Skip to main content
SpringerLink
Log in

Amphibian Pathogens in Southeast Asian Frog Trade

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

Abstract

Amphibian trade is known to facilitate the geographic spread of pathogens. Here we assess the health of amphibians traded in Southeast Asia for food or as pets, focusing on Batrachochytrium dendrobatidis (Bd), ranavirus and general clinical condition. Samples were collected from 2,389 individual animals at 51 sites in Lao PDR, Cambodia, Vietnam and Singapore for Bd screening, and 74 animals in Cambodia and Vietnam for ranavirus screening. Bd was found in one frog (n = 347) in Cambodia and 13 in Singapore (n = 419). No Bd was found in Lao PDR (n = 1,126) or Vietnam (n = 497), and no ranavirus was found in Cambodia (n = 70) or Vietnam (n = 4). Mild to severe dermatological lesions were observed in all East Asian bullfrogs Hoplobatrachus rugolosus (n = 497) sampled in farms in Vietnam. Histologic lesions consistent with sepsis were found within the lesions of three frogs and bacterial sepsis in two (n = 4); one had Gram-negative bacilli and one had acid-fast organisms consistent with mycobacterium sp. These results confirm that Bd is currently rare in amphibian trade in Southeast Asia. The presence of Mycobacterium-associated disease in farmed H. rugolosus is a cause for concern, as it may have public health implications and indicates the need for improved biosecurity in amphibian farming and trade.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2

Similar content being viewed by others

References

  • Agresti A, Coull BA (1998). Approximate is better than “exact” for interval estimation of binomial proportions. American Statistician 52, 119–126

    Google Scholar 

  • Andreone F, Cadle JE, Cox N, Glaw F, Nussbaum RA, Raxworthy CJ, Stuart SN, Vallan D, Vences M, (2005) Species review of amphibian extinction risks in Madagascar: Conclusions from the global amphibian assessment. Conservation Biology 19:1790-1802

    Article  Google Scholar 

  • Annis SL, Dastoor FP, Ziel H, Daszak P, Longcore JE (2004). A DNA-based assay identifies Batrachochytrium dendrobatidis in amphibians. Journal of Wildlife Diseases 40, 420–8

    PubMed  CAS  Google Scholar 

  • Bai C, Garner T, 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 

  • Berger L, Speare R, Daszak P, Green DE, Cunningham AA, Goggin CL, Slocombe R, Ragan MA, Hyatt AD, McDonald KR, Hines HB, Lips KR, Marantelli G, Parkes H (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  PubMed  CAS  Google Scholar 

  • Bollinger TK, Mao JH, Schock D, Brigham RM, Chinchar VG (1999) Pathology, isolation, and preliminary molecular characterization of a novel iridovirus from tiger salamanders in Saskatchewan. Journal of Wildlife Diseases 35:413-429

    PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Brem F, Mendelson III JR, Lips KR (2007) Field-sampling protocol for Batrachochytrium dendrobatidis from living amphibians, using alcohol preserved swabs. Version 1.0 (18 July 2007). Arlington, Virginia, USA. http://www.amphibianark.org/pdf/Field%20sampling%20protocol%20for%20amphibian%20chytrid%20fungi%201.0.pdf. Accessed 10 Dec 2010

  • Cannon RM, Roe RT, (1982) Livestock Disease Surveys: A Field Manual for Veterinarians. Australian Bureau of Animal Health, Canberra

    Google Scholar 

  • Catenazzi A, Lehr E, Rodriguez LO, Vredenburg VT (2011) Batrachochytrium dendrobatidis and the collapse of Anuran species richness and abundance in the Upper Manu National Park, Southeastern Peru. Conservation Biology 25:382-391

    Article  PubMed  Google Scholar 

  • Catenazzi A, Vredenburg VT, Lehr E (2010) Batrachochytrium dendrobatidis in the live frog trade of Telmatobius (Anura: Ceratophryidae) in the tropical Andes. Diseases of Aquatic Organisms 92:187-191

    Article  PubMed  Google Scholar 

  • Collins JP (2010) Amphibian decline and extinction: What we know and what we need to learn. Diseases of Aquatic Organisms 92:93-99

    Article  PubMed  Google Scholar 

  • Cunningham AA, Garner TWJ, Aguilar-Sanchez V, Banks B, Foster J, Sainsbury AW, Perkins M, Walker SF, Hyatt AD, Fisher MC, 2005. Emergence of amphibian chytridiomycosis in Britain. Veterinary Record 157:386-387

    PubMed  CAS  Google Scholar 

  • Cunningham AA, Langton TES, Bennett PM, Lewin JF, Drury SEN, Gough RE, MacGregor SK (1996) Pathological and microbiological findings from incidents of unusual mortality of the common frog (Rana temporaria). Philisophical Transactions of the Royal Society of London B - Biological Sciences 35:1539-1557

    Article  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 

  • Fisher MC, Garner TWJ, Walker SF (2009) Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annual Review of Microbiology 63:291-310

    Article  PubMed  CAS  Google Scholar 

  • Geng Y, Wang KY, Zhou ZY, Li CW, Wang J, He M, Yin ZQ, Lai WM (2011) First report of a Ranavirus associated with morbidity and mortality in farmed Chinese Giant Salamanders (Andrias davidianus). Journal of Comparative Pathology 145:95-102

    Article  PubMed  CAS  Google Scholar 

  • Global Bd-Mapping Project (2011) Bd-maps. http://www.bd-maps.net. Accessed 15 June 2010

  • Gratwicke B, Evans MJ, Jenkins PT, Kusrini MD, Moore RD, Sevin J, Wildt DE (2010) Is the international frog legs trade a potential vector for deadly amphibian pathogens? Frontiers in Ecology and the Environment 8:438-442

    Article  Google Scholar 

  • Green DE, Converse KA, Schrader AK (2002) Epizootiology of sixty-four amphibian morbidity and mortality events in the USA, 1996–2001. In: Domestic Animal/Wildlife Interface: Issue for Disease Control, Conservation, Sustainable Food Production, and Emerging Diseases, Gibbs EPJ, Bokma BH (editors), New York: New York Academy of Sciences, pp. 323–339

  • IUCN (2011) The IUCN Redlist of threatened species. http://www.iucnredlist.org/. Accessed 15 June 2010

  • James TY, Litvintseva AP, Vilgalys R, Morgan JAT, Taylor JW, Fisher MC, Berger L, Weldon C, du Preez L, Longcore JE (2009) Rapid global expansion of the fungal disease chytridiomycosis into declining and healthy amphibian populations. PloS Pathogens 5:1-12

    Article  Google Scholar 

  • Jancovich JK, Bremont M, Touchman JW, Jacobs BL (2010) Evidence for Multiple Recent Host Species Shifts among the Ranaviruses (Family Iridoviridae). Journal of Virology 84:2636-2647

    Article  PubMed  CAS  Google Scholar 

  • Jancovich JK, Davidson EW, Parameswaran N, Mao J, Chinchar VG, Collins JP, Jacobs BL, Storfer A (2005) Evidence for emergence of an amphibian iridoviral disease because of human-enhanced spread. Molecular Ecology 14:213-224

    Article  PubMed  CAS  Google Scholar 

  • Johnson AJ, Pessier AP, Wellehan JFX, Childress A, Norton TM, Stedman NL, Bloom DC, Belzer W, Titus VR, Wagner R, Brooks JW, Spratt J, Jacobson ER (2008) Ranavirus infection of free-ranging and captive box turtles and tortoises in the United States. Journal of Wildlife Diseases 44,:851-863

    PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Lips KR, Brem F, Brenes R, Reeve JD, Alford RA, Voyles J, Carey C, Livo L, Pessier AP, Collins JP (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  PubMed  CAS  Google Scholar 

  • McLeod DS, Sheridan JA, Jiraungkoorskul W, Khonsue W (2008) A survey for chytrid fungus in Thai amphibians. Raffles Bulletin of Zoology 56:199-204

    Google Scholar 

  • Neang T (2010) An Investigation into Frog Consumption and Trade in Cambodia. Flora and Fauna International, Cambodia Programme, Phnom Penh, Cambodia

  • Pallister J, Gould A, Harrison D, Hyatt A, Jancovich J, Heine H, (2007) Development of real-time PCR assays for the detection and differentiation of Australian and European ranaviruses. Journal of Fish Diseases 30:427-438

    Article  PubMed  CAS  Google Scholar 

  • Picco AM, Collins JP (2008) Amphibian commerce as a likely source of pathogen pollution. Conservation Biology 22:1582-1589

    Article  PubMed  Google Scholar 

  • Pounds JA, Bustamante MR, Coloma LA, Consuegra JA, Fogden MPL, Foster PN, La Marca E, Masters KL, Merino-Viteri A, Puschendorf R, Ron SR, Sánchez-Azofeifa GA, Still CJ, Young BE (2006) Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439:161-7

    Article  PubMed  CAS  Google Scholar 

  • Rowley J, Brown R, Bain R, Kusrini M, Inger R, Stuart B, Wogan G, Thy N, Chan-ard T, Trung CT, Diesmos A, Iskandar DT, Lau M, Ming LT, Makchai S, Truong NQ, Phimmachak S (2010) Impending conservation crisis for Southeast Asian amphibians. Biology Letters 6:336-338

    Article  PubMed  Google Scholar 

  • Rowley JJL, Chan SKF, Tang WS, Speare R, Skerratt LF, Alford RA, Cheung KS, Ho CY, Campbell R (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  PubMed  Google Scholar 

  • Savage AE, Grismer LL, Anuar S, Onn CK, Grismer JL, Quah E, Muin MA, Ahmad N, Lenker M, Zamudio KR (2011) First Record of Batrachochytrium dendrobatidis infecting four frog families from Peninsular Malaysia. EcoHealth 8(1):121-128

    Article  PubMed  Google Scholar 

  • Schloegel LM, Daszak P, Cunningham AA, Speare R, Hill B (2010) Two amphibian diseases, chytridiomycosis and ranaviral disease, are now globally notifiable to the World Organization for Animal Health (OIE): an assessment. Diseases of Aquatic Organisms 92:101-108

    Article  PubMed  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 

  • Schloegel LM, Toledo LF, Longcore JE, Greenspan SE, Vieira CA, Lee M, Zhao S, Wangen C, Ferreira CM, Hipolito M, Davies AJ, Cuomo CA, Daszak P, James TY (2012) Novel, panzootic and hybrid genotypes of amphibian chytridiomycosis associated with the bullfrog trade. Molecular Ecology doi:10.1111/j.1365-294X.2012.05710.x

  • Seimon TA, Seimon A, Daszak P, Halloy SRP, Schloegel LM, Aguilar CA, Sowell P, Hyatt AD, Konecky B, Simmons JE (2007) Upward range extension of Andean anurans and chytridiomycosis to extreme elevations in response to tropical deglaciation. Global Change Biology 13:288-299

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Swei A, Rowley JJL, Rödder D, Diesmos MLL, Diesmos AC, Briggs CJ, Brown R, Cao TT, Cheng TL, Chong RA, Han B, Hero J-M, Hoang HD, Kusrini MD, Le DTT, McGuire JA, Meegaskumbura M, Min M-S, Mulcahy DG, Neang T, Phimmachak S, Rao D-Q, Reeder NM, Schoville SD, Sivongxay N, Srei N, Stöck M, Stuart BL, Torres LS, Tran DTA, Tunstall TS, Vieites D, Vredenburg VT (2011) Is Chytridiomycosis an Emerging Infectious Disease in Asia? PLoS ONE 6, e23179

    Article  PubMed  CAS  Google Scholar 

  • Une Y, Kadekaru S, Tamukai K, Goka K, Kuroki T (2008) First report of spontaneous chytridiomycosis in frogs in Asia. Diseases of Aquatic Organisms 82:157-160

    Article  PubMed  Google Scholar 

  • Une Y, Sakuma A, Matsueda H, Nakai K, Murakami M (2009) Ranavirus outbreak in North American bullfrogs (Rana catesbeiana), Japan, 2008. Emerging Infectious Diseases 15:1146-1147

    Article  PubMed  Google Scholar 

  • Voyles J, Young S, Berger L, Campbell C, Voyles WF, Dinudom A, Cook D, Webb R, Alford RA, Skerratt LF, Speare R (2009) Pathogenesis of Chytridiomycosis,a Cause of Catastrophic Amphibian Declines. Science 236:592-585

    Google Scholar 

  • Vredenburg VT, Knapp RA, Tunstall TS, 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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Weldon C, DeVilliers AL, du Preez LH (2007) Quantification of the trade in Xenopus laevis from South Africa, with implications for biodiversity conservation. African Journal of Herpetology 56:77-83

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Xu K, Zhu D-Z, Wei Y, Schloegel L, Chen X-F, Wang X-L (2010) Broad distribution of ranavirus in free-ranging Rana dybowskii in Heilongjiang, China. EcoHealth 7:18-23

    Article  PubMed  Google Scholar 

  • Yang H, Baek H, Speare R, Webb R, Park S, Kim T, Lasater KC, 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. Diseases of Aquatic Organisms 86:9-13

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

General funding for this project was provided by the Wildlife Conservation Society Institute with fieldwork in Singapore funded by the National University of Singapore. We would like to thank Jenny Pramuk, Bryan Stuart, Jodi Rowley, Neang Thy, and Damien O. Joly for assistance in study design and species identification. Generous support was also given in Vietnam by the Department of Animal Health (Ministry of Agriculture and Rural Development), in particular Dr. Le Van Khoa, Department of Aquatic Animal Health and Dr. Ngo Thanh Long, Dr. Nguyen Truc Ha and Phan Thuy Thanh Duyen, Regional Animal Health Office No. 6, the National Animal Health Centre of Lao PDR (in particular Bounlom Douangngeun and Watthana Theppangna), Professor Bounthop Phaxaysombath of the National University of Laos (NUOL) and Nem Sok Heng. Particular thanks are due to sampling teams in Vietnam (Nguyễn Thị Thanh Nga, Phạm Thị Xao, Nguyễn Thị Lan Anh, Tạ Quốc Hiệu, Trịnh Thị Huyền, Mạc Thị Yến, Faculty of Veterinary Medicine, Hanoi University of Agriculture, Vietnam), Lao PDR (Vannasin Inoudom, Somsai Philakoum), Cambodia (Chea Sokha, Chor Kimashalen, Chea Samban,), and Singapore (Geraldine R. Joseph, Jamie Lim Jingmei, and Zhihan Yeo). Finally we thank Denise McAloose and two anonymous reviewers for help in improving the manuscript.

Author information

Authors and Affiliations

  1. Wildlife Conservation Society, 2300 Southern Blvd, Bronx, NY, 10460, USA

    Martin Gilbert, Leanne Clark, Arlyne Johnson, Priscilla H. Joyner, Lucy Ogg Keatts, Kongsy Khammavong, Long Nguyễn Văn, Alisa Newton, Scott Roberton, Soubanh Silithammavong, Angela Yang & Tracie A. Seimon

  2. Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore, 117543, Republic of Singapore

    David Bickford & Tiffany P. W. Seow

  3. Department of Biology, National University of Laos, Vientiane, Lao People’s Democratic Republic

    Sinpakhone Singhalath

Authors
  1. Martin Gilbert
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David Bickford
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Leanne Clark
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Arlyne Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Priscilla H. Joyner
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lucy Ogg Keatts
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kongsy Khammavong
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Long Nguyễn Văn
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Alisa Newton
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Tiffany P. W. Seow
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Scott Roberton
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Soubanh Silithammavong
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Sinpakhone Singhalath
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Angela Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Tracie A. Seimon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martin Gilbert.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gilbert, M., Bickford, D., Clark, L. et al. Amphibian Pathogens in Southeast Asian Frog Trade. EcoHealth 9, 386–398 (2012). https://doi.org/10.1007/s10393-013-0817-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10393-013-0817-7

Keywords

Search

Navigation