Retrospective Survey of Museum Specimens Reveals Historically Widespread Presence of Batrachochytrium dendrobatidis in China
- 807 Downloads
Chytridiomycosis, caused by the chytrid fungus Batrachochytrium dendrobatidis (Bd), has been implicated in amphibian population declines worldwide. However, no amphibian declines or extinctions associated with Bd have been reported in Asia. To investigate the history of this pathogen in China, we examined 1,007 museum-preserved amphibian specimens of 80 species collected between 1933 and 2009. Bd was detected in 60 individuals (6.0%), with the earliest case of Bd infection occurring in one specimen of Bufo gargarizans and two Fejervarya limnocharis, all collected in 1933 from Chongqing, southwest China. Although mainly detected in non-threatened native amphibians, Bd was also found in four endangered species. We report the first evidence of Bd for Taiwan and the first detection of Bd in the critically endangered Chinese giant salamander (Andrias davidianus). Bd appears to have been present at a low rate of infection since at least the 1930s in China, and no significant differences in prevalence were detected between decades or provinces, suggesting that a historical steady endemic relationship between Bd and Chinese amphibians has occurred. Our results add new insights on the global emergence of Bd and suggest that this pathogen has been more widely distributed in the last century than previously believed.
KeywordsAndrias davidianus Batrachochytrium dendrobatidis China Chytridiomycosis Museum specimens
- ASW (2013) Amphibian species of the World. Version 5.6. http://research.amnh.org/vz/herpetology/amphibia/. Accessed 7 October 2013.
- Bataille A, Fong JJ, Cha M, Wogan GO, Baek HJ, Lee H, et al. (2013) Genetic evidence for a high diversity and wide distribution of endemic strains of the pathogenic chytrid fungus Batrachochytrium dendrobatidis in wild Asian amphibians. Molecular Ecology. doi:10.1111/mec.12385.
- 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.PubMedCentralPubMedCrossRefGoogle Scholar
- Farrer RA, Weinert LA, Bielby J, Garner TWJ, Balloux F, Clare F, et al. (2011). Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. Proceedings of the National Academy of Sciences of the United States of America 108:18732-18736.PubMedCentralPubMedCrossRefGoogle Scholar
- Gang L, Baorong G, Ermi Z (2004) Andrias davidianus. In: IUCN 2012. IUCN Red List of Threatened Species, Version 2012.2. http://www.iucnredlist.org. Accessed 10 October 2012.
- 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.PubMedCentralPubMedCrossRefGoogle Scholar
- IUCN (2012) IUCN Red List of Threatened Species, Version 2012.2. http://www.iucnredlist.org. Accessed 10 October 2012.
- Lehtinen RM, Kam YC, and Richards CL (2010). Preliminary surveys for Batrachochytrium dendrobatidis in Taiwan. Herpetological Review 39:317.Google Scholar
- Lips KR, Brem F, Brenes R, Reeve JD, Alford RA, Voyles J, et al. (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.PubMedCentralPubMedCrossRefGoogle Scholar
- Liu X, Rohr JR, Li Y (2013) Climate, vegetation, introduced hosts and trade shape a global wildlife pandemic. Proceedings of the Royal Society B: Biological Sciences 280:1753. doi:10.1098/rspb.2012.2506.
- Martel A, Spitzen-van der Sluijs A, Blooi M, Bert W, Ducatelle R, Fisher MC, et al. (2013) Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians. Proceedings of the National Academy of Sciences of the United States of America, 110: 15325-15329.PubMedCentralPubMedCrossRefGoogle Scholar
- McLeod DS, Sheridan JA, Jiraungkoorskul W, and Khonsue W (2008). A survey for chytrid fungus in Thai amphibians. Raffles Bulletin of Zoology 56:199-204.Google Scholar
- Rosenblum EB, James TY, Zamudio KR, Poorten TJ, Ilut D, Rodriguez D, et al. (2013) Complex history of the amphibian-killing chytrid fungus revealed with genome resequencing data. Proceedings of the National Academy of Sciences of the United States of America 110: 9385-9390.PubMedCentralPubMedCrossRefGoogle Scholar
- White T, Bruns T, Lee S, and Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR protocols a guide to methods and applications, Innis MA, Gelfand DH, Shinsky JJ and White TJ (editors), New York: Academic Press, pp 315–322.Google Scholar
- Yiming L, Zhunwei K, Yihua W, and Tim M (2011). Frog community responses to recent American bullfrog invasions. Current Zoology 57:83-92.Google Scholar
- Zeng ZH, Bai SZ, Zhu YQ, and Wang XL (2011). Genetic Differentiation of the Pathogen of Batrachochytrium dendrobatidis in Toads. Journal of Economic Animal 15:160-163.Google Scholar