Susceptibility of Fish and Turtles to Three Ranaviruses Isolated from Different Ectothermic Vertebrate Classes

Abstract

Ranaviruses have been associated with mortality of lower vertebrates around the world. Frog virus 3 (FV3)-like ranaviruses have been isolated from different ectothermic vertebrate classes; however, few studies have demonstrated whether this pathogen can be transmitted among classes. Using FV3-like ranaviruses isolated from the American bullfrog Lithobates catesbeianus, eastern box turtle Terrapene carolina carolina, and Pallid Sturgeon Scaphirhynchus albus, we tested for the occurrence of interclass transmission (i.e., infection) and host susceptibility (i.e., percent mortality) for five juvenile fish and three juvenile turtle species exposed to each of these isolates. Exposure was administered via water bath (10(3) PFU/mL) for 3 d and survival was monitored for 28 d. Florida softshell turtles Apalone ferox experienced no mortality, but 10% and 20% of individuals became infected by the turtle and fish isolate, respectively. Similarly, 5% of Mississippi map turtles Graptemys pseudogeographica kohni were subclinically infected with the turtle isolate at the end of the experiment. Channel Catfish Ictalurus punctatus experienced 5% mortality when exposed to the turtle isolate, while Western Mosquitofish Gambusia affinis experienced 10% mortality when exposed to the turtle and amphibian isolates and 5% mortality when exposed to the fish isolate. Our results demonstrated that interclass transmission of FV3-like ranaviruses is possible. Although substantial mortality did not occur in our experiments, the occurrence of low mortality and subclinical infections suggest that fish and aquatic turtles may function as reservoirs for FV3-like ranaviruses. Additionally, our study is the first to report transmission of FV3-like ranaviruses between fish and chelonians.

Ranavirus Ecology and Evolution: From Epidemiology to Extinction

“…For example, morbid fi sh and turtles have been reported in association with amphibian die-offs due to ranaviral disease Farnsworth and Seigel 2013 ). Moreover, several laboratory studies have demonstrated that BIV and FV3-like viruses isolated from one vertebrate class could be used to experimentally infect animals in another (Moody and Owens 1994 ;Ariel and Owens 1997 ;Bang Jensen et al 2009, 2011bGobbo et al 2010 ;Bayley et al 2013 ;Brenes et al 2014b ). Recently, Brenes et al ( 2014a ) paired ranavirus-exposed and -unexposed hosts from different vertebrate classes on opposite sides of a fi ne mesh screen, preventing direct contact but allowing water and virions to pass through.…”

“…Until the recent studies by Brenes et al ( 2014a , b ), comparative studies involving reptiles were generally lacking, and those involving fi sh are largely restricted to EHNV (Becker et al 2013 ;Langdon 1989 ; but see Brenes et al 2014b ). Note, however, that several recent studies have exposed different fi sh species to multiple ranaviruses from fi sh and amphibians, so collectively information is accumulating on the relative susceptibility of fi sh (Bang Jensen et al 2009, 2011aGobbo et al 2010 ;Brenes et al 2014b ).…”

Design and Analysis of Ranavirus Studies: Surveillance and Assessing Risk

“…For example, if experimental exposures show that a species dies rapidly following ranavirus exposure, then high prevalence would be most consistent with sampling during the peak of an epidemic. Several studies have reported species-level susceptibility under controlled conditions (e.g., Hoverman et al 2011;Brenes et al 2014b;Brunner et al 2015). Biological context also can be gleaned from the density of the population and the timing of the survey relative to the phenology of the organism.…”

“…Given the apparent correlation between disease-related mortality and infection prevalence with FV3-like ranaviruses Hoverman et al 2011;Brenes et al 2014b), suggested that prevalence >40 % in amphibian populations might signal that an outbreak is occurring. Although these rules of thumb may be useful in interpreting prevalence levels, we urge caution in interpreting prevalence data outside of the broader biological context.…”

“…If funds are limited, a viable strategy would be to test amplification hosts, because these species tend to have lower resistance to ranavirus, and detection probabilities are therefore greater. Duffus et al (2015) provide a list of known ranavirus hosts, and several challenge studies (e.g., Hoverman et al 2011;Brenes et al 2014b) can provide insight into relative difference in susceptibility between species.…”