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http://dx.doi.org/10.1186/s41610-020-00179-2

First detection of ranavirus in a wild population of Dybowski's brown frog (Rana dybowskii) in South Korea  

Park, Jaejin (Department of Regional Innovation, Kangwon National University)
Grajal-Puche, Alejandro (Department of Biological Sciences, Northern Arizona University)
Roh, Nam-Ho (Natural Environmental Restoration Institute Co. Ltd.)
Park, Il-Kook (Division of Science Education, Kangwon National University)
Ra, Nam-Yong (Rana Eco-Consultant)
Park, Daesik (Division of Science Education, Kangwon National University)
Publication Information
Journal of Ecology and Environment / v.45, no.1, 2021 , pp. 10-16 More about this Journal
Abstract
Background: Ranavirus is an emerging infectious disease which has been linked to mass mortality events in various amphibian species. In this study, we document the first mass mortality event of an adult population of Dybowski's brown frogs (Rana dybowskii), in 2017, within a mountain valley in South Korea. Results: We confirmed the presence of ranavirus from all collected frogs (n = 22) via PCR and obtained the 500 bp major capsid protein (MCP) sequence from 13 individuals. The identified MCP sequence highly resembled Frog virus 3 (FV3) and was the same haplotype of a previously identified viral sequence collected from Huanren brown frog (R. huanrenensis) tadpoles in South Korea. Human habitat alteration, by recent erosion control works, may be partially responsible for this mass mortality event. Conclusion: We document the first mass mortality event in a wild Korean population of R. dybowskii. We also suggest, to determine if ranavirus infection is a threat to amphibians, government officials and researchers should develop continuous, country-wide, ranavirus monitoring programs of Korean amphibian populations.
Keywords
Ranavirus; Rana dybowskii; Mass mortality; Wild population; Major capsid protein;
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1 Kim S, Sim MY, Eom AH, Park D, Ra NY. PCR detection of ranavirus in gold-spotted pond frogs (Rana plancyi chosenica) from Korea. Korean J Environ Biol. 2009;27(1):110-3.
2 Kolby JE, Smith KM, Berger L, Karesh WB, Preston A, Pessier AP, Skerratt LF. First evidence of amphibian chytrid fungus (Batrachochytrium dendrobatidis) and ranavirus in Hong Kong amphibian trade. PloS one. 2014;9(3):e90750.   DOI
3 Kwon S, Park J, Choi WJ, Koo KS, Lee JG, Park D. First case of ranavirus-associated mass mortality in a natural population of the Huanren frog (Rana huanrenensis) tadpoles in South Korea. Anim Cells Syst. 2017;21(5):358-64.   DOI
4 Leduc J. Life-history trade-offs in Northern leopard frog (Lithobates [Rana] pipiens) tadpoles: interactions of trace metals, temperature, and ranavirus. PhD Thesis, Laurentian University of Sudbury; 2014.
5 Mao J, Hedrick RP, Chinchar VG. Molecular characterization, sequence analysis, and taxonomic position of newly isolated fish iridoviruses. Virology. 1997;229(1):212-20.   DOI
6 Meng Y, Ma J, Jiang N, Zeng LB, Xiao HB. Pathological and microbiological findings from mortality of the Chinese giant salamander (Andrias davidianus). Arch Virol. 2014;159(6):1403-12.   DOI
7 Miller D, Gray M, Storfer A. Ecopathology of ranaviruses infecting amphibians. Viruses. 2011;3(11):2351-73.   DOI
8 Miller D, Pessier A, Hick P, Whittington R. 2015. Comparative pathology of ranaviruses and diagnostic techniques. In: Gray MJ, Chinchar VG. Ranaviruses. Cham: Springer; 2015. p. 171-208.
9 Mu WH, Geng Y, Yu ZH, Wang KY, Huang XL, Ou YP, et al. FV3-like ranavirus infection outbreak in black-spotted pond frogs (Rana nigromaculata) in China. Microb Pathogenesis. 2018;123:111-4.   DOI
10 Norris DO, Jones RE. Hormones and reproduction in fishes, amphibians, and reptiles. Berlin: Springer Science & Business Media; 2012.
11 O'hanlon SJ, Rieux A, Farrer RA, Rosa GM, Waldman B, Bataille A, et al. Recent Asian origin of chytrid fungi causing global amphibian declines. Science. 2018;360(6389):621-7.   DOI
12 Park IK, Koo KS, Moon KY, Lee JG. Park D. PCR detection of ranavirus from dead Kaloula borealis and sick Hyla japonica tadpoles in the wild. Korean. J Herpetol. 2017;8:10-4.
13 Posada D, Crandall KA. Modeltest: testing the model of DNA substitution. Bioinformatics. 1998;14(9):817-8.   DOI
14 Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Hohna S, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61(3):539-42.   DOI
15 Thompson JD, Gibson TJ, Higgins DG. Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics. 2003;(1):2-3.
16 Scheele BC, Pasmans F, Skerratt LF, Berger L, Martel A, Beukema W, et al. Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science. 2019;363(6434):1459-63.   DOI
17 St-Amour V, Lesbarreres D. Genetic evidence of Ranavirus in toe clips: an alternative to lethal sampling methods. Conserv Genet. 2007;8(5):1247.   DOI
18 Swofford DL. Paup*: Phylogenetic analysis using parsimony (and other methods). Sunderland: Sinauer Associates; 2001. Ver.4.0.b5.
19 Une Y, Kudo T, Tamukai KI, Murakami M. Epidemic ranaviral disease in imported captive frogs (Dendrobates and Phyllobates spp.), Japan, 2012: a first report. JMM Case Rep. 2014;1(3):e001198.   DOI
20 Une Y, Nakajima K, Taharaguchi S, Ogihara K, Murakami M. Ranavirus infection outbreak in the salamander (Hynobius nebulosus) in Japan. J Comp Pathol. 2009a;4(141):310.
21 Yoo E, Jang Y. Abiotic effects on calling phenology of three frog species in Korea. Anim Cells Syst. 2012;16(3):260-7.   DOI
22 Une Y, Sakuma A, Matsueda H, Nakai K, Murakami M. Ranavirus outbreak in North American bullfrogs (Rana catesbeiana), Japan, 2008. Emerg Infect Dis. 2009b;15(7):1146.   DOI
23 Warne RW, Crespi EJ, Brunner JL. Escape from the pond: stress and developmental responses to ranavirus infection in wood frog tadpoles. Funct Ecol. 2011;25(1):139-46.   DOI
24 Weng SP, He JG, Wang XH, Lu L, Deng M, Chan SM. Outbreaks of an iridovirus disease in cultured tiger frog, Rana tigrina rugulosa. in southern China. J Fish Dis. 2002;25(7):423-7.   DOI
25 Xu K, Zhu DZ, Wei Y, Schloegel LM, Chen XF, Wang XL. Broad distribution of ranavirus in free-ranging Rana dybowskii in Heilongjiang, China. EcoHealth. 2010;7(1):18-23.   DOI
26 Yang H, Baek H, Speare R, Webb R, Park S, Kim T, et al. 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. 2009;86(1):9-13.   DOI
27 Yu Z, Mou W, Geng Y, Wang K, Chen D, Huang X, et al. Characterization and genomic analysis of a ranavirus associated with cultured black-spotted pond frogs (Rana nigromaculata) tadpoles mortalities in China. Transbound Emerg Dis. 2020. https://doi.org/10.1111/tbed.13534.   DOI
28 Zhang QY, Li ZQ, Jiang YL, Liang SC, Gui JF. Preliminary studies on virus isolation and cell infection from disease frog Rana grylio. Acta Hydrobiol Sin. 1996;20(4):390-2 (in Chinese).
29 Zhang QY, Xiao F, Li ZQ, Gui JF, Mao J, Chinchar VG. Characterization of an iridovirus from the cultured pig frog Rana grylio with lethal syndrome. Dis Aquat Organ. 2001;48(1):27-36.   DOI
30 Zhou ZY, Geng Y, Liu XX, Ren SY, Zhou Y, Wang KY, Huang XL, et al. Characterization of a ranavirus isolated from the Chinese giant salamander (Andrias davidianus, Blanchard, 1871) in China. Aquaculture. 2013;384:66-73.   DOI
31 Zhou ZY, Geng Y, Ren SY, Wang KY, Huang XL, Chen DF, et al. Ranavirus (family Iridoviridae) detection by polymerase chain reaction (PCR) in Chinese giant salamander (Andrias davidianus, Blanchard, 1871), China. Afr J Biotechnol. 2012;11(85):15130-4.
32 de Matos APA, da Silva Trabucho MFA, Papp T, Matos BADCA, Correia ACL, Marschang RE. New viruses from Lacerta monticola (Serra da Estrela, Portugal): further evidence for a new group of nucleo-cytoplasmic large deoxyriboviruses. Microsc Microanal. 2011;17(1):101-8.   DOI
33 Zhu YQ, Wang XL. Genetic diversity of ranaviruses in amphibians in China: 10 new isolates and their implications. Pak J Zool. 2016;48:107-14.
34 Carey C, Bradford DF, Brunner JL, Collins JP, Davidson EW, Longcore JE, et al. Biotic factors in amphibian population declines. In: Linder G, Krest SK, Sparling DW, editors. Amphibian decline: an integrated analysis of multiple stressor effects. Pensacola: SETAC Press; 2003. p. 153-208.
35 Ahne W, Schlotfeldt HJ, Thomsen I. Fish viruses: isolation of an icosahedral cytoplasmic deoxyribovirus from sheatfish (Silurus glanis). J Vet Med B. 1989;36(1-10):333-6.   DOI
36 Brunner JL, Storfer A, Gray MJ, Hoverman JT. Ranavirus ecology and evolution: from epidemiology to extinction. In: Gray MJ, Chinchar VG, editors. Ranaviruses. Cham: Springer; 2015. p. 71-104.
37 Carey C, Cohen N, Rollins-Smith L. Amphibian declines: an immunological perspective. Dev Comp Immunol. 1999;23(6):459-72.   DOI
38 Chen Z, Gui J, Gao X, Pei C, Hong Y, Zhang Q. Genome architecture changes and major gene variations of Andrias davidianus ranavirus (ADRV). Vet Res. 2013;44(1):1-13.   DOI
39 Chen ZX, Zheng JC, Jiang YL. A new iridovirus isolated from soft-shelled turtle. Virus Res. 1999;63(1-2):147-51.   DOI
40 Daszak P, Berger L, Cunningham AA, Hyatt AD, Green DE, Speare R. Emerging infectious diseases and amphibian population declines. Emerg Infect Dis. 1999;5(6):735.   DOI
41 Duffus ALJ, Pauli BD, Wozney K, Brunetti CR, Berrill M. Frog virus 3-like infections in aquatic amphibian communities. J Wildlife Dis. 2008;44(1):109-20.   DOI
42 Duffus ALJ, Waltzek TB, Stohr AC, Allender MC, Gotesman M, Whittington RJ, et al. Distribution and host range of ranaviruses. In: Gray MJ, Chinchar VG, editors. Ranaviruses. Cham: Springer; 2015. p. 9-57.
43 Fey SB, Siepielski AM, Nussle S, Cervantes-Yoshida K, Hwan JL, Huber ER, et al. Recent shifts in the occurrence, cause, and magnitude of animal mass mortality events. P Natl Acad Sci USA. 2015;112(4):1083-8.   DOI
44 Fox SF, Greer AL, Torres-Cervantes R, Collins JP. First case of ranavirus-associated morbidity and mortality in natural populations of the South American frog Atelognathus patagonicus. Dis Aquat Organ. 2006;72(1):87-92.   DOI
45 Gahl MK, Calhoun AJK. The role of multiple stressors in ranavirus-caused amphibian mortalities in Acadia National Park wetlands. Can J Zool. 2010;88(1):108-21.   DOI
46 Granoff A, Came PE, Rafferty KA Jr. The isolation and properties of viruses from Rana pipiens: their possible relationship to the renal adenocarcinoma of the leopard frog. Ann NY Acad Sci. 1965;126(1):237-55.   DOI
47 Garcia-Diaz P, Ross JV, Woolnough AP, Cassey P. Managing the risk of wildlife disease introduction: pathway-level biosecurity for preventing the introduction of alien ranaviruses. J Appl Ecol. 2017;54(1):234-41.   DOI
48 Geng Y, Wang K, Li C, Wang J, Liao Y, Huang J. Zhou Z. PCR detection and electron microscopic observation of bred Chinese giant salamander infected with ranavirus associated with mass mortality. Vet. Sci China. 2010;40(8):817-21.
49 Geng Y, Wang KY, Zhou ZY, Li CW, Wang J, He M, et al. First report of a ranavirus associated with morbidity and mortality in farmed Chinese giant salamanders (Andrias davidianus). J Comp Pathol. 2011;145(1):95-102.   DOI
50 Gray MJ, Miller DL, Hoverman JT. Ecology and pathology of amphibian ranaviruses. Dis Aquat Organ. 2009;87(3):243-66.   DOI
51 Green DE, Converse KA, Schrader AK. Epizootiology of sixty-four amphibian morbidity and mortality events in the USA, 1996-2001. Ann NY Acad Sci. 2002;969(1):323-39.   DOI
52 He JG, Lu L, Deng M, He HH, Weng SP, Wang XH, et al. Sequence analysis of the complete genome of an iridovirus isolated from the tiger frog. Virology. 2002;292(2):185-97.   DOI
53 Hengstberger SG, Hyatt AD, Speare R, Coupar BEH. Comparison of epizootic haematopoietic necrosis and Bohle iridoviruses, recently isolated Australian iridoviruses. Dis Aquat Organ. 1993;15(2):93-107.   DOI
54 Kang MJ, Kim KD, Oh KS, Park JW, Park JH. Analysis of forest environmental factors on torrent erosion control work area in Gyeongsangnam-do: focus on erosion control dam and stream conservation. J Agric & Life Sci. 2016;50(5):111-20 (in Korean).   DOI