Water Temperature Affects Susceptibility to Ranavirus

Abstract

The occurrence of emerging infectious diseases in wildlife populations is increasing, and changes in environmental conditions have been hypothesized as a potential driver. For example, warmer ambient temperatures might favor pathogens by providing more ideal conditions for propagation or by stressing hosts. Our objective was to determine if water temperature played a role in the pathogenicity of an emerging pathogen (ranavirus) that infects ectothermic vertebrate species. We exposed larvae of four amphibian species to a Frog Virus 3 (FV3)-like ranavirus at two temperatures (10 and 25°C). We found that FV3 copies in tissues and mortality due to ranaviral disease were greater at 25°C than at 10°C for all species. In a second experiment with wood frogs (Lithobates sylvaticus), we found that a 2°C change (10 vs. 12°C) affected ranaviral disease outcomes, with greater infection and mortality at 12°C. There was evidence that 10°C stressed Cope's gray tree frog (Hyla chrysoscelis) larvae, which is a species that breeds during summer-all individuals died at this temperature, but only 10% tested positive for FV3 infection. The greater pathogenicity of FV3 at 25°C might be related to faster viral replication, which in vitro studies have reported previously. Colder temperatures also may decrease systemic infection by reducing blood circulation and the proportion of phagocytes, which are known to disseminate FV3 through the body. Collectively, our results indicate that water temperature during larval development may play a role in the emergence of ranaviruses.

Environmental Drivers of Ranavirus in Free-Living Amphibians in Constructed Ponds

“…Water temperature was included in all best fit candidates for both models and produced negative trends with respect to FV3 prevalence. This was in contrast to controlled studies supporting positive trends (Bayley et al 2013; Brand et al 2016). However, unlike in laboratory settings, temperature levels fluctuated with daily and seasonal cycles and were not controlled and/or stable in these wild populations.…”

“…In regards to specifically FV3 and anuran ranid species (which includes L. sylvaticus and L. clamitans ), research has produced conflicting results. Many controlled studies supported a positive correlation, with higher mortality rates at warmer temperatures (Bayley et al 2013; Brand et al 2016). In contrast, Echaubard et al (2014) and Gray et al (2007) found that probability of both infection and mortality was lower at warmer temperatures.…”

“…Although both L. sylvaticus and L. clamitans have relatively high probabilities of infection and mortality when exposed to FV3, we expect highest prevalence rates overall in L. sylvaticus (Hoverman et al 2011). Water temperature produces different results with respect to infectivity and mortality, depending on both Ranavirus strain and host species (Rojas et al 2005; Bayley et al 2013; Echaubard et al 2014; Brand et al 2016). In regards to specifically FV3 and anuran ranid species (which includes L. sylvaticus and L. clamitans ), research has produced conflicting results.…”

Heterogeneities in the infection process drive ranavirus transmission

“…Perhaps tadpoles only succumb to infection when environmental conditions deteriorate (e.g., high temperatures; Brand et al. ), or during a critical window of vulnerability during development (Warne et al. ).…”

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

“…Ranavirus infections of amphibians are notifiable to the World Organization for Animal Health due to their potential to cause severe disease outbreaks as well as the risks of international spread through trade (Schloegel, Daszak, Cunningham, Speare, & Hill, 2010;Schloegel et al, 2009). Ranavirus growth and virulence can be affected by temperature (Ariel et al, 2009;Bayley, Hill, & Feist, 2013;Brand et al, 2016;Rojas, Richards, Jancovich, & Davidson, 2005) and environmental temperature is considered to be one possible explanation for observations of seasonality in outbreaks (Brunner, Storfer, Gray, & Hoverman, 2015). Indeed, incidents of ranavirosis in frogs in the USA were recently shown to be uncoupled from a pulse in transmission or the density of susceptible hosts, and instead were coincident with temperature increases and developmental changes in frog larvae (Hall, Goldberg, Brunner, & Crespi, 2018).…”