellipsoidal, flattened at one end, 30–35 x 20–25 without an OR and sporocysts were ovoidal 23 x 17 with a SR. Mesnil (1907) said that endogenous development occured in the epithelial cells of the small intestine, while oocysts remained in the rectum of the frog. Neither line drawing nor photomicrograph(s) accompanied Mesnil’s description.

    Isospora lieberkühni Labbé 1894 of Golemansky and Bitseva (1975), species inquirenda

    1. Host: Bombina variegata (L. 1758) (Yellow-bellied toad).
    2. Golemansky and Bitseva (1975) said they found I. lieberkühni in this host in Bulgaria. Because of host and geographic differences, this seems highly unlikely (also see Modrý et al. 2001).

    Isospora lieberkühni Labbé 1894, species inquirinda

    1. Host: Pelophylax spp. (European water frog).
    2. This has been an enigmatic organism that has perplexed coccidiologists since it was first reported by Lieberkühn (1854) as “Psorospermus,” a renal coccidium of water frogs (Pelophyla spp.). However, Modrý et al. (2001) sequenced its SSU rRNA and found that its true taxonomic position belongs in their re-erected (2001) genus, Hyaloklossia Labbé 1896. Thus, what was probably best considered a species inquirenda prior to 2001 is now known to be a valid species of Hyaloklossia (see Remarks under Hyaloklossia lieberküehni).

    “Oocysts” of Griner, 1982, species inquirenda

    1. Host: Megophrys nasuta (Schlegel 1858) (Malayan horned frog).
    2. Griner (1982) reported seeing oocysts in the glomeruli and tubules of 9 Megophrys nasuta necropsied from the San Diego Zoo and Wild Animal Park, California, as routine histological studies of postmortem animals. He also reported no evidence of any significant pathology compared to normal frog kidney tissue. He indicated that the oocysts in the horned frogs suggested that they may have been coccidia.

    “Unsporulated Coccidian” of Jirku and Modrý 2006a, species inquirenda

    1. Host: Ptychadena sp. 1.
    2. In a study describing the endogenous and exogenous stages of E. terraepokotorum from Hoplobatrachus occipitalis from Kenya, Jirku and Modrý (2006a) examined 16 taxa of anurans and reported seeing unsporulated coccidian oocysts in 1 of 2 Ptychadena sp. Unfortunately, the oocysts did not sporulate and it is not clear what coccidium this was.

    INCERTAE SEDIS

    Eimeria sp. 1 (Eimer, 1870) Upton and McAllister 1988, incertae sedis

    1. Host: Pelophylax esculenta, (L. 1758 (Pool frog).
    2. No oocysts were measured or described (see Eimer 1870; Upton & McAllister 1988).

    Eimeria sp. of Fantham and Porter 1947, incertae sedis

    1. Host: Lithobates clamitans (Latreille In Sonnini de Manoncourt & Latreille 1801)(Green frog).
    2. Fantham and Porter (1947) collected 1 Necturus maculosus, 1 Anaxyrus americanus, 5 L. catesbeianus, 3 L. pipiens, and 3 L. clamitans from Lad Des Sableets, north-west of Montreal, Canada and reported seeing a few Eimeria oocysts in a single female green frog without giving any description of the oocysts.

    Eimeria sp. of Hegner and Chu 1930, incertae sedis

    1. Host: Fejervarya vittigera (Wiegmann 1834) (Luzon wart frog).
    2. The report of Hegner and Chu (1930) is of an unidentified coccidium in F. vittigera from the Philippines; it is not complete enough, and makes this species of Eimeria of uncertain taxonomic position.

    Eimeria sp. 2 (Pachinger 1886) Upton and McAllister 1988, incertae sedis

    1. Synonym: Molybdis entzii Pachinger 1886.
    2. Host: Pelophylax esculenta, (L. 1758) (Pool frog).
    3. Mention was made only of an ovoidal oocyst, 30 x 13.

    Isospora sp. of Chakravarty and Kar 1944, incertae sedis

    1. Synonym: Eimeria wenyoni Ray and Das Gupta, 1935 of Chakravarty and Kar 1944.
    2. Hosts: Fejervarya limnocharis (Gravenhorst 1829) (Indian cricket frog); Hoplobatrachus tigerinus (Daudin 1802) (Tiger frog).
    3. See Remarks in Isospora wenyoni.

    Isospora sp. of Grassi, 1882, incertae sedis.

    1. Host: Bufo spp. (?).
    2. Mention has been made of an isosporan in Bufo spp. (?) by a number of authors (Grassi 1882; Grassi & Feletti 1892; Labbé 1899; Walton 1941), but little else is known about it.

    Isospora sp. of Kazubski and Grabda-Kazubska 1973, incertae sedis

    1. Host: Rana arvalis Nilsson 1842 (Moor frog).
    2. Oocysts are subspheroidal, 21–22 x 19–20 and sporocysts are 16.2 x 12.8 (15–18.5 x 12–14.5); this species was found in Poland.

    Unsporulated oocyst 1 of Rzepczyk, 1976, incertae sedis

    1. Host: Chaunus (=Bufo) marinus (L. 1758) (Cane toad).
    2. Rzepczyk (1976) mentioned seeing 1 spheroidal, unsporulated oocyst in the intestinal contents of a cane toad, C. marinus.

    Unsporulated oocyst 2 of Rzepczyk 1976, incertae sedis

    1. Host: Chaunus (=Bufo) marinus (L. 1758), (Cane toad).
    2. Rzepczyk (1976) found what she said was a subspheroidal unsporulated oocyst, 28 x 26.6, in the intestinal contents of a second cane toad C. marinus.

    Unsporulated oocyst 3 of Rzepczyk 1976, incertae sedis

    1. Host: haunus (=Bufo) marinus (L. 1758) (Cane toad).
    2. Rzepcyzk (1976) found 2 unsporulated oocysts of a third coccidium in the intestinal contents of a third cane toad, C. marinus. These were 28 x 28 and 26.6 x 23.6 and were were similar to her unsporulated oocyst 2, but neither sporulated.

    Unsporulated oocyst 4 of Rzepczyk 1976, incertae sedis

    1. Host: Chaunus (=Bufo) marinus (L. 1758) (Cane toad).
    2. Rzepcyzk (1976) found two other oocysts in the third cane toad. The first was another unsporulated oocyst, 26.6 x 26.6, with a thick brown wall and an “elaborate” M.

    Isospora-like oocysts/sporocysts 5 of Rzepczyk 1976, incertae sedis

    1. Host: Chaunus (=Bufo) marinus (L. 1758) (Cane toad).
    2. In the third cane toad mentioned above, she also diagnosed Isospora sporocysts with four sporozoites. Sporocysts (N=12) were 19.2 x 10.0 (22–16 x 10–8), L/W of 1.9 (1.6–2.1) and with a “prominent” sporocyst wall and an ovoidal SR, 6.4 x 4.5.

    Unsporulated oocyst 6 of Rzepczyk 1976, incertae sedis

    1. Host: Litoria caerulea (White 1790) (White's treefrog).
    2. In 6 of 12 treefrogs she saw 3 distinct coccidian types, but no treefrogs had more than one type. The first morphotype she saw was an unsporulated oocyst that was heart-shaped, 39.2 x 33.6, with a thick, brown wall and an “elaborate” M. She only saw 2 oocysts in 1 frog.

    Unsporulated oocyst 7 of Rzepczyk 1976, incertae sedis

    1. Host: Litoria caerulea (White 1790) (White's treefrog).
    2. Her second morphotype was seen in each of 3 of the 12 treefrogs examined; in these she saw 1 unsporulated oocyst; each of which was broadly ovoidal, 28 x 25.

    Isospora (?) sp. 8 of Rzepczyk 1976, incertae sedis

    1. Host: Litoria caerulea (White 1790) (White's treefrog).
    2. The third morphotype she reported in the L. caerulea she examined were spheroidal to ovoidal, colorless oocysts that sporulated in 6 days in K2Cr2O7. She identified these oocysts as being an Isospora sp. that measured 16.8–20.7 x 14.0–16.8. This form was found in only 2 frogs with “only 1–4 oocysts in the total rectal contents of each frog.”

    Isospora sp. of Wenyon 1926, incertae sedis

    1. Host: Bufo bufo (L. 1758) (Common European toad).
    2. Endogenous sporulation in epithelial cells of the intestine.

    NOMENA NUDA

    Eimeria pylori (Gebhardt, 1897) Levine and Becker, 1933, nomen nudum

    1. Synonym: Coccidium pylori Gebhardt, 1897
    2. Host: Rana sp.(?)
    3. No oocysts were measured or described (see Gebhardt 1897; Levine & Becker 1933; Walton 1941, 1949c).

    Isospora ranae (Rivolta, 1878) Dobell, 1909 of Walton, 1941, nomen nudum

    1. Synonym: Cytospermium ranae Rivolta, 1878
    2. Host: Rana esculenta (Green frog)
    3. No oocysts were measured or described (see Dobell 1909; Pellérdy 1974; Rivolta 1878; Walton 1941).



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