Supen WANG,Wei ZHU,Liqing FAN,et al.Amphibians Testing Negative for Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans on the Qinghai-Tibetan Plateau, China[J].Asian Herpetological Reserch(AHR),2017,8(3):190-198.[doi:10.16373/j.cnki.ahr.170010]
Click Copy

Amphibians Testing Negative for Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans on the Qinghai-Tibetan Plateau, China
Share To:

Asian Herpetological Research[ISSN:2095-0357/CN:51-1735/Q]

Issue:
2017 VoI.8 No.3
Page:
190-198
Research Field:
Publishing date:
2017-09-25

Info

Title:
Amphibians Testing Negative for Batrachochytrium dendrobatidis and Batrachochytrium salamandrivorans on the Qinghai-Tibetan Plateau, China
Author(s):
Supen WANG1# Wei ZHU12# Liqing FAN123# Jiaqi LI4 and Yiming LI12*
1 Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
2 University of Chinese Academy of Sciences, 19 Yuquan Road, Beijing 100049, China
3 Institute of Plateau Ecology, Agriculture and Animal Husbandry College of Tibet University, No. 8 Xueyuan Street, Bayi Town, Linzhi County, Xizang Province 860000, China
4 Nanjing Institute of Environmental Sciences under Ministry of Environmental Protection of China. No. 8 Jiang Wang Miao Street, Nanjing 210042, China
Keywords:
Chytridiomycosis Amphibians invasive species museum specimens Qinghai-Tibetan Plateau
PACS:
-
DOI:
10.16373/j.cnki.ahr.170010
Abstract:
A disease caused by the fungi Batrachochytrium dendrobatidis (Bd) and Batrachochytrium salamandrivorans (Bsal) is responsible for recent worldwide declines and extinctions of amphibian populations. The Qinghai-Tibetan Plateau (QTP) is aglobal biodiversity hotspot, yet little is known about the prevalence of Bd and Bsal in this region. In this study, we collected 336 non-invasive skin swabs from wild amphibians (including an exotic amphibian species) on the QTP. In addition, to assess the historical prevalence of Bd and Bsal on the QTP, we collected 117 non-invasive skin swabs from museum-archived amphibian samples (from 1964–1982) originating from the QTP. Our results showed all samples to be negative for Bd and Bsal. The government should ban the potentially harmful introduction of non-native amphibian species to the QTP and educate the public about the impacts of releasing exotic amphibians from chytrid-infected areas into native environments of the QTP.

References:

Amphibia China. 2016. The database of Chinese amphibians. Kunming, Yunnan. Retrieved from http://www.amphibiachina.org
Annis S. L., Dastoor F. P., Ziel H., Daszak P., Longcore J. E. 2004. A DNA-based assay identifies Batrachochytrium dendrobatidis in amphibians. J Wildl Dis, 40: 420–428
Bai C. M., Garner T. W. J., Li Y. M. 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
Bai C. M., Liu X., Fisher M. C., Garner T. W. J., Li Y. M. 2012. Global and endemic Asian lineages of the emerging pathogenic fungus Batrachochytrium dendrobatidis widely infect amphibians in China. Divers Distrib, 18: 307–318
Bataille A., Fong J. J., Cha M., Wogan G. O. U., Baek H. J., Lee H., Min M. S., Waldman B. 2013. Genetic evidence for a high diversity and wide distribution of endemic strains of the pathogenic chytrid fungus Batrachochytrium dendrobatidis in wild Asian amphibians. Mol Ecol, 22: 4196–4209
Berger L., Speare R., Daszak P., Green D. E., Cunningham A. A., Goggin C. L., Slocombe R., Ragan M. A., Hyatt A. D., McDonald K. R., Hines H. B., Lips K. R., Marantelli G., Parkes H. 1998. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc Natl Acad Sci U S A, 95: 9031–9036
Cheng T. L., Rovito S. M., Wake D. B., Vredenburg V. T. 2011. Coincident mass extirpation of neotropical amphibians with the emergence of the infectious fungal pathogen Batrachochytrium dendrobatidis. Proc Natl Acad Sci U S A, 108: 9502–9507
Cunningham A. A., Beckmann K., Perkins M., Fitzpatrick L., Cromie R., Redbond J., O’Brien M. F., Ghosh P., Shelton J., Fisher M. C. 2015. Emerging disease in UK amphibians. Vet Rec, 176: 468–468
Dahanukar N., Krutha K., Paingankar M. S., Padhye A. D., Modak N., Molur S. 2013. Endemic Asian chytrid strain infection in threatened and endemic anurans of the northern Western Ghats, India. PLOS ONE, 8: e77528
Davidson E. W., Parris M., Collins J. P., Longcore J. E., Pessier A. P., Brunner J. 2003. Pathogenicity and transmission of chytridiomycosis in tiger salamanders (Ambystoma tigrinum). Copeia, 2003: 601–607
Di RosaI., Simoncelli F., Fagotti A., Pascolini R. 2007. Ecology: the proximate cause of frog declines? Nature, 447: E4–5; discussion E5–6
Fisher M. C., Garner T. W. J. 2007. The relationship between the emergence of Batrachochytrium dendrobatidis, the international trade in amphibians and introduced amphibian species. Fungal Biol Rev, 21: 2–9
Fisher M. C., Garner T. W. J., Walker S. F. 2009. Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annu Rev Microbiol, 63: 291–310
Fisher M. C., Henk D. A., Briggs C. J., Brownstein J. S., Madoff L. C., McCraw S. L., Gurr S. J. 2012. Emerging fungal threats to animal, plant and ecosystem health. Nature, 484: 186–194
Gaertner J. P., Forstner M. R. J., O’Donnell L., Hahn D. 2009. Detection of Batrachochytrium dendrobatidis in endemic salamander species from Central Texas. Ecohealth, 6: 20–26
Garmyn A., Van Rooij P., Pasmans F., Hellebuyck T., Van den Broeck W., Haesebrouck F., Martel A. 2012. Waterfowl: Potential environmental reservoirs of the chytrid fungus Batrachochytrium dendrobatidis. PLOS ONE, 7: e35038
Goka K., Yokoyama J., Une Y., Kuroki T., Suzuki K., Nakahara M., Kobayashi A., Inaba S., Mizutani T., Hyatt A. D. 2009. Amphibian chytridiomycosis in Japan: Distribution, haplotypes and possible route of entry into Japan. Mol Ecol, 18: 4757–4774
Gower D. J., Doherty-Bone T., Loader S. P., Wilkinson M., Kouete M. T., Tapley B., Orton F., Daniel O. Z., Wynne F., Flach E., Müller H., Menegon M., Stephen I., Browne R. K., Fisher M. C., Cunningham A. A., Garner T. W. J. 2013. Batrachochytrium dendrobatidis infection and lethal Chytridiomycosis in caecilian amphibians (Gymnophiona). Ecohealth, 10: 173–183
Gründler M. C., Toledo L. F., Parra-Olea G., Haddad C. F. B., Giasson L. O. M., Sawaya R. J., Prado C. P. A., Araujo O. G. S., Zara F. J., Centeno F. C., Zamudio K. R. 2012. Interaction between breeding habitat and elevation affects prevalence but not infection intensity of Batrachochytrium dendrobatidis in Brazilian anuran assemblages. Dis Aquat Organ, 97: 173–184
Hyatt A. D., Boyle D. G., Olsen V., Boyle D. B., Berger L., Obendorf D., Dalton A., Kriger K., Heros M., Hines H., Phillott R., Campbell R., Marantelli G., Gleason F., Coiling A. 2007. Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Dis Aquat Organ, 73: 175–192
James T. Y., Toledo L. F., R?dder D., da Silva Leite D., Belasen A. M., Betancourt-Román C. M., Jenkinson T. S., Soto-Azat C., Lambertini C., Longo A. V., Ruggeri J., Collins J. P., Burrowes P. A., Lips K. R., Zamudio K. R., Longcore J. E. 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: 4079–4097
Kilpatrick A. M., Briggs C. J., Daszak P. 2010. The ecology and impact of chytridiomycosis: An emerging disease of amphibians. Trends Ecol Evol, 25: 109–118
Knapp R. A., Briggs C. J., Smith T. C., Maurer J. R. 2011. Nowhere to hide: impact of a temperature-sensitive amphibian pathogen along an elevation gradient in the temperate zone. Ecosphere, 2
Kolby J. E., Smith K. M., Berger L., Karesh W. B., Preston A., Pessier A. P., SkerrattL. F. 2014. First evidence of amphibian chytrid fungus (Batrachochytrium dendrobatidis) and ranavirus in Hong Kong amphibian trade. PLOS ONE, 9: e90750
Kusrini M. D., Skerratt L. F., Garland S., Berger L., Endarwin W. 2008. Chytridiomycosis in frogs of Mount Gede Pangrango, Indonesia. Dis Aquat Organ, 82: 187–194
Laking A. E., Ngo H. N., Pasmans F., Martel A., Nguyen T. T. 2017. Batrachochytrium salamandrivorans is the predominant chytrid fungus in Vietnamese salamanders. Sci Rep, 7: 44443
Li X., Liu X., Kraus F., Tingley R., Li Y. 2016. Risk of biological invasions is concentrated in biodiversity hotspots. Front Ecol Environ, 14: 411–417
Lips K. R., Brem F., Brenes R., Reeve J. D., Alford R. A., Voyles J., Carey C., Livo L., Pessier A. P., Collins J. P. 2006. Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proc Natl Acad Sci U S A, 103: 3165–3170
Liu X. D., Chen B. D. 2000. Climatic warming in the Tibetan Plateau during recent decades. Int J Climatol, 20: 1729–1742
Liu X., Rohr J. R., Li Y. 2013. Climate, vegetation, introduced hosts and trade shape a global wildlife pandemic. Proc Biol Sci, 280: 20122506
Longcore J. E., Pessier A. P., Nichols D. K.1999. Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia, 91: 219–227
Martel A., Blooi M., Adriaensen C., Van Rooij P., Beukema W., Fisher M. C., Farrer R. A., Schmidt B. R., Tobler U., Goka K., Lips K. R., Muletz C., Zamudio K. R., Bosch J., L?tters S., Wombwell E., Garner T. W. J., Cunningham A. A., Spitzen-van der Sluijs A., Salvidio S., Ducatelle R., Nishikawa K., Nguyen T. T., Kolby J. E., Van Bocxlaer I., Bossuyt F., Pasmans F. 2014. Wildlife disease. Recent introduction of a chytrid fungus endangers Western palearctic salamanders. Science, 346: 630–631
Martel A., Spitzen-van der Sluijs A., Blooi M., Bert W., Ducatelle R., Fisher M. C., Woeltjes A., Bosman W., Chiers K., Bossuyt F., Pasmans F. 2013. Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians. Proc Natl Acad Sci U S A, 110: 15325–15329
McMahon T. A., Brannelly L. A., Chatfield M. W. H., Johnson P. T. J., Joseph M. B., McKenzie V. J., Richards-Zawacki C. L., Venesky M. D., Rohr J. R. 2013. Chytrid fungus Batrachochytrium dendrobatidis has nonamphibian hosts and releases chemicals that cause pathology in the absence of infection. Proc Natl Acad Sci U S A, 110: 210–215
Mittermeier R. A., Turner W. R., Larsen F. W., Brooks T. M., GasconC. 2011. Global biodiversity conservation: The critical role of hotspots. 3–22. In Zachos F. E., Habel J. C. (Eds.), Biodiversity hotspots. Berlin, Germany: Springer
Muths E., Pilliod D. S., Livo L. J. 2008. Distribution and environmental limitations of an amphibian pathogen in the Rocky mountains, USA. Biol Conserv, 141: 1484–1492
Olson D. H., Aanensen D. M., Ronnenberg K. L., Powell C. I., Walker S. F., Bielby J., Garner T. W. J., Weaver G., Bd Mapping Group, Fisher M. C. 2013. Mapping the global emergence of Batrachochytrium dendrobatidis, the amphibian chytrid fungus. PLOS ONE, 8: e56802
Phillott A. D., Speare R., Hines H. B., Skerratt L. F., Meyer E., McDonald K. R., Cashins S. D., Mendez D., Berger L. 2010. Minimising exposure of amphibians to pathogens during field studies. Dis Aquat Organ, 92: 175–185
Qin J., Yang K., Liang S. L., Guo X. F. 2009. The altitudinal dependence of recent rapid warming over the Tibetan Plateau. Clim Change, 97: 321–327
R Development Core Team. 2012. R: A language and environment for statistical computing. Vienna, Austria: R Foundation Statistical Computing. Retrieved from http://www.R-project.org/
Rosa G. M., Anza I., Moreira P. L., Conde J., Martins F., Fisher M. C., Bosch J. 2013. Evidence of chytrid-mediated population declines in common midwife toad in Serra da Estrela, Portugal. Anim Conserv, 16: 306–315
Sabino-Pinto J., Bletz M., Hendrix R., Perl R. B., Martel A., Pasmans F., L?tters S., Mutschmann F., Schmeller D. S., Schmidt B. R., Veith M., Wagner N., Vences M., Steinfartz S. 2015. First detection of the emerging fungal pathogen Batrachochytrium salamandrivoransin Germany. Amphib Reptil, 36: 411–416
Savage A. E., Grismer L. L., Anuar S., Onn C. K., Grismer J. L., Quah E., Muin M. A., Ahmad N., Lenker M., Zamudio K. R. 2011. First Record of Batrachochytrium dendrobatidis infecting four frog families from peninsular Malaysia. Ecohealth, 8: 121–128
Skerratt L. F., BergerL., Hines H. B., McDonald K. R., Mendez D., Speare R. 2008. Survey protocol for detecting chytridiomycosis in all Australian frog populations. Dis Aquat Organ, 80: 85–94
Skerratt L. F., Berger L., Speare R., Cashins S., McDonald K. R., Phillott A. D., Hines H. B., Kenyon N. 2007. Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. Ecohealth, 4: 125–134
Soto-Azat C., Clarke B. T., Fisher M. C., Walker S. F., Cunningham A. A 2009. Non-invasive sampling methods for the detection of Batrachochytrium dendrobatidis in archived amphibians. Dis Aquat Organ, 84: 163–166
Spitzen-van der Sluijs A., Spikmans F., Bosman W., de Zeeuw M., van der Meij T., Goverse E., Kik M., Pasmans F., Martel A. 2013. Rapid enigmatic decline drives the fire salamander (Salamandra salamandra) to the edge of extinction in the Netherlands. Amphib Reptil, 34: 233–239
Swei A., Rowley J. J. L., R?dder D., Diesmos M. L. L., Diesmos A. C., Briggs C. J., Brown R., Cao T. T., Cheng T. L., Chong R. A., Han B., Hero J. M., Hoang H. D., Kusrini M. D., Le D. T., McGuire J. A., Meegaskumbura M., Min M. S., Mulcahy D. G., Neang T., Phimmachak S., Rao D. Q., Reeder N. M., Schoville S. D., Sivongxay N., Srei N., St?ck M., Stuart B. L., Torres L. S., Tran D. T., Tunstall T. S., Vieites D., Vredenburg V. T. 2011. Is chytridiomycosis an emerging infectious disease in Asia? PLOS ONE, 6: e23179
Vredenburg V. T., Knapp R. A., Tunstall T. S., Briggs C. J. 2010. Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proc Natl Acad Sci U S A, 107: 9689–9694
Walker S. F., Bosch J., James T. Y., Litvintseva A. P., Oliver Valls J. A., Pi?a S., García G., Rosa G. A., Cunningham A. A., Hole S., Griffiths R., Fisher M. C. 2008. Invasive pathogens threaten species recovery programs. Curr Biol, 18: R853–R854
Wang S., Fan L., Liu C., Li J., Gao X., Zhu W., Li Y. 2017. The origin of invasion of the alien Pelophylax nigromaculatus in Tibet, China. Curr Zool. doi:10.1093/cz/zow1117
Wei Y. Q., Fang Y. P. 2013. Spatio-temporal characteristics of global warming in the Tibetan Plateau during the last 50 years based on a generalised temperature zone-elevation model. PLOS ONE, 8: e60044
White T., Bruns T., Lee S., Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: A Guide to Methods and Applications, 18: 315–322
Yang H., Baek H., Speare R., Webb R., Park S., Kim T., Lasater K. C., Shin S., Son S., Park J., Min M., Kim Y., Na K., Lee H., Park S. 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 Organ, 86: 9–13
Zhang H., Fu H., Li W. 2015. Pelophylax nigromaculatus record in Qinghai Province was confirmed. Chin J Zool, 50: 145–147
Zhou S. Z., WangX. L., WangJ., XuL. B. 2006. A preliminary study on timing of the oldest Pleistocene glaciation in Qinghai-Tibetan Plateau. Quatern Int, 154–155: 44–51
Zhu W., Bai C., Wang S., Soto-Azat C., Li X., Liu X., Li Y. 2014a. Retrospective survey of museum specimens reveals historically widespread presence of Batrachochytrium dendrobatidis in China. Ecohealth, 11: 241–250
Zhu W., Fan L., Soto-Azat C., Yan S., Gao X., Liu X., Wang S., Liu C., Yang X., Li Y. 2016. Filling a gap in the distribution of Batrachochytrium dendrobatidis: Evidence in amphibians from northern China. Dis Aquat Organ, 118: 259–265
Zhu W., Xu F., Bai C. M., Liu X., Wang S. P., Gao X., Yan S. F., Li X. P., Liu Z. T., Li Y. M. 2014b. A survey for Batrachochytrium salamandrivorans in Chinese amphibians. Curr Zool, 60: 729–735

Memo

Memo:
-
Last Update: 2017-09-25