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      Spontaneous oral chytridiomycosis in wild bullfrog tadpoles in Japan

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          Abstract

          Batrachochytrium dendrobatidis (Bd) infects Anuran larvae (tadpole) mouthparts and causes oral chytridiomycosis, which can be diagnosed in tadpoles by detecting mouthparts deformities. However, oral chytridiomycosis may or may not be observable, depending on species, tadpole stage and season, and has never been reported in Japan. We aimed to observe oral chytridiomycosis characteristics in bullfrog ( Lithobates catesbeiana) tadpoles, determine associated pathologic features and investigate the usability of bullfrog tadpoles in Japanese Bd field surveys. Wild-captured bullfrog tadpole mouthparts were examined macroscopically, histopathologically and by molecular biological examination. Macroscopic lesions were observed in 21 of 59 tadpole mouthparts. Lesions were most frequently located in the lower jaw sheaths and were mainly recognized by partial depigmentation (11 tadpoles; some were completely depigmented) and thinning of the pigmented layer (10 tadpoles). Partial defects of the tips and blunt cutting edges of the jaw sheaths were observed with severe jaw sheath depigmentation. Whitened tooth rows were observed in 7 tadpoles. Histologically, the stratified epithelium (pigmented epithelium) showed partial or diffuse hypopigmentation or pigment loss. Irregular stratified epithelium thickening with hyperkeratosis or parakeratosis was observed in the jaw sheaths. Bd infection was confirmed in 20 of 21 tadpoles presenting jaw sheath deformities, by histopathological examination and/or nested polymerase chain reaction. Depigmentation and thinning of the pigmented layers of jaw sheaths were associated with Bd infection. Thus, diagnosis of Bd infection by macroscopic observation of bullfrog tadpole mouthparts is feasible. This is the first report of oral chytridiomycosis in wild bullfrog tadpoles in Japan.

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          Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America.

          Epidermal changes caused by a chytridiomycete fungus (Chytridiomycota; Chytridiales) were found in sick and dead adult anurans collected from montane rain forests in Queensland (Australia) and Panama during mass mortality events associated with significant population declines. We also have found this new disease associated with morbidity and mortality in wild and captive anurans from additional locations in Australia and Central America. This is the first report of parasitism of a vertebrate by a member of the phylum Chytridiomycota. Experimental data support the conclusion that cutaneous chytridiomycosis is a fatal disease of anurans, and we hypothesize that it is the proximate cause of these recent amphibian declines.
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            Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis.

            Batrachochytrium dendrobatidis is a fungus belonging to the Phylum Chytridiomycota, Class Chytridiomycetes, Order Chytridiales, and is the highly infectious aetiological agent responsible for a potentially fatal disease, chytridiomycosis, which is currently decimating many of the world's amphibian populations. The fungus infects 2 amphibian orders (Anura and Caudata), 14 families and at least 200 species and is responsible for at least 1 species extinction. Whilst the origin of the agent and routes of transmission are being debated, it has been recognised that successful management of the disease will require effective sampling regimes and detection assays. We have developed a range of unique sampling protocols together with diagnostic assays for the detection of B. dendrobatidis in both living and deceased tadpoles and adults. Here, we formally present our data and discuss them in respect to assay sensitivity, specificity, repeatability and reproducibility. We suggest that compliance with the recommended protocols will avoid the generation of spurious results, thereby providing the international scientific and regulatory community with a set of validated procedures which will assist in the successful management of chytridiomycosis in the future.
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              Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians.

              Batrachochytrium dendrobatidis is a pathogen of amphibians that has been implicated in severe population declines on several continents. We investigated the zoospore activity, physiology and protease production of B. dendrobatidis to help understand the epidemiology of this pathogen. More than 95% of zoospores stopped moving within 24 h and swam less than 2 cm before encysting. Isolates of B. dendrobatidis grew and reproduced at temperatures of 4-25 C and at pH 4-8. Growth was maximal at 17-25 C and at pH 6-7. Exposure of cultures to 30 C for 8 d killed 50% of the replicates. B. dendrobatidis cultures grew on autoclaved snakeskin and 1% keratin agar, but they grew best in tryptone or peptonized milk and did not require additional sugars when grown in tryptone. B. dendrobatidis produced extracellular proteases that degraded casein and gelatin but had no measurable activity against keratin azure. The proteases were active against azocasein at temperatures of 6-37 C and in a pH range of 6-8, with the highest activity at temperatures of 23-30 C and at pH 8. The implications of these observations on disease transmission and development are discussed.
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                Author and article information

                Journal
                J Vet Med Sci
                J. Vet. Med. Sci
                JVMS
                The Journal of Veterinary Medical Science
                The Japanese Society of Veterinary Science
                0916-7250
                1347-7439
                20 December 2015
                April 2016
                : 78
                : 4
                : 573-577
                Affiliations
                [1) ]Laboratory of Veterinary Pathology, Azabu University, 1–17–71 Fuchinobe, Chuo-ku, Sagamihara, Kanagawa 252–5201, Japan
                [2) ]Den-en-chofu Animal Hospital, 2–1–3 Denenchofu, Ota-ku, Tokyo 145–0071, Japan
                [3) ]Faculty of Education Lifelong Education Program, University of the Ryukyu, 1 Senbaru, Nishihara, Nakagami-gun,Okinawa 903–0213, Japan
                [4) ]National Institute for Environmental Studies, 16–2 Onogawa, Tsukuba, Ibaraki 305–8506, Japan
                Author notes
                [* ]Correspondence to: Une, Y., Laboratory of Veterinary Pathology, Azabu University, 1–17–71 Fuchinobe, Chuo-ku, Sagamihara, Kanagawa 252–5201, Japan. e-mail: une@ 123456azabu-u.ac.jp
                Article
                15-0486
                10.1292/jvms.15-0486
                4873846
                26685882
                2a2a912c-0dba-4c9f-bee7-4a8a5bd731a3
                ©2016 The Japanese Society of Veterinary Science

                This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial No Derivatives (by-nc-nd) License.

                History
                : 25 August 2015
                : 29 November 2015
                Categories
                Wildlife Science
                Full Paper

                bullfrog,chytridiomycosis,mouthparts,pathology,tadpole
                bullfrog, chytridiomycosis, mouthparts, pathology, tadpole

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