Screening of a long-term sample set reveals two Ranavirus lineages in British herpetofauna

Abstract

Reports of severe disease outbreaks in amphibian communities in mainland Europe due to strains of the common midwife toad virus (CMTV)-like clade of Ranavirus are increasing and have created concern due to their considerable population impacts. In Great Britain, viruses in another clade of Ranavirus–frog virus 3 (FV3)-like—have caused marked declines of common frog (Rana temporaria) populations following likely recent virus introductions. The British public has been reporting mortality incidents to a citizen science project since 1992, with carcasses submitted for post-mortem examination, resulting in a long-term tissue archive spanning 25 years. We screened this archive for ranavirus (458 individuals from 228 incidents) using molecular methods and undertook preliminary genotyping of the ranaviruses detected. In total, ranavirus was detected in 90 individuals from 41 incidents focused in the north and south of England. The majority of detections involved common frogs (90%) but also another anuran, a caudate and a reptile. Most incidents were associated with FV3-like viruses but two, separated by 300 km and 16 years, involved CMTV-like viruses. These British CMTV-like viruses were more closely related to ranaviruses from mainland Europe than to each other and were estimated to have diverged at least 458 years ago. This evidence of a CMTV-like virus in Great Britain in 1995 represents the earliest confirmed case of a CMTV associated with amphibians and raises important questions about the history of ranavirus in Great Britain and the epidemiology of CMTV-like viruses. Despite biases present in the opportunistic sample used, this study also demonstrates the role of citizen science projects in generating resources for research and the value of maintaining long-term wildlife tissue archives.

Effects of historic and projected climate change on the range and impacts of an emerging wildlife disease

“…The small overall decrease in the rate of disease incidents observed over the 20 years of data analyzed, which was observed after controlling for the effect of temperature ( Figure 2d), may be due to fewer opportunities for spread arising from a more complete colonization of the suitable range or might be explained by efforts to limit the risk of translocations through advice disseminated in the media (e.g., BBC, 2008;Price et al, 2016). Alternatively, the severe impacts of recurrent ranavirus outbreaks-previously shown to have caused declines of common frogs in South-East England (Teacher et al, 2010) Although it is challenging to detect disease and mortality in larval amphibians, all evidence points to adult common frogs as the major life history stage and species affected by ranavirosis in the wild in the United Kingdom (Cunningham, 2001;Duffus, 2009;Price et al, 2017). This observation is intriguing since larval forms are usually more affected by FV3 elsewhere in the world and common frog larvae have been shown to be highly susceptible to wild-type ranaviruses in the laboratory (Duffus, Nichols, & Garner, 2013Gray et al, 2009 October outbreaks will alter the life history stages at risk.…”

“…The FMP dataset has been reliably filtered for incidents of ranavirosis previously (North, Hodgson, Price, & Griffiths, 2015;Price et al, 2016;Teacher et al, 2010) based on detailed postmortem examinations of dead and sick amphibians reported from multiple sites over multiple years (Cunningham, 2001;Cunningham et al, 1996;. To date, no diagnosis other than ranavirosis has been made from pathological examinations of common frogs from such mortality incidents in the United Kingodm (Cunningham, 2001;Cunningham et al, 1996;Price et al, 2017). To date, no diagnosis other than ranavirosis has been made from pathological examinations of common frogs from such mortality incidents in the United Kingodm (Cunningham, 2001;Cunningham et al, 1996;Price et al, 2017).…”

“…In this study, the same criteria as Cunningham (2001) and Price et al (2016) (the presence of indicative signs of disease ["ulceration," "red spots on the body," and "limb necrosis/loss of digits"; see Appendix S1 and Figure S1] and a minimum of five dead animals) were used to create a binary variable describing the ranavirus status of each incident. To date, no diagnosis other than ranavirosis has been made from pathological examinations of common frogs from such mortality incidents in the United Kingodm (Cunningham, 2001;Cunningham et al, 1996;Price et al, 2017). The detectability of amphibians varies seasonally, while reporting to the FMP was subject to possible temporal and spatial variation in effort (Price et al, 2016).…”

Temperature is a key driver of a wildlife epidemic and future warming will increase impacts

“…We previously screened a UK amphibian and reptile tissue archive and found 39 ranaviruspositive mortality incidents out of a total of 229 incidents 28 . Temperature was again a highly significant predictor of ranavirus status when these records with precise timestamps, and where ranavirus status had been confirmed, were analyzed.…”

“…Although it is challenging to detect disease and mortality in larval amphibians, all evidence points to adult common frogs as the major life history stage and species affected by ranavirosis in the wild 23,28,31 . This observation is intriguing since larval forms are usually more affected by FV3 elsewhere in the world and common frog larvae have been shown to be highly susceptible to wild-type ranaviruses in the laboratory [32][33][34] .…”