Register      Login
Pacific Conservation Biology Pacific Conservation Biology Society
A journal dedicated to conservation and wildlife management in the Pacific region.
RESEARCH ARTICLE

Detection of ranavirus in endemic and threatened amphibian populations of the Australian Wet Tropics Region

Felicity J. Wynne https://orcid.org/0000-0003-2487-2623
+ Author Affiliations
- Author Affiliations

School of Biological and Marine Sciences, University of Plymouth, Plymouth, Devon, PL4 8AA, United Kingdom. Email: felicity.wynne@plymouth.ac.uk

Pacific Conservation Biology 26(1) 93-97 https://doi.org/10.1071/PC19009
Submitted: 4 March 2019  Accepted: 27 May 2019   Published: 25 June 2019

Abstract

The amphibian chytrid fungus (Batrachochytrium dendrobatidis) has driven severe amphibian declines in the Australian tropics. These declines have resulted in species extirpations and extinctions, with many surviving in small, highly threatened populations. Despite the fragility of remaining populations, another group of lethal pathogens, ranaviruses, have rarely been investigated among native amphibians. Ranaviruses have previously been associated with fish, reptile and amphibian mortality events in Australia, yet remain poorly understood here, especially among amphibian hosts. Here, quantitative polymerase chain reaction assays were used to detect ranavirus presence from eight of 17 tested sites containing populations of endangered and critically endangered Australian frog species. Although present in these populations, ranavirus seems to be at the lower bounds of detectability of the assay, which makes firm diagnosis at the individual level unreliable. Repeated (n = 14) detections of this pathogen, however, are highly indicative of its presence at each area where it was detected. Therefore, these populations are likely often exposed to ranavirus. The results of this study are not characteristic of populations experiencing rapid disease-associated die-offs or declines, but further investigations should be undertaken to examine the potential drivers of these pathogens to predict future emergence and potential threats to endangered Australian amphibians.

Additional keywords: Litoria, Queensland, rainforest, ranavirus, sclerophyll.


References

Ariel, E. (1997). Pathology and serological aspects of Bohle iridovirus infections in six selected water-associated reptiles in North Queensland. Ph.D. Thesis, James Cook University, Townsville.

Ariel, E., Wirth, W., Burgess, G., Scott, J., and Owens, L. (2015). Pathogenicity in six Australian reptile species following experimental inoculation with Bohle iridovirus. Diseases of Aquatic Organisms 115, 203–212.
Pathogenicity in six Australian reptile species following experimental inoculation with Bohle iridovirus.Crossref | GoogleScholarGoogle Scholar | 26290505PubMed |

Ariel, E., Elliott, E., Meddings, J., Miller, J., Santos, M., and Owens, L. (2017). Serological survey of Australian native reptiles for exposure to ranavirus. Diseases of Aquatic Organisms 126, 173–183.
Serological survey of Australian native reptiles for exposure to ranavirus.Crossref | GoogleScholarGoogle Scholar | 29160216PubMed |

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., and 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.
Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America.Crossref | GoogleScholarGoogle Scholar | 9671799PubMed |

Bertelsen, M., and Crawshaw, G. (2003). 5-minute guide to amphibian disease. Exotic DVM 5, 23–26.

Burgin, S., Schell, C. B., and Briggs, C. L. (2005). Is Batrachochytrium dendrobatidis really the proximate cause of frog decline? Dong Wu Xue Bao 51, 344–348.

Campbell, L. J., Hammond, S. A., Price, S. J., Sharma, M. D., Garner, T. W. J., Birol, I., Helbing, C. C., Wilfert, L., and Griffiths, A. G. F. (2018). A novel approach to wildlife transcriptomics provides evidence of disease-mediated differential expression and changes to the microbiome of amphibian populations. Molecular Ecology 27, 1413–1427.
A novel approach to wildlife transcriptomics provides evidence of disease-mediated differential expression and changes to the microbiome of amphibian populations.Crossref | GoogleScholarGoogle Scholar | 29420865PubMed |

Cullen, B. R., and Owens, L. (2002). Experimental challenge and clinical cases of Bohle iridovirus (BIV) in native Australian anurans. Diseases of Aquatic Organisms 49, 83–92.
Experimental challenge and clinical cases of Bohle iridovirus (BIV) in native Australian anurans.Crossref | GoogleScholarGoogle Scholar | 12078986PubMed |

Cullen, B. R., Owens, L., and Whittington, R. J. (1995). Experimental infection of Australian anurans (Limnodynastes terraereginae and Litoria latopalmata) with Bohle iridovirus. Diseases of Aquatic Organisms 23, 83–92.
Experimental infection of Australian anurans (Limnodynastes terraereginae and Litoria latopalmata) with Bohle iridovirus.Crossref | GoogleScholarGoogle Scholar |

Gray, M. J., Miller, D. L., and Hoverman, J. T. (2012). Reliability of non-lethal surveillance methods for detecting ranavirus infection. Diseases of Aquatic Organisms 99, 1–6.
Reliability of non-lethal surveillance methods for detecting ranavirus infection.Crossref | GoogleScholarGoogle Scholar | 22585297PubMed |

Green, D. E., Converse, K. A., and Schrader, A. K. (2002). Epizootiology of sixty-four amphibian morbidity and mortality events in the USA, 1996–2001. Annals of the New York Academy of Sciences 969, 323–339.
Epizootiology of sixty-four amphibian morbidity and mortality events in the USA, 1996–2001.Crossref | GoogleScholarGoogle Scholar | 12381613PubMed |

Greer, A., Berrill, M., and Wilson, P. (2005). Five amphibian mortality events associated with ranavirus infection in south central Ontario, Canada. Diseases of Aquatic Organisms 67, 9–14.
Five amphibian mortality events associated with ranavirus infection in south central Ontario, Canada.Crossref | GoogleScholarGoogle Scholar | 16385802PubMed |

Hall, E. M., Crespi, E. J., Goldberg, C. S., and Brunner, J. L. (2016). Evaluating environmental DNA-based quantification of ranavirus infection in wood frog populations. Molecular Ecology Resources 16, 423–433.
Evaluating environmental DNA-based quantification of ranavirus infection in wood frog populations.Crossref | GoogleScholarGoogle Scholar | 26308150PubMed |

Hick, P. M., Subramaniam, K., Thompson, P., Whittington, R. J., and Waltzek, T. B. (2016). Complete genome sequence of a Bohle iridiovirus isolate from ornate burrowing frogs (Limnodynastes ornatus) in Australia. Genome Announcements 4, e00632–16.
Complete genome sequence of a Bohle iridiovirus isolate from ornate burrowing frogs (Limnodynastes ornatus) in Australia.Crossref | GoogleScholarGoogle Scholar | 27540051PubMed |

Hoverman, J. T., Mihaljevic, J. R., Richgels, K. L. D., Kerby, J. L., and Johnson, P. T. J. (2012). Widespread co-occurrence of virulent pathogens within California amphibian communities. EcoHealth 9, 288–292.
Widespread co-occurrence of virulent pathogens within California amphibian communities.Crossref | GoogleScholarGoogle Scholar | 22766887PubMed |

Hyatt, A. D., Gould, A. R., Zupanovic, Z., Cunningham, A. A., Hengstberger, S., Whittington, R. J., Kattenbelt, J., and Coupar, B. E. H. (2000). Comparative studies of piscine and amphibian iridoviruses. Archives of Virology 145, 301–331.
Comparative studies of piscine and amphibian iridoviruses.Crossref | GoogleScholarGoogle Scholar | 10752555PubMed |

Hyatt, A., Boyle, D. D., Olsen, V., Boyle, D. D., Berger, L., Obendorf, D., Dalton, A., Kriger, K., Hero, M., Hines, H., Phillott, R., Campbell, R., Marantelli, G., Gleason, F., and Colling, A. (2007). Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 73, 175–192.
Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis.Crossref | GoogleScholarGoogle Scholar | 17330737PubMed |

IUCN (2018). The IUCN Red List of Threatened Species (Version 2018-2). Available at: http://www.iucnredlist.org [accessed 14 September 2018].

Kik, M., Martel, A., der Sluijs, A. S., Pasmans, F., Wohlsein, P., Gröne, A., and Rijks, J. M. (2011). Ranavirus-associated mass mortality in wild amphibians, The Netherlands, 2010: a first report. Veterinary Journal (London, England) 190, 284–286.
Ranavirus-associated mass mortality in wild amphibians, The Netherlands, 2010: a first report.Crossref | GoogleScholarGoogle Scholar |

Laurance, W. F., McDonald, K. R., and Speare, R. (1996). Epidemic disease and the catastrophic decline of Australian rain forest frogs. Conservation Biology 10, 406–413.
Epidemic disease and the catastrophic decline of Australian rain forest frogs.Crossref | GoogleScholarGoogle Scholar |

Leung, W. T. M., Thomas-Walters, L., Garner, T. W. J., Balloux, F., Durrant, C., and Price, S. J. (2017). A quantitative-PCR based method to estimate ranavirus viral load following normalisation by reference to an ultraconserved vertebrate target. Journal of Virological Methods 249, 147–155.
A quantitative-PCR based method to estimate ranavirus viral load following normalisation by reference to an ultraconserved vertebrate target.Crossref | GoogleScholarGoogle Scholar |

Maclaine, A., Mashkour, N., Scott, J., and Ariel, E. (2018). Susceptibility of eastern water dragons Intellagama lesueurii lesueurii to Bohle iridovirus. Diseases of Aquatic Organisms 127, 97–105.
Susceptibility of eastern water dragons Intellagama lesueurii lesueurii to Bohle iridovirus.Crossref | GoogleScholarGoogle Scholar | 29384479PubMed |

Maclaine, A., Forzán, M. J., Mashjour, N., Scott, J., and Ariel, E. (2019). Pathogenesis of Bohle iridovirus (Genus Ranavirus) in experimentally infected juvenile eastern water dragons (Intellagama lesueurii lesueurii). Veterinary Pathology 56, 465–475.
Pathogenesis of Bohle iridovirus (Genus Ranavirus) in experimentally infected juvenile eastern water dragons (Intellagama lesueurii lesueurii).Crossref | GoogleScholarGoogle Scholar | 30686212PubMed |

McDonald, K., and Alford, R. (1999). A review of declining frogs in northern Queensland. In ‘Declines and Disappearances of Australian Frogs’. (Ed. A. Campbell.) pp. 14–22. (Environment Australia: Canberra.)

McKnight, D. T., Alford, R. A., Hoskin, C. J., Schwarzkopf, L., Greenspan, S. E., Zenger, K. R., and Bower, D. S. (2017). Fighting an uphill battle: the recovery of frogs in Australia’s Wet Tropics. Ecology 98, 3221–3223.
Fighting an uphill battle: the recovery of frogs in Australia’s Wet Tropics.Crossref | GoogleScholarGoogle Scholar | 29141097PubMed |

Miller, D. L., Pessier, A. P., Hick, P., and Whittington, R. J. (2015). Comparative pathology of ranaviruses and diagnostic techniques. In ‘Ranaviruses’. (Eds M. J. Gray, and V. G. Chinchar.) pp. 171–208. (Springer International Publishing: Cham.)

Moody, N. J. G., and Owens, L. (1994). Experimental demonstration of the pathogenicity of a frog virus, Bohle iridovirus, for a fish species, barramundi Lates calcarifer. Diseases of Aquatic Organisms 18, 95–102.
Experimental demonstration of the pathogenicity of a frog virus, Bohle iridovirus, for a fish species, barramundi Lates calcarifer.Crossref | GoogleScholarGoogle Scholar |

OIE (2018). Manual of diagnostic tests for aquatic animals (2018). Available at: http://www.oie.int/standard-setting/aquatic-manual/access-online/ [accessed 14 September 2018].

Price, S. J. (2014). Emergence of a virulent wildlife disease: using spatial epidemiology and phylogenetic methods to reconstruct the spread of amphibian viruses. Ph.D. Thesis, Queen Mary University of London.

Price, S. J., Garner, T. W. J., Nichols, R. A., Balloux, F., Ayres, C., Mora-Cabello De Alba, A., and Bosch, J. (2014). Collapse of amphibian communities due to an introduced ranavirus. Current Biology 24, 2586–2591.
Collapse of amphibian communities due to an introduced ranavirus.Crossref | GoogleScholarGoogle Scholar | 25438946PubMed |

Puschendorf, R. (2009). Environmental effects on a host–pathogen system: frogs and Batrachochytrium dendrobatidis in wet and dry habitats. Ph.D. Thesis, James Cook University, Townsville.

Puschendorf, R., Hoskin, C. J., Cashins, S. D., Mcdonald, K., Skerratt, L. F., Vanderwal, J., and Alford, R. A. (2011). Environmental refuge from disease-driven amphibian extinction. Conservation Biology 25, 956–964.
Environmental refuge from disease-driven amphibian extinction.Crossref | GoogleScholarGoogle Scholar | 21902719PubMed |

Richards, S. J., and Alford, R. A. (2005). Structure and dynamics of a rainforest frog (Litoria genimaculata) population in northern Queensland. Australian Journal of Zoology 53, 229–236.
Structure and dynamics of a rainforest frog (Litoria genimaculata) population in northern Queensland.Crossref | GoogleScholarGoogle Scholar |

Richards, S. J., McDonald, K. R., and Alford, R. A. (1994). Declines in populations of Australia’s endemic tropical rainforest frogs. Pacific Conservation Biology 1, 66–77.
Declines in populations of Australia’s endemic tropical rainforest frogs.Crossref | GoogleScholarGoogle Scholar |

Rosa, G. M., Sabino-Pinto, J., Laurentino, T. G., Martel, A., Pasmans, F., Rebelo, R., Griffiths, R. A., Stöhr, A. C., Marschang, R. E., Price, S. J., Garner, T. W. J., and Bosch, J. (2017). Impact of asynchronous emergence of two lethal pathogens on amphibian assemblages. Scientific Reports 7, 43260.
Impact of asynchronous emergence of two lethal pathogens on amphibian assemblages.Crossref | GoogleScholarGoogle Scholar | 28240267PubMed |

Sainsbury, A. W., and Vaughan-Higgins, R. J. (2012). Analyzing disease risks associated with translocations. Conservation Biology 26, 442–452.
Analyzing disease risks associated with translocations.Crossref | GoogleScholarGoogle Scholar | 22533691PubMed |

Scheele, B. C., Skerratt, L. F., Grogan, L. F., Hunter, D. A., Clemann, N., McFadden, M., Newell, D., Hoskin, C. J., Gillespie, G. R., Heard, G. W., Brannelly, L., Roberts, A. A., and Berger, L. (2017). After the epidemic: ongoing declines, stabilizations and recoveries in amphibians afflicted by chytridiomycosis. Biological Conservation 206, 37–46.
After the epidemic: ongoing declines, stabilizations and recoveries in amphibians afflicted by chytridiomycosis.Crossref | GoogleScholarGoogle Scholar |

Schloegel, L. M., Hero, J.-M., Berger, L., Speare, R., McDonald, K., and Daszak, P. (2006). The decline of the sharp-snouted day frog (Taudactylus acutirostris): the first documented case of extinction by infection in a free-ranging wildlife species? EcoHealth 3, 35–40.
The decline of the sharp-snouted day frog (Taudactylus acutirostris): the first documented case of extinction by infection in a free-ranging wildlife species?Crossref | GoogleScholarGoogle Scholar |

Speare, R., and Smith, J. R. (1992). An iridovirus-like agent isolated from the ornate burrowing frog Limnodynastes ornatus in northern Australia. Diseases of Aquatic Organisms 14, 51–57.
An iridovirus-like agent isolated from the ornate burrowing frog Limnodynastes ornatus in northern Australia.Crossref | GoogleScholarGoogle Scholar |

Stark, T., Laurijssens, C., Weterings, M., der Sluijs, A. S., Martel, A., and Pasmans, F. (2014). Death in the clouds: ranavirus associated mortality in assemblage of cloud forest amphibians in Nicaragua. Acta Herpetologica 9, 125–127.

Teacher, A. G. F., Cunningham, A. A., and Garner, T. W. J. (2010). Assessing the long-term impact of Ranavirus infection in wild common frog populations. Animal Conservation 13, 514–522.
Assessing the long-term impact of Ranavirus infection in wild common frog populations.Crossref | GoogleScholarGoogle Scholar |

TNCMAPS (2009). Conservation GIS data – the Nature Conservancy. Available at: http://maps.tnc.org/ [accessed 7 July 2018].

Warne, R. W., LaBumbard, B., LaGrange, S., Vredenburg, V. T., and Catenazzi, A. (2016). Co-infection by chytrid fungus and ranaviruses in wild and harvested frogs in the tropical Andes. PLoS One 11, e0145864.
Co-infection by chytrid fungus and ranaviruses in wild and harvested frogs in the tropical Andes.Crossref | GoogleScholarGoogle Scholar | 26726999PubMed |

Weir, R., Moody, N., Hyatt, A., Crameri, S., Voysey, R., Pallister, J., and Jerrett, I. (2012). Isolation and characterisation of a novel Bohle-like virus from two frog species in the Darwin rural area, Australia. Diseases of Aquatic Organisms 99, 169–177.
Isolation and characterisation of a novel Bohle-like virus from two frog species in the Darwin rural area, Australia.Crossref | GoogleScholarGoogle Scholar | 22832715PubMed |

Wirth, W., Schwarzkopf, L., Skerratt, L. F., and Ariel, E. (2018). Ranaviruses and reptiles. PeerJ 6, e6083.
Ranaviruses and reptiles.Crossref | GoogleScholarGoogle Scholar | 30581674PubMed |

Wynne, F. J. (2019). The ecology and two emerging amphibian pathogens in Costa Rica. Ph.D. Thesis, University of Plymouth, UK.