Skip to main content

Advertisement

Log in

Retrospective Survey of Museum Specimens Reveals Historically Widespread Presence of Batrachochytrium dendrobatidis in China

  • Original Contribution
  • Published:
EcoHealth Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1

Similar content being viewed by others

References

  • Annis SL, Dastoor FP, Ziel H, Daszak P, and Longcore JE (2004). A DNA-based assay identifies Batrachochytrium dendrobatidis in amphibians. Journal of Wildlife Diseases 40:420-428.

    Article  CAS  PubMed  Google Scholar 

  • ASW (2013) Amphibian species of the World. Version 5.6. http://research.amnh.org/vz/herpetology/amphibia/. Accessed 7 October 2013.

  • Bai C, Garner TW, and Li Y (2010). 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.

    Article  PubMed  Google Scholar 

  • Bai CM, Liu X, Fisher MC, Garner TWJ, and Li YM (2012). Global and endemic Asian lineages of the emerging pathogenic fungus Batrachochytrium dendrobatidis widely infect amphibians in China. Diversity and Distributions 18:307-318.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cheng TL, Rovito SM, Wake DB, and Vredenburg VT (2011). Coincident mass extirpation of neotropical amphibians with the emergence of the infectious fungal pathogen Batrachochytrium dendrobatidis. Proceedings of the National Academy of Sciences 108:9502-9507.

    Article  CAS  Google 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fisher MC (2009). Endemic and introduced haplotypes of Batrachochytrium dendrobatidis in Japanese amphibians: sink or source? Molecular Ecology 18:4731-4733.

    Article  PubMed  Google Scholar 

  • Gaertner JP, Forstner MRJ, O’Donnell L, and Hahn D (2009). Detection of Batrachochytrium dendrobatidis in endemic salamander species from Central Texas. Ecohealth 6:20-26.

    Article  PubMed  Google 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • Goka K, Yokoyama J, Une Y, Kuroki T, Suzuki K, Nakahara M, et al (2009). Amphibian chytridiomycosis in Japan: distribution, haplotypes and possible route of entry into Japan. Molecular Ecology 18:4757-4774.

    Article  CAS  PubMed  Google Scholar 

  • IUCN (2012) IUCN Red List of Threatened Species, Version 2012.2. http://www.iucnredlist.org. Accessed 10 October 2012.

  • James TY, Litvintseva AP, Vilgalys R, Morgan JAT, Taylor JW, Fisher MC, et al. (2009). Rapid global expansion of the fungal disease chytridiomycosis into declining and healthy amphibian populations. PLoS Pathogens 5:e1000458.

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu X, Li Y, and McGarrity M (2010). Geographical variation in body size and sexual size dimorphism of introduced American bullfrogs in southwestern China. Biological Invasions 12:2037-2047.

    Article  Google 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.

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

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed Central  PubMed  Google 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 

  • Morehouse EA, James TY, Ganley ARD, Vilgalys R, Berger L, Murphy PJ, et al. (2003). Multilocus sequence typing suggests the chytrid pathogen of amphibians is a recently emerged clone. Molecular Ecology 12:395-403.

    Article  CAS  PubMed  Google Scholar 

  • Olson DH, Aanensen DM, Ronnenberg KL, Powell CI, Walker SF, Bielby J, et al. (2013). Mapping the global emergence of Batrachochytrium dendrobatidis, the Amphibian Chytrid Fungus. PLOS One 8: e56802.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Rachowicz LJ, Hero JM, Alford RA, Taylor JW, Morgan JAT, Vredenburg VT, et al. (2005). The novel and endemic pathogen hypotheses: competing explanations for the origin of emerging infectious diseases of wildlife. Conservation Biology 19:1441-1448.

    Article  Google Scholar 

  • Richards-Hrdlicka KL (2012). Extracting the amphibian chytrid fungus from formalin-fixed specimens. Methods in Ecology and Evolution 3:842-849.

    Article  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.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rowley J, Brown R, Bain R, Kusrini M, Inger R, Stuart B, et al. (2010). Impending conservation crisis for Southeast Asian amphibians. Biology Letters 6:336-338.

    Article  PubMed Central  PubMed  Google Scholar 

  • Ryan MJ, Lips KR, and Eichholz MW (2008). Decline and extirpation of an endangered Panamanian stream frog population (Craugastor punctariolus) due to an outbreak of chytridiomycosis. Biological Conservation 141:1636-1647.

    Article  Google Scholar 

  • Savage AE, Grismer LL, Anuar S, Onn CK, Grismer JL, Quah E, et al. (2011). First Record of Batrachochytrium dendrobatidis infecting four frog families from Peninsular Malaysia. Ecohealth 8:121-128.

    Article  PubMed  Google Scholar 

  • Schloegel LM, Toledo LF, Longcore JE, Greenspan SE, Vieira CA, Lee M, et al. (2012). Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade. Molecular Ecology 21:5162-5177.

    Article  PubMed  Google Scholar 

  • Skerratt LF, Berger L, Speare R, Cashins S, McDonald KR, Phillott AD, et al. (2007). Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. Ecohealth 4:125-134.

    Article  Google Scholar 

  • Soto-Azat C, Clarke BT, Fisher MC, Walker SF, and 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  PubMed  Google Scholar 

  • Soto-Azat C, Clarke BT, Poynton JC, and Cunningham AA (2010). Widespread historical presence of Batrachochytrium dendrobatidis in African pipid frogs. Diversity and Distributions 16:126-131.

    Article  Google Scholar 

  • Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, et al. (2004). Status and trends of amphibian declines and extinctions worldwide. Science 306:1783-1786.

    Article  CAS  PubMed  Google Scholar 

  • Swei A, Rowley JJL, Rödder D, Diesmos MLL, Diesmos AC, Briggs CJ, et al. (2011). Is chytridiomycosis an emerging infectious disease in Asia? PLOS ONE 6:e23179.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Voyles J, Young S, Berger L, Campbell C, Voyles WF, Dinudom A, et al. (2009). Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 326:582-585.

    Article  CAS  PubMed  Google Scholar 

  • Vredenburg VT, Felt SA, Morgan EC, McNally SVG, Wilson S, and Green SL (2013). Prevalence of Batrachochytrium dendrobatidis in Xenopus Collected in Africa (1871-2000) and in California (2001-2010). Plos One 8:e63791.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vredenburg VT, Knapp RA, Tunstall TS, and Briggs CJ (2010). Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proceedings of the National Academy of Sciences of the United States of America 107:9689-9694.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  PubMed  Google 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 

  • 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  PubMed  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.

    CAS  Google Scholar 

Download references

Acknowledgements

We thank Enqi Ye of the National Zoological Museum (Beijing) and Zhiqing Xu of the Chongqing Museum of Natural History (Chongqing) for assistance with sampling. We are also grateful to Kris Murray and two anonymous reviewers for helpful comments on the draft of the manuscript. This research was supported by grants from the National Natural Science Foundation of China (code: 31172111, 31200416) and the Beijing Natural Science Foundation (code: 5132026).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yiming Li.

Additional information

Wei Zhu, Changming Bai, and Supen Wang contributed equally to this article.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhu, W., Bai, C., Wang, S. et al. Retrospective Survey of Museum Specimens Reveals Historically Widespread Presence of Batrachochytrium dendrobatidis in China. EcoHealth 11, 241–250 (2014). https://doi.org/10.1007/s10393-013-0894-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10393-013-0894-7

Keywords

Navigation