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First Evidence of Batrachochytrium dendrobatidis in China: Discovery of Chytridiomycosis in Introduced American Bullfrogs and Native Amphibians in the Yunnan Province, China

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Abstract

Although the chytrid fungus Batrachochytrium dendrobatidis (Bd), the etiological agent of amphibian chytridiomycosis, has been implicated in mass mortality and population declines on several continents around the world, there have been no reports on the presence of Bd infections in amphibians in China. We employed quantitative PCR and histological techniques to investigate the presence of Bd in introduced North American bullfrogs (Rana catesbeiana) (referred to hereafter as bullfrog) and native amphibians in bullfrog-invaded areas of the Yunnan Province, China. A total of 259 samples at five wild sites were collected between June and September in 2007 and 2008, including bullfrogs and four native amphibian species (Rana pleuraden, Rana chaochiaoensis, Odorrana andersonii, and Bombina maxima). In addition, 37 samples of adult bullfrogs were obtained from a food market. Bd infections were discovered in bullfrogs and three native amphibian species from all of the surveyed sites. Of the 39 Bd-positive samples, 35 were from wild-caught bullfrog tadpoles, postmetamorphic bullfrogs, R. pleuraden, R. chaochiaoensis, and O. andersonii, and four were from adult bullfrogs from the market. Our results provide the first evidence of the presence of Bd in Chinese amphibians, suggesting that native amphibian diversity in China is at risk from Bd. There is an urgent need to monitor the distribution of Bd in amphibians in China and understand the susceptibility of native amphibian species to chytridiomycosis. Strict regulations on the transportation of bullfrogs and the breeding of bullfrogs in markets and farms should be drafted in order to stop the spread of Bd by bullfrogs.

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References

  • Berger L, Speare R, Daszak P, Green DE, Cunningham AA, Goggin CL, et al. (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proceedings of the National Academy of Sciences of the United States of America 95:9031–9036

    Article  CAS  Google Scholar 

  • Berger L, Speare R, Kent A (1999) Diagnosis of chytridiomycosis in amphibians by histologic examination. Zoo’s Print Journal 15:184–190

    Google Scholar 

  • Bielby J, Cooper N, Cunningham AA, Garner TWJ, Purvis A (2008) Predictors of rapid decline in frog species. Conservation Letters 1:80–90

    Article  Google Scholar 

  • Blaustein AR, Romansic JM, Scheessele EA, Han BA, Pessier AP, Longcore JE (2005) Interspecific variation in susceptibility of frog tadpoles to the pathogenic fungus Batrachochytrium dendrobatidis. Conservation Biology 19:1460–1468

    Article  Google Scholar 

  • Bosch J, Martínez-Solano I, García-París M (2001) Evidence of a chytrid fungus infection involved in the decline of the common midwife toad (Alytes obstetricans) in protected areas of central Spain. Biological Conservation 97:331–337

    Article  Google Scholar 

  • Boyle DG, Boyle DB, Olsen V, Morgan JAT, Hyatt AD (2004) Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Diseases of Aquatic Organisms 60:141–148

    Article  CAS  Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2003) Infectious disease and amphibian population declines. Diversity and Distributions 9:141–150

    Article  Google Scholar 

  • Daszak P, Strieby A, Cunningham AA, Longcore JE, Brown CC, Porter D (2004) Experimental evidence that the bullfrog (Rana catesbeiana) is a potential carrier of chytridiomycosis, an emerging fungal disease of amphibians. Herpetological Journal 14:201–207

    Google Scholar 

  • Daszak P, Schloegal L, Maranda L, Cronin A, Pokras M, Smith K, et al. (2006) The Global Trade in Amphibians: Summary Interim Report of a CCM Study, New York: Consortium for Conservation Medicine

    Google Scholar 

  • David S, Sheridan JA, Jiraungkoorskul W, Khonsue W (2008) A survey for chytrid fungus in Thai amphibians. The Raffles Bulletin of Zoology 56:199–204

    Google Scholar 

  • Fisher MC, Garner TWJ (2007) The relationship between the emergence of Batrachochytrium dendrobatidis, the international trade in amphibians and introduced amphibian species. Fungal Biology Reviews 21:2–9

    Article  Google Scholar 

  • Garner TWJ, Walker S, Bosch J, Hyatt AD, Cunningham AA, Fisher MC (2005) Chytrid fungus in Europe. Emerging Infectious Diseases 11:1639–1641

    Google Scholar 

  • Garner TWJ, Perkins MW, Govindarajulu P, Seglie D, Walker S, Cunningham AA, et al. (2006) The emerging amphibian pathogen Batrachochytrium dendrobatidis globally infects introduced populations of the North American bullfrog, Rana catesbeiana. Biology Letters 2:455–459

    Article  Google Scholar 

  • Hanselmann R, Rodriguez A, Lampo M, Fajardo-Ramos L, Aguirre AA, Kilpatrick AM, et al. (2004) Presence of an emerging pathogen of amphibians in introduced bullfrogs Rana catesbeiana in Venezuela. Biological Conservation 120:115–119

    Article  Google Scholar 

  • Houlahan JE, Findley CS, Schmidy BR, Meyer AH, Kuzmin SL (2000) Quantitative evidence for global amphibian declines. Nature 404:752–755

    Article  CAS  Google Scholar 

  • Hyatt AD, Boyle DG, Olsen V, Boyle DB, Berger L, Obendorf D, et al. (2007) Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 73:175–192

    Article  CAS  Google Scholar 

  • International Union for Conservation of Nature and Natural Resources (IUCN) (2008) 2008 IUCN Red List of Threatened Species. www.iucnredlist.org/details/54815. Accessed March 6, 2009

  • Kriger KM, Hines HB, Hyatt AD, Boyle DG, Hero JM (2006) Techniques for detecting chytridiomycosis in wild frogs: comparing histology with real-time Taqman PCR. Diseases of Aquatic Organisms 71:141–148

    Article  CAS  Google Scholar 

  • Kriger KM, Pereoglou F, Hero J-M (2007) Latitudinal variation in the prevalence and intensity of chytrid (Batrachochytrium dendrobatidis) infection in eastern Australia. Conservation Biology 21:1280–1290

    Article  Google Scholar 

  • Kusrini MD, Skerratt LF, Garland S, Berger L, Endarwin W (2008) Chytridiomycosis in frogs of Mount Gede Pangrango, Indonesia. Diseases of Aquatic Organisms 82:187–194

    Article  CAS  Google Scholar 

  • Li YM, Wu ZJ, Duncan RP (2006) Why islands are easier to invade: human influences on bullfrog invasion in the Zhoushan archipelago and neighboring mainland China. Oecologia 148:129–136

    Article  Google Scholar 

  • Lips KR (1999) Mass mortality and population declines of anurans at an upland site in western Panama. Conservation Biology 13:117–125

    Article  Google Scholar 

  • Lips KR, Brem F, Brenes R (2006) Emerging infectious disease and the loss of biodiversity in a neotropical amphibian community. Proceedings of the National Academy of Sciences of the United States of America 103:3165–3170

    Article  CAS  Google Scholar 

  • Liu X, Li Y (2009) Aquaculture enclosures relate to the establishment of feral populations of introduced species. PLoS ONE 4:e6199. doi: 10.1371/journal.pone.0006199

    Article  Google Scholar 

  • Liu X, Li Y, McGarrity ME (2009) Geographical variation in body size and sexual size dimorphism of introduced American bullfrogs in southwestern China. Biological Invasions. doi: 10.1007/s10530-009-9606-1

  • Longcore JE, Pessier AP, Nichols DK (1999) Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 91:219–227

    Article  Google Scholar 

  • Muths E, Pilliod DS, Livo LJ (2008) Distribution and environmental limitations of an amphibian pathogen in the Rocky Mountains, USA. Biological Conservation 141:1484–1492

    Article  Google Scholar 

  • Ouellet M, Mikaelian I, Pauli BD, Rodrigue J, Green DM (2005) Historical evidence of widespread chytrid infection in North American amphibian populations. Conservation Biology 19:1431–1440

    Article  Google Scholar 

  • Rachowicz LJ, Vredenburg VT (2004) Transmission of Batrachochytrium dendrobatidis within and between amphibian life stages. Diseases of Aquatic Organisms 61:75–83

    Article  Google Scholar 

  • Rollins-Smith LA, Woodhams DC, Reinert LK, Vredenburg VT, Briggs CJ, Nielsen PF, et al. (2006) Antimicrobial peptide defenses of the mountain yellow-legged frog (Rana muscosa). Developmental and Comparative Immunology 30:831–842

    Article  CAS  Google Scholar 

  • Rowley JJL, Chan SKF, Tang WS, Speare R, Skerratt LF, Alford RA, et al. (2007) Survey for the amphibian chytrid Batrachochytrium dendrobatidis in Hong Kong in native amphibians and in the international amphibian trade. Diseases of Aquatic Organisms 78:87–95

    Article  Google Scholar 

  • Schloegel LM, Hero JM, Berger L, Speare R, McDonald K, Daszak P (2006) The decline of the sharp-snouted day frog (Taudactylus acutirostris): the first documented case of extinction by infection in a free-ranging wildlife species? EcoHealth 3:35–40

    Article  Google Scholar 

  • Schloegel LM, Picco AM, Kilpatrick AM, Davies AJ, Hyatt AD, Daszak P (2009) Magnitude of the US trade in amphibians and presence of Batrachochytrium dendrobatidis and ranavirus infection in imported North American bullfrogs (Rana catesbeiana). Biological Conservation 142:1420–1426

    Article  Google Scholar 

  • Skerratt LF, Berger L, Hines HB, McDonald KR, Mendez D, Speare R (2008) Survey protocol for detecting chytridiomycosis in all Australian frog populations. Diseases of Aquatic Organisms 80:85–94

    Article  Google Scholar 

  • Soto-Azat C, Clarke BT, Fisher MC, Walker SF, Cunningham AA (2009) Non-invasive sampling methods for the detection of Batrachochytrium dendrobatidis in archived amphibians. Diseases of Aquatic Organisms 84:163–166

    Article  CAS  Google Scholar 

  • Stuart S, Chanson J, Cox N, Young B, Rodrigues A, Fischman D, et al. (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786

    Article  CAS  Google Scholar 

  • Walker SF, Bosch J, James TY, Litvintseva AP, Valls JAO (2008) Invasive pathogens threaten species recovery programs. Current Biology 18:R853–R854

    Article  CAS  Google Scholar 

  • Warkentin IG, Bickford D, Sodhi NS, Bradshaw CJA (2009) Eating frogs to extinction. Conservation Biology 23:1056–1059

    Article  Google Scholar 

  • Weldon C, du Preez LH, Hyatt AD, Muller R, Speare R (2004) Origin of the amphibian chytrid fungus. Emerging Infectious Diseases 10:2100–2105

    Google Scholar 

  • Woodhams DC, Vredenburg VT, Simon MA, Billheimer D, Shakhtour B, Shyr Y, et al. (2007) Symbotic bacteria contribute to innate immune defences of the threatened mountain yellow-legged frog, Rana muscosa. Biological Conservation 138:390–398

    Article  Google Scholar 

  • Yang H, Baek H, Speare R, Webb R, Park S, Kim T, et al. (2009) First detection of the amphibian chytrid fungus Batrachochytrium dendrobatidis in free-ranging populations of amphibians on mainland Asia: survey in South Korea. Diseases of Aquatic Organisms 86:9–13

    Article  Google Scholar 

  • Yumi U, Sho K, Kenichi T, Kouichi G, Toshiro K (2008) First report of spontaneous chytridiomycosis in frogs in Asia. Diseases of Aquatic Organisms 82:157–160

    Article  Google Scholar 

Download references

Acknowledgments

We thank Feng Xu, Xuan Liu, and Yu Luo for collecting samples, and Xiaoping Chen and Fanchen Meng for the use of their Quantitative-PCR equipment and Beadbeater. We are grateful to Tsai Jian and one anonymous referee for their useful comments on the manuscript. All of the collection and handling of amphibians was conducted under the approval of the Animal Care and Ethics Committee, Institute of Zoology, Chinese Academy of Sciences. This research was supported by grants from the “973” program (code: 2007CB411600) and the National Science Foundation (code: 30870312).

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Authors and Affiliations

  1. Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, 1 Beichen West Road, Chaoyang District, 100101, Beijing, China

    Changming Bai & Yiming Li

  2. Graduate School of Chinese Academy of Sciences, 19 Yuquan Road, Shijingshan, 100039, Beijing, China

    Changming Bai

  3. Institute of Zoology, Zoological Society of London, Regent’s Park, London, NW1 4RY, UK

    Trenton W. J. Garner

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  1. Changming Bai
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  2. Trenton W. J. Garner
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Correspondence to Yiming Li.

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Bai, C., Garner, T.W.J. & Li, Y. First Evidence of Batrachochytrium dendrobatidis in China: Discovery of Chytridiomycosis in Introduced American Bullfrogs and Native Amphibians in the Yunnan Province, China. EcoHealth 7, 127–134 (2010). https://doi.org/10.1007/s10393-010-0307-0

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