Helminths of the bullfrog, Rana catesbeiana (Ranidae), in California with revisions to the California anuran helminth list.
Abstract.--Thirty-one bullfrogs, Rana cateshejana, from northern California were examined for helminths. Gravid individuals representing three species of Trematoda, Glypthelmins quieta, Haematoloechus longiplexus and Megalodiscus ternperatus; one species of Cestoda, Ophiotaenia magna; and three species of Nematoda, Cosmocerco ides variabilis, Falcaustra catesbeianae and Oswaldocruzia pipiens were found. Larvae representing three species of Nematoda, Contracaecurn sp., Eustrongylides sp., and Physaloptera sp. were also found. Rana catesbeiana is parasitized by generalist helminths that occur in other frogs and have previously been found in R. catesbeiana in other parts of North America. This is the first report of Falcaustra catesbeianae, Contracaecum sp. and Eustrongylides sp. from California anurans. The helminth host list for California anurans is revised.**********
The bullfrog, Rana catesbeiana was first described from a collection taken in the vicinity of Charleston, South Carolina (Shaw, 1802). The original range covered most of eastern North America from the mouth of the Pecos River, Texas through the Panhandles of Texas and Oklahoma, extreme western Kansas, Nebraska and Minnesota, eastward to Maine and the northern half of Florida (Wright and Wright 1995). Subsequently, the bullfrog was introduced into each of the western states as well as Mexico and British Columbia, Canada (Stebbins 1985). In California, bullfrogs were first introduced in 1896 (Heard 1904) for human food after populations of native frogs, particularly the red-legged frog, Rana aurora, were overharvested (Jennings and Hayes 1985). Introductions and subsequent range expansions of the bullfrog have coincided with declines of native ranid frogs in western North America which has in turn generated interest in frog population ecology and competition (Kiesecker and Blaustein 1997; Kupferberg 1997; Lawl er et al. 1999). However, little attention has been given to helminths of introduced frogs. To our knowledge, there are four reports of helminths in California bullfrogs (Ingles 1936; Nicol et al. 1985; Shields 1987; Wootton et al. 1993). Helminths of the bullfrog in North America have been summarized by Andrews et al. (1992). Additional helminths are listed in Bursey and DeWolf (1998), Goldberg et al. (1998) and McAlpine and Burt (1998). The purpose of this paper is to report additional helminths of California bullfrogs and to revise the helminth list for California anurans.
Methods
Thirty-one bullfrogs collected in 1997 and 1998 from northern California were examined for helminths. All frogs were deposited in the herpetology collection of the Natural History Museum of Los Angeles County (LACM) after examination. Sixteen frogs (LACM 144342-144357) were from Upper Searsville Lake, Jasper Ridge Biological Preserve, Woodside, San Mateo County (37[degrees]30'N, 122[degrees]30'W); 15 frogs (LACM 146746-146751, 146753, 146754, 146756-146762) were from sites between Uvas and Calero Reservoirs, Santa Clara County (37[degrees]05'N, 121[degrees]45'W). The frogs were initially fixed in 10% formalin and preserved in 70% ethanol. The body cavity was opened by a longitudinal incision from throat to pelvis and the gastrointestinal tract, lungs and urinary bladder were removed. Each organ was opened and examined for helminths under a dissecting microscope. The surface of the liver and the body cavity were also searched. Nematodes were placed on a microscope slide and cleared in glycerine. A coyerslip wa s added to the slide and the nematode was identified using a compound microscope. Cestodes and trematodes were rehydrated, stained in hematoxylin, dehydrated in a series of graded ethanols, cleared in xylene, mounted on a glass slide in Canada balsam and identified using a compound microscope.
Three similarity indices were calculated in order to compare the R. catesbeiana helmiaths from San Mateo and Santa Clara Counties. The Jaccard coefficient is based on species presence in a community and ranges from 0 (no species in common) to 1.0 (all species in common); Morisita's index considers number of species, number of individuals, and proportion of the total represented by each species and ranges from 0 (no similarity) to 1.0 (identical); percent similarity is based on species abundance and ranges from 0 (no similarity) to 100 (same species found in both communities at similar abundances) (Brower et al. 1997).
Results
Gravid individuals of three species of Trematoda, Glyptheimins quieta (Stafford, 1900), Haematoloechus ion giplexus Stafford 1902, Megalodiscus temperatus (Stafford, 1905); one species of Cestoda, Ophiotaenia magna Hannum, 1925; and three species of Nematoda, Cosmocercoides variabilis (Harwood, 1930), Falcaustra catesbeianae Walton, 1929, Oswaldocruzia pipiens Walton, 1929, were found. Larvae representing three species of Nematoda, Contracaecum sp., Eustrongylides sp., and Physaloptera sp. were also found. Prevalence (percent of sample infected) and mean intensity (mean number of helminths per infected frog [+ or -] 1 SD) by helminth species are given in Table 1.
The helminths exhibited site specific infections: Glypthelmins quieta, Ophictaenia magna, Cosmocerco ides variabilis and Oswaldocruzia pipiens were found in the small intestine, Megalodiscus temperatus and Falcaustra catesbeianae in the large intestine, and Haematoloechus longiplexus in the lungs. Larvae of Contracaecum sp., and Eustrongylides sp. were found in cysts within the body cavity and most often attached to the mesenteries; larvae of Physaloptera sp. were found within the lumen of the stomach. In no cases did two parasite species occupy the same site in a single host.
Selected helminths were deposited in the United States National Parasite Collection, USNPC, Beltsville, Maryland 20705 as: Glypthelmins quieta (91248),
Haematoloechus Ion giplexus (91244), Megalodiscus temperatus (91245), Ophiotaenia magna (91249), Cosmocercoides variabilis (91250), Falcaustra catesbeianae (91246), Oswaldocruzia pipiens (91251), Contracaecum sp. (91247), Eustrongylides sp. (91252), Physaloptera sp. (91253).
Discussion
All helminths found in this study have previously been reported from Rana catesbeiana in other parts of its range as well as from other ranids (Dyer 1991; Andrews et al. 1992). However, this is the first report of Falcaustra catesbeianae, Contracaecum sp. (larvae) and Eustrongylides sp. (larvae) from California anurans (Table 2).
Glypthelmins quieta, Haematoloechus ion giplexus and Megalodiscus temperatus are common trematode parasites of North American frogs (Smyth and Smyth 1980). These three species require a molluscan first intermediate host. After release from the molluscan host, cercariae of Glypthelmins quieta and Megalodiscus temperatus penetrate the skin of anurans and encyst beneath the epidennis. Infection occurs when a frog ingests its own cast skin after molting. Cercariae of Haematoloechus ion giplexus penetrate and encyst in naiads of dragonflies; infection occurs through ingestion of dragonflies (Smyth and Smyth 1980). The host list for Glypthelmins quieta includes five genera of anurans, Acris, Bufo, Hyla, Pseudacris and Rana; for Huematoloechus ion giplexus, two genera, Bufo and Rana; for Megalodiscus temperatus, four genera of anurans, Bufo, Hyla, Pseudacris, and Rana, five genera of Caudata, Ambystoma, Amphiuma, Desmognathus, Notophthalmus and Pseudotriton, and one genus of Serpentes, Coluber (Parker 1941; Catalano et al. 1982; Prudhoe and Bray 1982).
There is some confusion surrounding the identity of North American ranid proteocephalid cestodes; four have been reported, namely, Ophiotaenia magna, Ophiotaenia saphena Osler, 1931, Crepidobothrium olor Ingles, 1936 and Ophiotaenia gracilis Jones, Cheng and Gillespie, 1958. Brooks (1978) discussed morphological characteristics of these species and concluded no significant morpho logical differences existed between them. He did not place them in synonymy but assigned all to Proteocephalus. More recently, Schmidt (1986) assigned these species to Ophiotaenia. Since it is not possible to distinguish these four species and because we can find no difference between individuals collected in California and Ohio (see Bursey and DeWolf 1998), we have assigned our specimens to Ophiotaenia magna which has priority. In addition, we have referred all California ranid proteocephalids to Ophiotaenia magna (Table 2).
Cosmocerco ides variabilis, Falcaustra catesbeianae and Oswaldocruzia pipiens are common nematode parasites of North American frogs (Baker 1987). Like the trematodes found in this study, these nematodes are generalists, i.e., found in more than one host. However, some uncertainty exists for hosts of North American species of Cosmocercoides. Cosmocercoides variabilis, originally described as Oxysomatium variabilis by Harwood (1930) from Bufo valliceps collected at Houston, Texas was considered a synonym of the molluscan parasite Cosmocercoides dukae by Ogren (1953, 1959) who presumed that amphibians acquired C. dukae infections by ingesting infected molluscs. Cosmocercoides dukae was first described as Cosmocerca dukae by Holl (1928) from Triturus yindescens collected in North Carolina. Wilkie (1930) established the genus Cosmocercoides, and Travassos (1931) included both C. dukae and C. variabilis in his .monograph on the Cosmocercidae. Vanderburgh and Anderson (1987) demonstrated that these two species of Co smocercoides are distinct. The major difference between the two species is the number of rosette papillae of the male; C. dukae with 12 pairs; C. variabilis with 14 to 20. Specimens collected in this study exhibited 16-18 rosette papillae. The host list for C. variabilis includes the five genera of anurans, Bufo, Gastrophryne, Hyla, Pseudacris, Rana, two genera of Caudata, Ambystoma, Notophthalmus; two genera of lizards, Scincella, Ophisaurus; three of snakes, Heterodon, Micrurus, Storeria; and one of tortoises, Terrapene (Baker 1987). Ingles (1936) reported C. dukae from Taricha torosa, Rana aurora and Bufo boreas from California but illustrated 16 papillae and for this reason we have referred his specimens to Cosmocerco ides variabilis (Table 2). Falcaustra catesbeianae has been reported from four genera of Anura, namely, Gastrophryne, Hyla, Pseudacris, Rana, and two genera of Caudata, Siren and Typhlotriton (Baker 1987). All North American specimens of the genus Oswaldocruzia have been referred to 0. pipie ns by Baker (1977). This species is widely distributed in North America and has been reported from six genera of anurans, Acris, Bufo, Hyla, Pseudacris, Rana, Scaphiopus; three of Caudata, Desmognathus, Eurycea, Plethodon, seven genera of lizards, Anolis, Eumeces, Elgaria, Gerrhonotus, Heloderma, Sceloporus, Scincella; and one of tortoises, Terrapene (Baker 1987; Goldberg and Bursey 1991).
Three species of nematodes not reaching maturity in frogs were present: Contracaecum sp., Eustrongylides sp. and Physaloptera sp. Species of these genera require intermediate hosts: Contracaecum, aquatic invertebrates; Eustrongylides, aquatic oligochaetes; Physaloptera, terrestrial insects (Anderson 2000). The definitive hosts of species of Contracaecum are piscivorous birds and aquatic mammals, species of Eustrongylides are limited to piscivorous birds, and species of Physaloptera parasitize mammals, birds and reptiles (Anderson 2000). Because individuals of Contracaecum and Eustrongylides were found in cysts, the possibility of Rana catesbeiana as a paratenic host must be considered. The absence of Physaloptera in cysts suggests that they are taken with insect prey but cannot establish infection and are soon excreted.
Interestingly, of the ten species of helminths found in this study, only two trematodes, Glypthelmins quieta and Haematoloechus longiplexus were found at both locations of bullfrog collections. The 16 bullfrogs from San Mateo harbored 94 individuals representing 5 helminth species; 15 bullfrogs from Santa Clara harbored 67 individuals representing seven helminth species. The calculated results for Jaccard coefficient, Morisita's index and percent similarity were 0.2, 0.7, 47.9, respectively, indicating that the helminth communities harbored by the two bullfrog populations were not similar in structure. Other studies of California anurans (see Koller and Gaudin 1977; Goldberg and Bursey 2001a, 2001b) from multiple localities have reported similar results, i.e., spotty distribution of helminths for a particular host species.
The anuran helminths listed in Table 1 are generalists in that they are capable of infecting a number of hosts. Thus, it is possible that a particular host is unimportant; infection in a particular host may fluctuate from location to location, but the helminth population maintains an overall presence. Given the earlier introduction of the bullfrog to California and the later helminthological surveys (Table 2), it is not possible to determine whether bullfrogs acquired these helminths in California or transported them into the state. Neither is it possible to gauge the breadth of helminth infection for California anurans because only 8 (35%) of the 23 species of anurans known to occur in California (Stebbins 1985) have been examined for helminths. Examination of additional California anuran species must occur before the helminth community of these hosts can be assessed.
Table 1 Prevalence (as %), mean intensity [+ or -] 1 SD, and range for helminths from Rana catesbeiana from San Mateo and Santa Clara Counties, California; n = hosts examined. San Mateo County n = 16 (SVL = 109 mm [+ or -] 18 mm SD) Preva- Mean lence Intensity Range Glypthelmins quieta 6 1 -- Haematoloechus longiplexus 56 4.8 [+ or -] 5.2 1-17 Megalodiscus temperatus 56 3.2 [+ or -] 3.5 1-12 Ophiotoenia magna -- -- -- Cosmocercoides variabilis -- -- -- Falcaustra catesbeianae 50 4.3 [+ or -] 3.6 1-12 Oswaldocruzia pipiens -- -- -- Contraacaecum sp. (larvae) 38 2.3 [+ or -] 1.4 1-5 Eustrongylides sp. (larvae) -- -- -- Physaloptera sp. (larvae) -- -- -- Santa Clara County n = 15 (SVL = 153 mm [+ or -] 17 mm SD) Preva- Mean lence Intensity Range Glypthelmins quieta 7 12 -- Haematoloechus longiplexus 49 3.7 [+ or -] 5.1 1-17 Megalodiscus temperatus -- -- -- Ophiotoenia magna 20 1 [+ or -] 0 -- Cosmocercoides variabilis 7 2 -- Falcaustra catesbeianae -- -- -- Oswaldocruzia pipiens 7 6 -- Contraacaecum sp. (larvae) -- -- -- Eustrongylides sp. (larvae) 20 1 [+ or -] 0 -- Physaloptera sp. (larvae) 20 2.7 [+ or -] 1.5 1-4 Table 2 Helminths of California Anura. Helminth County Trematoda Alaria mustelae Bosma, 1931 Hyla regilla Santa Clara Alaria sp. (mesocercaria) Hyla cadaverina Riverside Hyla regilla Santa Clara Brachycoelium lynchi Ingles, 1935 Rana aurora Siskiyou Cephalogonimus americanus Stafford, 1902 = Cephalogonimus brevicirrus Ingles, 1932 = Cephalogonimus retusus of Walton, 1938 Rana aurora Kern Rana aurora Kern Clinostomum sp. (metacercaria) Hyla regilla Humboldt, Santa Clara Rana aurora not given Rana boylii not given Fibricola sp. (metacercaria) Hyla cadaverina Los Angeles Glypthelmins sp. Bufo boreas Los Angeles Glypthelmins quieta (Stafford, 1900) Stafford, 1905 = Distomum quietum Stafford, 1900 = Margeana californiensis Cort, 1919 = Glypthelmins californiensis (Cort, 1919) Miller, 1930 = Glypthelmins subtropica Harwood, 1932 Rana aurora referred by Sullivan, 1976 San Francisco Rana aurora referred by Sullivan, 1976 San Diego, Butte Rana boylii referred by Sullivan, 1976 Butte Rana boylii referred by Sullivan, 1976 Marin, Sonoma Rana catesbeiana San Mateo, Santa Clara Glypthelmins shastai Ingles, 1935 Bufo boreas Shasta Gorgoderina sp. Bufo boreas Siskyou Hyla cadaverina Los Angeles, Orange Rana aurora Kern Gorgoderina aurora Ingles, 1935 Rana aurora San Francisco, San Joaquin Gorgoderina multilobata Ingles and Langston, 1933 Rana aurora Los Angeles Rana aurora Butte Rana boylii Butte Rana boylii Butte Rana pretiosa Butte Gyrodactylus catesbeianae Wootton, Ryan, Demaree and Critchfield, 1993 Rana catesbejana (tadpoles) Glenn Haematoloechus sp. Rana aurora Kern Rana aurora Marin, Sonoma Rana boylii Mario, Sonoma Haematoloechus complexus (Seely, 1906) Yamaguti, 1958 = Pneumonoeces complexus Seely, 1906 = Hoematoloechus confusus Ingles, 1932 = Hoematoloechus oxyorchis Ingles, 1932 = Ostiolum oxyorchis (Ingles, 1932) Ingles, 1936 Rana aurora San Francisco Rana aurora Los Angeles Rana aurora San Francisco Haematoloechus kernensis Ingles, 1932 = Haematoloechus tumidus Ingles, 1932 Bufo boreas San Bernardino Rana aurora Kern Rana aurora Kern Haematoloechus longiplexus Stafford, 1902 Rana catesbeiana Ventura Rana catesbeiana San Mateo, Santa Clara Haematoloechus variplexus Stafford, 1902 = Hoematoloechus buttensis Ingles, 1936 Rana boylii Butte Halipegus aspina Ingles, 1932 Rana boylii Butte Rana boylli Marin, Sonoma Langeronia burseyi Dailey and Goldberg, 2000 Hyla cadaverina Orange Hyla cadaverina Orange Levinseniella ophidea Nicol, Demaree and Wootton, 1985 Rana catesbeiana Lassen Megalodiscus microphagus Ingles, 1936 Bufo boreas Shasta Megalodiscus temperatus (Stafford, 1905) Yamaguti, 1958 Rana boylii Marin, Sonoma Rana catesbeiana Butte Rana catesbeiana San Mateo Ribeiroia sp. (metacercaria) Bufo boreas Santa Clara Hyla regilla Santa Clara Rana catesbeiana Santa Clara Cestoda Cylindrotaenia americana Jewell, 1916 Bufo canorus Mariposa Distoichometra bufonis Dickey, 1921 Bufo boreas referred by Goldberg Los Angeles et al., 1999 Bufo boreas Los Angeles, San Bernardino Hyla cadaverina Riverside Hyla regilla referred by Goldberg Los Angeles et al., 1999 Hyla regilla Santa Clara Ophiotaenia magna Hannum, 1925 = Ophiotaenia saphena Osler, 1931 = Crepidobothrium olor Ingles, 1936 = Ophiotaenia gracilis Jones, Cheng and Gillespie , 1958 Rana aurora Alameda Rana catesbeiana Santa Clara Unidentified dilepinid Rana boylii Siskiyou Nematoda Aplectana itzocanensis Bravo Hollis, 1943 Bufo boreas Orange, Riverside, San Bernardino Contracaecum sp. (larvae) Rana catesbeiana San Mateo Cosmocercoides variabilis (Harwood, 1930) Travassos, 1931 = Cosmocerca dukae Holl, 1928 (in part) = Oxysomatium americana Walton, 1929 = Oxysomatium variables Harwood, 1930 Bufo boreas referred by Goldberg Shasta et al., 1999 Bufo boreas referred by Goldberg Los Angeles et al., 1999 Bufo boreas Riverside Bufo canorus Mariposa Hyla regilla referred by Goldberg Los Angeles et al., 1999 Rana aurora referred by Goldberg Butte et al., 1999 Rana catesbeiana Kern Rana catesbeiana Santa Clara Eustrongylides sp. (larvae) Rana catesbeiana Santa Clara Falcaustra catesbeianae Walton, 1929 Rana catesbeiana San Mateo Falcaustra inglisi (Anderson, 1964) Baker, 1980 = Oxysomatium inglisi Anderson, 1964 Bufo boreas Los Angeles Falcaustra pretiosa (Ingles, 1935) Freitas and Lent, 1941 = Spironoura pretiosa Ingles, 1935 Bufo boreas Inyo Rana aurora Santa Clara Rana boylii Tuolumne Rana pretiosa Plumas Falcaustra ranae (Walton, 1941) Chabaud and Golvan, 1957 = Spironoura ranae Walton, 1941 Rana boylii Mariposa Oswaldocruzia pipiens Walton, 1929 = Oswaldocruzia waltoni Ingles, 1935 Bufo boreas Butte, Kern, San Diego Bufo boreas referred by Goldberg Los Angeles et al., 1999 Bufo boreas Los Angeles, Riverside Hyla regilla referred by Goldberg Los Angeles et al., 1999 Hyla regilla Santa Clara, Imperial, Los Angeles, Orange, Riverside Rana aurora Butte, Kern, San Diego Rana catesbeiana Santa Clara Physaloptera sp. (larvae) Bufo boreas Orange Hyla cadaverina Los Angeles, Orange Hyla regilla Orange Rana catesbejana Santa Clara Rhabidas sp. Bufo boreas not given Bufa boreas Los Angeles Hyla regilla Los Angeles Rana boylii not given Rana boylii Marin, Sonoma Rhabdias americanus Baker, 1978 Bufo boreas San Bernardino Rhabdias joaquinensis Ingles, 1935 Rana aurora San Joaquin Rhabdias ranae Walton, 1929 Hyla cadaverina Los Angeles, Riverside Hyla regilla Orange, Riverside Helminth Reference Trematoda Alaria mustelae Bosma, 1931 Hyla regilla Johnson et al. 1999 Alaria sp. (mesocercaria) Hyla cadaverina Goldberg and Bursey 2001 (a) Hyla regilla Goldberg and Bursey 2001 (b) Brachycoelium lynchi Ingles, 1935 Rana aurora Ingles 1936 Cephalogonimus americanus Stafford, 1902 = Cephalogonimus brevicirrus Ingles, 1932 = Cephalogonimus retusus of Walton, 1938 Rana aurora Ingles 1932 (a) Rana aurora Ingles 1936 Clinostomum sp. (metacercaria) Hyla regilla Goldberg and Bursey 2001 (a) Rana aurora Ingles 1936 Rana boylii Ingles 1936 Fibricola sp. (metacercaria) Hyla cadaverina Goldberg and Bursey 2001 (a) Glypthelmins sp. Bufo boreas Koller and Gaudin 1977 Glypthelmins quieta (Stafford, 1900) Stafford, 1905 = Distomum quietum Stafford, 1900 = Margeana californiensis Cort, 1919 = Glypthelmins californiensis (Cort, 1919) Miller, 1930 = Glypthelmins subtropica Harwood, 1932 Rana aurora referred by Sullivan, 1976 Cort 1919 Rana aurora referred by Sullivan, 1976 Ingles 1936 Rana boylii referred by Sullivan, 1976 Ingles 1936 Rana boylii referred by Sullivan, 1976 Lehmann 1960 Rana catesbeiana this study Glypthelmins shastai Ingles, 1935 Bufo boreas Ingles 1936 Gorgoderina sp. Bufo boreas Ingles 1936 Hyla cadaverina Goldberg and Bursey 2001a Rana aurora Ingles 1932a Gorgoderina aurora Ingles, 1935 Rana aurora Ingles 1936 Gorgoderina multilobata Ingles and Langston, 1933 Rana aurora Ingles and Langston 1933 Rana aurora Ingles 1936 Rana boylii Ingles and Langston 1933 Rana boylii Ingles 1936 Rana pretiosa Ingles 1936 Gyrodactylus catesbeianae Wootton, Ryan, Demaree and Critchfield, 1993 Rana catesbejana (tadpoles) Wootton, et al. 1993 Haematoloechus sp. Rana aurora Ingles 1932a Rana aurora Lehmann 1960 Rana boylii Lehmann 1960 Haematoloechus complexus (Seely, 1906) Yamaguti, 1958 = Pneumonoeces complexus Seely, 1906 = Hoematoloechus confusus Ingles, 1932 = Hoematoloechus oxyorchis Ingles, 1932 = Ostiolum oxyorchis (Ingles, 1932) Ingles, 1936 Rana aurora Ingles 1932b Rana aurora Ingles 1933 Rana aurora Ingles 1936 Haematoloechus kernensis Ingles, 1932 = Haematoloechus tumidus Ingles, 1932 Bufo boreas Goldberg et al. 1999 Rana aurora Ingles 1932b Rana aurora Ingles 1936 Haematoloechus longiplexus Stafford, 1902 Rana catesbeiana Shields 1987 Rana catesbeiana this study Haematoloechus variplexus Stafford, 1902 = Hoematoloechus buttensis Ingles, 1936 Rana boylii Ingles 1936 Halipegus aspina Ingles, 1932 Rana boylii Ingles 1936 Rana boylli Lehmann 1960 Langeronia burseyi Dailey and Goldberg, 2000 Hyla cadaverina Dailey and Goldberg 2000 Hyla cadaverina Goldberg and Bursey 2001a Levinseniella ophidea Nicol, Demaree and Wootton, 1985 Rana catesbeiana Nicol et al. 1985 Megalodiscus microphagus Ingles, 1936 Bufo boreas Ingles 1936 Megalodiscus temperatus (Stafford, 1905) Yamaguti, 1958 Rana boylii Lehmann 1960 Rana catesbeiana Ingles 1936 Rana catesbeiana this study Ribeiroia sp. (metacercaria) Bufo boreas Johnson et al. 1999 Hyla regilla Johnson et al. 1999 Rana catesbeiana Johnson et al. 1999 Cestoda Cylindrotaenia americana Jewell, 1916 Bufo canorus Walton 1941 Distoichometra bufonis Dickey, 1921 Bufo boreas referred by Goldberg Koller and Gaudin 1977 et al., 1999 Bufo boreas Goldberg et al. 1999 Hyla cadaverina Goldberg and Bursey 2001 (a) Hyla regilla referred by Goldberg Koller and Gaudin 1977 et al., 1999 Hyla regilla Goldberg and Bursey 2001 (b) Ophiotaenia magna Hannum, 1925 = Ophiotaenia saphena Osler, 1931 = Crepidobothrium olor Ingles, 1936 = Ophiotaenia gracilis Jones, Cheng and Gillespie , 1958 Rana aurora Ingles 1936 Rana catesbeiana this paper Unidentified dilepinid Rana boylii Ingles 1936 Nematoda Aplectana itzocanensis Bravo Hollis, 1943 Bufo boreas Goldberg et al. 1999 Contracaecum sp. (larvae) Rana catesbeiana this study Cosmocercoides variabilis (Harwood, 1930) Travassos, 1931 = Cosmocerca dukae Holl, 1928 (in part) = Oxysomatium americana Walton, 1929 = Oxysomatium variables Harwood, 1930 Bufo boreas referred by Goldberg Ingles 1936 et al., 1999 Bufo boreas referred by Goldberg Koller and Gaudin 1977 et al., 1999 Bufo boreas Goldberg et al. 1999 Bufo canorus Walton 1941 Hyla regilla referred by Goldberg Koller and Gaudin 1977 et al., 1999 Rana aurora referred by Goldberg Ingles 1936 et al., 1999 Rana catesbeiana Ingles 1936 Rana catesbeiana this study Eustrongylides sp. (larvae) Rana catesbeiana this study Falcaustra catesbeianae Walton, 1929 Rana catesbeiana this study Falcaustra inglisi (Anderson, 1964) Baker, 1980 = Oxysomatium inglisi Anderson, 1964 Bufo boreas Goldberg et al. 1999 Falcaustra pretiosa (Ingles, 1935) Freitas and Lent, 1941 = Spironoura pretiosa Ingles, 1935 Bufo boreas Walton 1941 Rana aurora Walton 1941 Rana boylii Walton 1941 Rana pretiosa Ingles 1936 Falcaustra ranae (Walton, 1941) Chabaud and Golvan, 1957 = Spironoura ranae Walton, 1941 Rana boylii Walton 1941 Oswaldocruzia pipiens Walton, 1929 = Oswaldocruzia waltoni Ingles, 1935 Bufo boreas Ingles 1936 Bufo boreas referred by Goldberg Koller and Gaudin 1977 et al., 1999 Bufo boreas Goldberg et al. 1999 Hyla regilla referred by Goldberg Koller and Gaudin 1977 et al., 1999 Hyla regilla Goldberg and Bursey 2001b Rana aurora Ingles 1936 Rana catesbeiana this study Physaloptera sp. (larvae) Bufo boreas Goldberg et al. 1999 Hyla cadaverina Goldberg and Bursey 2001a Hyla regilla Goldberg and Bursey 2001b Rana catesbejana this study Rhabidas sp. Bufo boreas Ingles 1936 Bufa boreas Koller and Gaudin 1977 Hyla regilla Koller and Gaudin 1977 Rana boylii Ingles 1936 Rana boylii Lehmann 1960 Rhabdias americanus Baker, 1978 Bufo boreas Goldberg et al. 1999 Rhabdias joaquinensis Ingles, 1935 Rana aurora Ingles 1936 Rhabdias ranae Walton, 1929 Hyla cadaverina Goldberg and Bursey 2001a Hyla regilla Goldberg and Bursey 2001b
Acknowledgment
Pieter T. J. Johnson (Stanford University) collected the sample of Rana catesbeiana.
Accepted for publication 11 October 2001.
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| Author: | Goldberg, Stephen R.; Bursey, Charles R. |
|---|---|
| Publication: | Bulletin (Southern California Academy of Sciences) |
| Geographic Code: | 1U9CA |
| Date: | Dec 1, 2002 |
| Words: | 4884 |
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