Independent Origin of Chytrid Fungus in China

Huan Wang, Hao-Ning Wang, Joka Fekede Regassa, Xiao-Long Wang

Abstract


Chytridiomycosis is an emerging infectious fungal disease of wildlife worldwide. This disease implicated in the decline or extinction of about 200 amphibian species, thereby contributing to the ongoing sixth great extinction event on the world. With this emerging disease, international trade, specifically import and export from unknown sources, has been associated with novel pathogen transmission. Thus, identifying the potential sources of transmission of the pathogen is a key step in international risk management. China may unknowingly be an important source of pathogen in this regard and a «mixer» of pathogens in the import and export trade. Here, we report evidence for an independent origin of Batrachochytrium dendrobatidis in China. We evaluated American bullfrog (Lithobates catesbeianus) introductions over time and performed phylogenetic analyses of DNA recovered from native Chinese B. dendrobatidis infections in comparison with B. dendrobatidis DNA sequences from other geographically distinct isolates. It is hoped that this study can be used to improve international risk management of chytridiomycosis. The pathogenic mechanism and implications of B. dendrobatidis isolates from China warrants reassessment.

Keywords


Amphibians; Batrachochytrium dendrobatidis; China; origin

Full Text:

PDF

References


Bai C., Garner T. W., 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(1), 127 – 134.

Bai C. M., Liu X., Fisher M. C., Garner T. W. J., and Li Y. M. (2012), «Global and endemic Asian lineages of the emerging pathogenic fungus Batrachochytrium dendrobatidis widely infect amphibians in China», Divers. Distrib., 18(3), 307 – 318.

Bai S. Z. (2012), Risk identification and characterization for Batrachochytrium dendrobatidis in Anura in Changbai Mountain Natural Reserve, Northeast Forestry University, Harbin, China.

Bai S. Z., Wei Y., Wang X. L., and Scholegel L. (2012). «Survey for Batrachochytrium dendrobatidis in wild Rana dybowskii larvae in northern China», in: World Automation Congress, pp. 1 – 4.

Becker C. G. (2011), «Tropical amphibian populations experience higher disease risk in natural habitats», Proc. Natl. Acad. Sci. USA, 108(24), 9893 – 9898.

Bell R. C., Gata Garcia A. V., Stuart B. L., and Zamudio K. R. (2011), «High prevalence of the amphibian chytrid pathogen in Gabon», EcoHealth, 8(1), 116 – 120.

Berger L., Speare R., Daszak P., Green D. E., Cunningham A. A., and Goggin C. L. (1998), «Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America», Proc. Natl. Acad. Sci. USA, 95(15), 9031 – 9036.

Berger L., Hyatt A. D., Olsen V., Hengstberger S. G., Boyle D. and Marantelli G. (2002), «Production of polyclonal antibodies to Batrachochytrium dendrobatidis and their use in an immunoperoxidase test for chytridiomycosis in amphibians», Dis. Aquat. Organisms, 48(3), 213.

Berger L., Speare R., Hines H. B., Marantelli G., Hyatt A. D., and Mcdonald K. R. (2004), «Effect of season and temperature on mortality in amphibians due to Chytridiomycosis», Austral. Veter. J., 82(7), 434 – 439.

Boyle D. G., Boyle D. B., Olsen V., Morgan J. A., and Hyatt A. D. (2004), «Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay», Dis. Aquat. Organisms, 60(2), 141 – 148.

Farrer R. A. and Fisher M. C. (2011), «Multiple emergencies of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage», Proc. Natl. Acad. Sci. USA, 108(46), 18732 – 18736.

Fisher M. C. (2009), «Endemic and introduced haplotypes of Batrachochytrium dendrobatidis in Japanese amphibians: sink or source?» Mol. Ecol., 18(23), 4731 – 4733.

Flechas S. V., Sarmiento C., and Amézquita A. (2012), «B. dendrobatidis on the beach: high prevalence of Batrachochytrium dendrobatidis in the lowland forests of Gorgona island (Colombia, South America)», EcoHealth, 9(3), 298 – 302.

Friesen L. R. and Kuhn R. E. (2012), «Fluorescent microscopy of viable Batrachochytrium dendrobatidis», J. Parasitol., 98(3), 509 – 512.

Garner T. W. J., Walker S., Bosch J., Hyatt A. D., Cunningham A. A., and Fisher M. C. (2005), «Chytrid fungus in Europe», Emerg. Infect. Dis., 11(10), 1639 – 1641.

Goldberg T. L., Readel A. M., and Lee M. H. (2007), «Chytrid fungus in frogs from an equatorial African montane forest in western Uganda», J. Wildlife Dis., 43(3), 521 – 524.

Goka K., Yokoyama J., Une Y., Kuroki T., Suzuki K., and Nakahara M. (2009), «Amphibian chytridiomycosis in Japan: distribution, haplotypes and possible route of entry into Japan», Mol. Ecol., 18(23), 4757 – 4774.

Hidalgo-Vila J., Díaz-Paniagua C., Marchand M. A., and Cunningham A. A. (2012), «Batrachochytrium dendrobatidis infection of amphibians in the Doñana National Park, Spain», Dis. Aquat. Organisms, 98(2), 113 – 119.

Houlahan J. E., Findlay C. S., Schmidt B. R., Meyer A. H., and Kuzmin S. L. (2000), «Quantitative evidence for global amphibian population declines», Nature, 404(404), 752 – 755.

Hunter D. A., Speare R., Marantelli G., Mendez D., Pietsch R., and Osborne W. (2010), «Presence of the amphibian chytrid fungus Batrachochytrium dendrobatidis in threatened corroboree frog populations in the Australian Alps», Dis. Aquat. Organisms, 92(2 – 3), 209 – 216.

Hyatt A. D., Boyle D. G., Olsen V., Boyle D. B., Berger L., and Obendorf D. (2007), «Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis», Dis. Aquat. Organisms, 73(3), 175 – 192.

James T. Y., Toledo L. F., Rödder D., Da S. L. D., Belasen A. M., and Betancourtromán C. M. (2015), «Disentangling host, pathogen, and environmental determinants of a recently emerged wildlife disease: lessons from the first 15 years of amphibian chytridiomycosis research», Ecol. Evol., 5(18), 4079 – 4097.

Kolby J. E., Smith K. M., Berger L., Karesh W. B., Preston A., and Pessier A. P. (2014), «First evidence of amphibian chytrid fungus (Batrachochytrium dendrobatidis) and ranavirus in Hong Kong amphibian trade», PLoS One, 9(3), e90750.

Kriger K. M., Hines H. B., Hyatt A. D., Boyle D. G., and Hero J. M. (2006), «Techniques for detecting chytridiomycosis in wild frogs: comparing histology with real-time Taqman PCR», Dis. Aquat. Organisms, 71(2), 141 – 148.

Kusrini M. D., Skerratt L. F., Garland S., Berger L., and Endarwin W. (2008), «Chytridiomycosis in frogs of Mount Gede Pangrango, Indonesia», Dis. Aquat. Organisms, 82(3), 187 – 194.

Lehtinen R. M., Richards C. L., and Kam Y. C. (2008), «Preliminary surveys for Batrachochytrium dendrobatidis in Taiwan», Herpetol. Rev., 39(39), 1783 – 1786.

Li C., Wang L. J., Shi H. T., Wang J. C., Liu D., and Ma K. (2013), «Attention to invasive risk of American bullfrog for Hainan island», Chin. J. Zool., 48(2), 284 – 286.

Li Y. M., Wu Z. J., and Duncan R. P. (2006), «Why islands are easier to invade: human influences on bullfrog invasion in the Zhoushan archipelago and neighboring mainland China», Oecologia, 148(1), 129 – 136.

Li Y. M., Ke Z. W., Wang Y. H., and Blackburn T. M. (2011), «Frog community responses to recent American bullfrog invasions», Curr. Zool., 57(1), 83 – 92.

Li Z. Y. and Xie Y. (2002), Invasive Alien Species in China, China Forestry Publishing House, Beijing [in Chinese].

Lips K. R., Brem F., Brenes R., Reeve J. D., Alford R. A., and Voyles J. (2006), «Emerging infectious disease and the loss of biodiversity in a neotropical amphibian community», Proc. Natl. Acad. Sci. USA, 103(9), 3165 – 3170.

Liu X., Li Y. M., and Mcgarrity M. (2010), «Geographical variation in body size and sexual size dimorphism of introduced American bullfrogs in southwestern China», Biol. Invas., 12(7), 2037 – 2047.

Liu X., Rohr J. R., and Li Y. (2011), «Climate, vegetation, introduced hosts and trade shape a global wildlife pandemic», Proc. Roy. Soc. B. Biol. Sci., 280(1753), 20122506.

Longcore J. E., Pessier A. P., and Nichols D. K. (1999), «Batrachochytrium dendrobatidis gen. et sp. nov. a chytrid pathogenic to amphibians», Mycologia, 91(2), 219.

Mazzoni R., Cunningham A. A., Daszak P., Apolo A., Perdomo E., and Speranza G. (2003), «Emerging pathogen of wild amphibians in frogs (Rana catesbeiana) farmed for international trade», Emerg. Infect. Dis., 9(8), 995 – 8.

Mei J., Huang Y., Wang S., Huang Z., Qi B., and Zhang H. (2004), «A study on influential factors of drug action in Rana catesbeiana», J. Hunan Agricult. Univ., 30(5), 457 – 461.

Mutschmann F., Berger L., Zwart P., and Gaedicke C. (2000), «Chytridiomycosis in amphibians — first report in Europe», Berl. Münch. Tierärztl. Wochensch., 113(10), 380.

Nichols D. K., Lamirande E. W., Pessier A. P., and Longcore J. E. (2001), «Experimental transmission of cutaneous chytridiomycosis in dendrobatid frogs», J. Wildlife Dis., 37(1), 1 – 11.

OIE (2016), Manual of Diagnostic Tests for Aquatic Animals: Infection with Batrachochytrium dendrobatidis. URL: http://www.oie.int/en/international-standard-setting/aquatic-manual/access-online (accessed Aug 16, 2016).

Picco A. M. and Collins J. P. (2008), «Amphibian commerce as a likely source of pathogen pollution», Conserv. Biol., 22(22), 1582 – 1589.

Rodriguez D., Becker C. G., Pupin N. C., Haddad C. F., and Zamudio K. R. (2014), «Long-term endemism of two highly divergent lineages of the amphibian-killing fungus in the Atlantic forest of Brazil», Mol. Ecol., 23(4), 774 – 787.

Rambaut A. (2006 – 2016), Institute of Evolutionary Biology, University of Edinburgh. URL: http://tree.bio.ed.ac.uk

Schloegel L. M., Picco A. M., Kilpatrick A. M., Davies A. J., Hyatt A. D., and 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)», Biol. Conserv., 142(7), 1420 – 1426.

Schloegel L. M., Daszak P., Cunningham A. A., Speare R., Hill B., and Hyatt A. D. (2010), «Two amphibian diseases, chytridiomycosis and ranaviral disease, are now globally notifiable to the world organization for animal health (OIE): an assessment», Dis. Aquat. Organisms, 92(2 – 3), 101 – 108.

Schloegel L. M., Toledo L. F., Longcore J. E., Greenspan S. E., Vieira C. A., and Lee M. (2012), «Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade», Mol. Ecol., 21(21), 5162.

Schock D. M., Ruthig G. R., Collins J. P., Kutz S. J., Carrière S., and Gau R. J. (2010), «Amphibian chytrid fungus and ranaviruses in the northwest territories, Canada», Dis. Aquat. Organisms, 92(2 – 3), 231 – 240.

Shi H. T. (2009), A lecture on harmfulness of invasive species — a case of Red-eared Slider (Trachemys scripta elegans) and other exotic species of Amphibian and Reptile in China, Auditorium of Chinese National Geography. URL: http://bbs.dili360.com/thread-89672-1-1.html (accessed on May 14, 2009).

Sotoazat C., Clarke B. T., Poynton J. C., and Cunningham A. A. (2009), «Widespread historical presence of Batrachochytrium dendrobatidis in African pipid frogs», Divers. Distrib., 16(1), 126 – 131.

Tamura K., Stecher G., Peterson D., Filipski A., and Kumar S. (2013), «Mega6: molecular evolutionary genetics analysis version 6.0», Mol. Biol. Evol., 30(12), 2725.

Talley B. L., Muletz C. R., Vredenburg V. T., Fleischer R. C., and Lips K. R. (2015), «A century of Batrachochytrium dendrobatidis, in Illinois amphibians (1888 – 1989)», Biol. Conserv., 182, 254 – 261.

Voordouw M. J., Adama D., Houston B., Govindarajulu P., and Robinson J. (2010), «Prevalence of the pathogenic chytrid fungus, Batrachochytrium dendrobatidis, in an endangered population of northern leopard frogs, Rana pipiens», BMC Ecol., 10(1), 6.

Voyles J. and Speare R. (2009), «Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines», Science, 326(5952), 582 – 585.

Wake D. B. (2007), «Climate change implicated in amphibian and lizard declines», Proc. Natl. Acad. Sci. USA, 104(20), 8201 – 8202.

Wei Y., Xu K., Zhu D. Z., Chen X. F., and Wang X. L. (2010), «Early-spring survey for Batrachochytrium dendrobatidis in wild Rana dybowskii in Heilongjiang province, China», Dis. Aquat. Organisms, 92(2 – 3), 241 – 244.

Weldon C., Preez L. H. D., Hyatt A. D., Muller R., and Speare R. (2004), «Origin of the amphibian chytrid fungus», Dis. Aquat. Organisms, 10(12), 2100 – 2105.

Wu Z. J., Wang Y. P., and Li Y. M. (2004), «Natural populations of bullfrog (Rana catesbeiana) and their potential threat in the east of Zhejiang Province», Biodiversity, 4, 441 – 446 [in Chinese].

Xie Z. M. (1999), Bullfrog: Breeding Techniques of Economic Frogs, China Agriculture Press, Beijing [in Chinese].

Yang H., Baek H., Speare R., Webb R., Park S., and Kim T. (2009), «First detection of the amphibian chytrid fungus Batrachochytrium dendrobatidis in free-ranging populations of amphibians on mainland Asia: survey in South Korea», Dis. Aquat. Organisms, 86(1), 9 – 13.

Zhu Y. Q. (2014), Detection of Amphibian Chytrid Fungus and Pest Risk Analysis (PRA) in China, Northeast Forestry University, Harbin, China.

Zhu W., Bai C., Wang S., Soto-Azat C., Li X., and Liu X. (2014), «Retrospective survey of museum specimens reveals historically widespread presence of Batrachochytrium dendrobatidis in China», EcoHealth, 11(2), 241 – 250.

Zhu W., Fan L., Sotoazat C., Yan S., Gao X., and Liu X. (2016), «Filling a gap in the distribution of Batrachochytrium dendrobatidis: evidence in amphibians from northern China», Dis. Aquat. Organisms, 118(3), 259.




DOI: https://doi.org/10.30906/1026-2296-2018-25-4-299-310

Refbacks

  • There are currently no refbacks.