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Tadpole Deaths Prompt Research into Viral Vernal Pools

Ranavirus might be part of normal dynamics of vernal pools
9/11/2009

In mid-June 2006, just about the time larval spotted salamanders and wood frog tadpoles should emerge from vernal pools onto land as new adults, Adirondack Ecological Center researcher Stacy McNulty instead stumbled upon a die-off. Scores of dead and dying tadpoles were found in several vernal pools. The juvenile amphibians swam weakly if at all, and their gill areas were red and swollen with blood.

When a die-off occurred again in 2008, I collected several individuals from each pool. I thought that what we were seeing was caused by a virus, a ranavirus. I extracted DNA from these animals and, using primers that recognized a DNA sequence found only in ranaviruses, amplified part of a gene that makes up the viral coat. This was strong evidence that a ranavirus was involved in these die-offs.

Allan Granoff, a virologist at St. Jude's Children's Research Hospital, first isolated an amphibian ranavirus in 1962 while he was following up on a novel hypothesis that tumors, particularly a common renal carcinoma of leopard frogs, were caused by a virus. Granoff did not find the virus he was looking for (a herpesvirus called Lucke tumour herpesvirus, later renamed Rana herpesvirus 1, the first herpesvirus known to cause cancer), but he did isolate a novel virus, which he called Frog Virus 3 (FV3). FV3 became the "type" virus for the genus Ranavirus, a group of DNA-based viruses that infect cold-blooded vertebrates such as fish, amphibians, and reptiles.

Initially, amphibian ranaviruses were thought to be fairly benign. FV3, for instance, was found in an apparently healthy frog. But a series of disease outbreaks among commercially and recreationally important fish, cultured and wild frogs, and an endangered salamander began to change this view. Ranaviruses have been identified in catastrophic die-offs in aquaculture and in wild populations around the world, although there is little evidence that these viruses cause widespread population declines, unlike the Chytrid fungus that is devastating global amphibian populations.

What we saw in the pools of the Huntington Wildlife Forest, however, makes one wonder. Die-offs can kill every individual in a pool, essentially wiping out a year's reproductive effort. While these amphibians can live for two to five years, successive die-offs might result in local extinctions.

How do these ranaviruses persist long enough to cause successive die-offs if they wipe out their hosts? We know that a ranavirus of tiger salamanders called ATV cannot tolerate drying in pond sediment, so it seems unlikely that this virus persists in the pool itself. Another possibility is that the ranavirus persists in sublethally infected adults. In my dissertation, I demonstrated how chronically infected adult tiger salamanders could reintroduce ATV into ponds in Arizona when they returned to breed, sparking epidemics in the new larval population. Others have shown that FV3, like the one I identified at HWF, can cause sublethal infections in the African clawed frog.

With die-offs occurring in 2008 and 2006, and an unconfirmed instance in 2000, it appears that this ranavirus might be part of the normal dynamics of vernal pool communities. Vernal pools usually exist in semi-connected networks. When the population in a given pool is extirpated because of repeated years of failed breeding or because of ranavirus epidemics, we expect that it will eventually be recolonized by neighboring populations. As long as pathogens like FV3 do not spread between vernal pools readily and the ponds are not isolated by roads or clearcuts, the overall metapopulation persists. And sometimes even a mass die-off does not get every animal; in 2008 some wood frogs survived and metamorphosed in virus-affected pools. Stacy and I will be watching to see what happens to these ponds in 2009.

- By Jesse Brunner, Department of Environmental and Forest Biology

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