Mosquitoes as a Potential Vector of Ranavirus Transmission in Terrestrial Turtles

Abstract

Ranaviruses are significant pathogens of amphibians, reptiles, and fishes, contributing to mass mortality events worldwide. Despite an increasing focus on ranavirus ecology, our understanding of ranavirus transmission, especially among reptilian hosts, remains limited. For example, experimental evidence for oral transmission of the virus in chelonians is mixed. Consequently, vector-borne transmission has been hypothesized in terrestrial turtle species. To test this hypothesis, mosquitoes captured during a 2012/2013 ranavirus outbreak in box turtles from southwestern Indiana were pooled by genus and tested for ranavirus DNA using qPCR. Two of 30 pools tested positive for ranavirus. Additionally, an individual Aedes sp. mosquito observed engorging on a box turtle also tested positive for ranavirus. Although our approach does not rule out the possibility that the sequenced ranavirus was simply from virus in bloodmeal, it does suggests that mosquitoes may be involved in virus transmission as a mechanical or biological vector among ectothermic vertebrates. While additional studies are needed to elucidate the exact role of mosquitoes in ranavirus ecology, our study suggests that a greater focus on vector-borne transmission may be necessary to fully understand ranaviral disease dynamics in herpetofauna.

Distribution and Host Range of Ranaviruses

“…Therefore, it is likely that susceptibility of chelonians to ranaviruses differs among developmental stages similar to amphibians . Some outbreaks in box turtles have involved translocation events that congregate many individuals, resulting in high infection prevalence and death (Belzer and Seibert 2011 ;Farnsworth and Seigel 2013 ;Kimble et al 2014 ). In a multiyear survey of box turtles in the USA, ranavirus prevalence has not been reported above 5 % in a population without abnormal mortality events (Allender et al 2013 ).…”

“…In a multiyear survey of box turtles in the USA, ranavirus prevalence has not been reported above 5 % in a population without abnormal mortality events (Allender et al 2013 ). Reports of single cases and outbreaks in reptiles so far have mainly involved box turtles within North America (De Voe et al 2004 ;Allender et al 2006 ;Johnson et al 2008Johnson et al , 2010Ruder et al 2010 ;Allender 2012 ;Kimble et al 2014 ). While eastern box turtles are primarily terrestrial, they have been shown to spend a considerable amount of time in temporary ponds (Donaldson and Echternacht 2005 ), which may expose them to ranavirus through water or sympatric amphibians (Belzer and Seibert 2011 ;Currylow et al 2014 ).…”

“…While eastern box turtles are primarily terrestrial, they have been shown to spend a considerable amount of time in temporary ponds (Donaldson and Echternacht 2005 ), which may expose them to ranavirus through water or sympatric amphibians (Belzer and Seibert 2011 ;Currylow et al 2014 ). Some studies have indicated that increased ranaviral mortality in box turtles may correlate with increased exposure to infected sympatric amphibians, possibly via predation on infected amphibians, exposure to water containing ranavirus shed by amphibians, or via hematophagous insects (Belzer and Seibert 2011 ;Kimble et al 2014 ). A study of wild Eastern painted turtles, an aquatic species, in Virginia, USA, reported infection prevalence of 4.8-31.6 % in different ponds, with no apparent disease (Goodman et al 2013 ).…”

Ranavirus Ecology and Evolution: From Epidemiology to Extinction

“…Allender et al ( 2006 ) speculated that ranaviruses may be transmitted between chelonians by vectors because the virus is found in circulating blood cells in turtles. Kimble et al ( 2014 ) recently detected ranavirus in mosquitoes at a site with ranavirus-infected eastern box turtles. Mosquito transmission might help explain how ranaviruses continue to spread between turtles that rarely encounter one another and die fairly quickly from infection.…”

Ranaviruses

“…Therefore, it is likely that susceptibility of chelonians to ranaviruses differs among developmental stages similar to amphibians . Some outbreaks in box turtles have involved translocation events that congregate many individuals, resulting in high infection prevalence and death (Belzer and Seibert 2011 ;Farnsworth and Seigel 2013 ;Kimble et al 2014 ). In a multiyear survey of box turtles in the USA, ranavirus prevalence has not been reported above 5 % in a population without abnormal mortality events (Allender et al 2013 ).…”