Ranavirus Infection of Free-Ranging and Captive Box Turtles and Tortoises in the United States

Abstract

ABSTRACT:Iridoviruses of the genus Ranavirus are well known for causing mass mortality events of fish and amphibians with sporadic reports of infection in reptiles. This article describes five instances of Ranavirus infection in chelonians between 2003 and 2005 in Georgia, Florida, New York, and Pennsylvania, USA. Affected species included captive Burmese star tortoises (Geochelone platynota), a free-ranging gopher tortoise (Gopherus polyphemus), free-ranging eastern box turtles (Terrapene carolina carolina), and a Florida box turtle (Terrepene carolina bauri). Evidence for Ranavirus infection was also found in archived material from previously unexplained mass mortality events of eastern box turtles from Georgia in 1991 and from Texas in 1998. Consistent lesions in affected animals included necrotizing stomatitis and/or esophagitis, fibrinous and necrotizing splenitis, and multicentric fibrinoid vasculitis. Intracytoplasmic inclusion bodies were rarely observed in affected tissues. A portion of the major capsid protein (MCP) gene was sequenced from each case in 2003-2005 and found to be identical to each other and to Frog virus 3 (FV3) across 420 base pairs. Ranavirus infections were also documented in sympatric species of amphibians at two locations with infected chelonians. The fragment profiles of HindIIIdigested whole genomic DNA of Ranavirus, isolated from a dead Burmese star tortoise and a southern leopard frog (Rana utricularia) found nearby, were similar. The box turtle isolate had a low molecular weight fragment that was not seen in the digestion profiles for the other isolates. These results suggest that certain amphibians and chelonians are infected with a similar virus and that different viruses exist among different chelonians. Amphibians may serve as a reservoir host for susceptible chelonians. This report also demonstrated that significant disease associated with Ranavirus infections are likely more widespread in chelonians than previously suspected.

Ranavirus Ecology and Evolution: From Epidemiology to Extinction

“…While several outbreaks in free-ranging chelonians have been observed (Allender et al 2006 ;Johnson et al 2008 ;Belzer and Seibert 2011 ;Farnsworth and Seigel 2013 ), there are no similar reports of ranaviruses in free-living populations of other reptile taxa. Unlike in fi sh and amphibians, ranavirus outbreaks in chelonians, at least in North America, are more diffuse.…”

“…Most individuals that are infected will die within several weeks, so the prevalence of infection at any given point in time is low. For instance, 15 of 71 (21 %) free-ranging eastern box turtles ( Terrapene carolina carolina ) died during a ranavirus die-off at a private nature sanctuary in Pennsylvania, USA (Johnson et al 2008 ;Belzer and Seibert 2011 ). The following year only one of the 55 surviving turtles was seropositive, strongly suggesting that the vast majority of infected individuals died (Johnson et al 2010 ).…”

Distribution and Host Range of Ranaviruses

“…In addition to the box turtle cases described above, several other reports of FV3-like infections have been seen in captive chelonians (Marschang et al 1999 ;De Voe et al 2004 ;Benetka et al 2007 ;Johnson et al 2008 ;Blahak and Uhlenbrok 2010 , Table 4 ). Ranavirus infections were described in two juvenile diseased Hermann's tortoises ( Testudo hermanni ) in Germany using PCR.…”

“…Both appeared to be FV3-like based on partial MCP gene sequences and restriction endonuclease analysis (Mao et al 1997 ). No clinical information on those two chelonians was Allender et al 2006 ;Johnson et al 2008 ;Allender 2012 , Table 4 ). Although ranavirus detection in chelonians has been reported most frequently, detection of these viruses in lizards and snakes has been increasing, mostly from captive populations (Stöhr et al 2013b ;Behncke et al 2013 ;Marschang 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 ).…”