What’s climate change got to do with frog ebola?

For ten years I’ve been working on a viral disease of amphibians (and sometimes reptiles and fish) caused by ranaviruses. We’ve just published some new research showing how changes to the climate have been facilitating the spread of this disease and leading to some very serious outcomes for UK frogs. This blog post briefly covers the background to this important wildlife disease and the findings of this latest research.

THE PROBLEM:

• Ranavirus disease (ranavirosis) is a pretty nasty viral disease in frogs, typified by systemic haemorrhaging
  • what that means is the frogs bleed throughout their bodies, something akin to what can be seen in the human disease caused by ebola virus.
• Diseased animals usually die.
• The disease is already widespread in England, where it kills the adult frogs, and has been shown to have caused population numbers to decline by more than 80% in ponds in south-east England within a decade.

FUNDAMENTAL FINDINGS: We showed that warmer temperatures help the virus grow and make it more virulent, more deadly if you like. In the wild, this has led to more frequent outbreaks of disease that each killed more frogs on average.

CLIMATE CHANGE: With respect to climate change, these were our key findings:

1. Climate change has already had an impact on this disease. Looking at the last few decades, the rate of outbreaks tracked temperatures, so during warmer years there were more outbreaks of disease
2. The things we’ve learned about what has already been happening give us a good basis to make predictions about how the future will unfold. When we did that we found a couple of things:
   • One is that climate change will help the disease to spread and we can expect to see these big frog die-offs happening across more of the UK. The disease is already pretty widespread in England but will expand northwards and westwards, affecting frogs in more of England as well as Scotland and Wales
   • The second thing is that the length of the disease season will increase. At the moment we mostly see disease during the warm summer months but going forwards conditions could become suitable for disease in April in the south of England. This is when tadpoles and froglets are still in the pond and would almost certainly mean we’d start to see them dying as well as the adults. If that meant that the adults that died were no longer replaced, then those frog populations could disappear almost overnight.

FROGS: And just to say what I mean by frogs here so that there’s no confusion. The species we’ve been studying is the common frog, which is the only frog that people commonly find in the UK. So when I’m talking about frogs disappearing, it’s not like it’s one type of frog and people will continue to see other types…we’re talking about ALL frogs.

A POSITIVE: This is all obviously pretty depressing and extremely worrying BUT some of our results hinted at possible mitigation measures. Where frogs had the means to stay cooler via shading or deep ponds, things weren’t so bad. It might be that if people start making their garden ponds more like a natural pond, with shading and a range of depths and dedicated to wildlife, instead of bowls full of fish (which can also make disease outcomes worse) surrounded by paving, we might give frogs a better chance of being able to tolerate infections.

TAKE HOME MESSAGES:

• People are generally pretty aware that the climate in the UK is changing and are probably used to headlines about the “hottest temperatures on record” and such, but this study shows how climate change has already impacted our wildlife and is changing the make up and appearance of our environment, even the animals we encounter in our back gardens. This situation is very likely to worsen.
• Although climate change has been a gradual process, the suggestion here is that the impacts won’t always be gradual. Predicting the future of complex ecological interactions is really difficult but we’ve been able to unpack some of the complexity in this system and it looks like the effect of climate change on this disease could reach a tipping point, which would mean that frogs disappear almost overnight in some places.
• Our study also shows a pretty indirect effect of climate change on wildlife and how climate change can act synergistically with other threats/factors, which can make it hard to predict the impacts.

BIG PICTURE: I think you can look beyond this study and generalise our findings. Science is just beginning to comprehend the astonishing amount of viral diversity that surrounds us, but has previously gone undescribed. Environmental change means that new threats to wildlife and human health will emerge that we don’t really have adequate means to predict.

You can find links to the complete research paper here

Citation: Price SJ, Leung WTM, Owen CJ, Puschendorf R, Sergeant C, Cunningham AA, Balloux F, Garner TWJ & RA Nichols (2019). Effects of historic and projected climate change on the range and impacts of an emerging wildlife disease. Global Change Biology. https://doi.org/10.1111/gcb.14651

Ranavirus & amphibian community collapse – commentary

With a particular multi host pathogen on the tip of everyone’s tongue at the moment (see my blog on public health consequences of ebola emergence) my own work on a deadly virus which has been wreaking havoc among amphibian communities was just published in Current Biology.

Ebola is grabbing the headlines for its capacity to cause gruesome disease in humans (which usually ends in death), for its rapid emergence over the course of the 2014 outbreak, and for the recent exports of infection to distant parts of the world. My paper in Current Biology will naturally fail to generate the same level of excitement due to the affected host species but, nevertheless, it reports on some fairly terrifying viruses.

In a nutshell, we show that a recently discovered lineage of Ranavirus seems to have been introduced to northern Spain with catastrophic consequences for amphibian host communities. Common midwife toad virus (CMTV) and its relative Bosca’s newt virus (BNV) appear to have pre-existing capacity to infect and cause severe disease (which, like Ebola, can be characterised by systemic haemorrhaging, aka vomiting blood) in pretty much any amphibian they come across and reptiles too. We have recorded simultaneous and rapid declines of three amphibian species in the Picos de Europa National Park (PNPE) since disease was first observed there in 2005 as well as mass die-offs covering all the other common amphibian species present and representing a remarkable diversity of hosts.

The PNPE is a pretty unusual place to find this emerging pathogen when it’s not been reported elsewhere in Spain. in the UK the ranavirus disease we know about has tended to be focused in domestic garden ponds. In China it’s mostly reported in amphibian farms, but the PNPE is protected and pretty wild. Some of our study sites are remote, only visited by the occasional hiker or shepherd. So how it got there is a bit of a mystery but it’s hard to look past a big role for humans.

BNV turned up at a reservoir about 200km away from the PNPE in 2010 and has been hammering two amphibian species there ever since. But perhaps more incredible was the discovery of a dead snake (Natrix maura) at the site which had been feeding on the infected amphibians. The snake was similarly diseased and infected with BNV.

Our findings are important on two fronts. We document a serious threat to amphibian conservation in light of the rapid declines we have observed and the likelihood that CMTV is emerging elsewhere in Europe. A pathogen that can utilise a number of available hosts has the potential to drive local extinctions, since it is able to persist in an alternative host even when numbers of any preferred host species collapse and eventually reach zero. We have also begun to characterise what we think could be an excellent model system for understanding an aspect of what equips a pathogen to exploit multiple and diverse hosts.

Some of the key questions about our research:

Ranaviruses have been linked to disease and mortality in amphibians over the last couple of decades. What’s exceptional about the mortality in Spain?

It’s true that ranavirus infection is often associated with severe disease and die-offs in amphibians. However amphibian declines have only previously been documented in a single species (common frogs in the UK). We have shown that at least three species have undergone simultaneous population collapses in the Picos de Europa National Park (PNPE) and that all the common species present seem to be highly susceptible. We have found a related virus in Galicia that is not only extremely virulent for amphibians but also killed a snake that had been feeding on them. So the breadth of the observed host range is pretty exceptional and more so because of the severe impact observed in all these different hosts.

How many animals have died?

It’s not really possible to say how many have died but our data does give us a clear idea of the magnitude of the declines, which are in the range of 60% to nearly 100%.

Is it possible that some amphibians in Spain might become extinct?

Yes, local extinctions at individual sites are certainly a possibility in the short term. These viruses seem to have the capacity to infect the entire amphibian community. That means that even when one host is reduced to low numbers, the virus can persist in alternative hosts and continue to exploit the remaining individuals of the rare species whenever it’s possible. The reduction in numbers to the low levels that we’ve shown for some populations also makes them vulnerable to stochastic events such as a late spring.

How did these viruses arrive in the region?

We don’t know that yet, but our findings do provide some clues. The park staff are continually monitoring the park habitat. The disease and level of mortality are striking so we can be confident that it hadn’t gone unnoticed for long prior to the first observed events in 2005. Also, we found three viruses which, in the context of overall ranavirus diversity, are more different than would normally be explained by diversification in Spain alone; these ‘Spanish’ viruses are more closely related to viruses from China than to each other. Finally, we have seen almost simultaneous emergence at multiple sites across the park which are separated by many miles of rugged, mountainous terrain and on the whole this scenario is not really consistent with amphibians moving the virus around the park. When you put these three things in the broader context of what we know about ranavirus translocations – for example, the fact that ranaviruses are present in traded and farmed amphibians – it seems likely that humans are responsible for the introductions.

Amphibians have already been hit hard by another pathogen, the chytrid fungus. Are they a particularly vulnerable group?

Amphibians do seem vulnerable right now, they are the most threatened vertebrate group on earth (though I don’t think reptiles are far behind). Their challenges come in many forms though, not just disease, and the fact that many species rely on both land and freshwater to complete their life-cycles probably does expose them to more risks and environmental impacts. Amphibians have fairly sophisticated immune systems incorporating both the innate and adaptive components (at least in adults) that also characterise human immunity so they’re not particularly vulnerable in that respect.

How can we stop these declines?

To prevent or limit further introductions it’s important to reconstruct virus movement. This is a challenge to be addressed at a global as well as a local scale and is something that i’m working on. In terms of what can be done at infected sites, it’s very difficult to see how this can be tackled, but it’s important to raise awareness about actions which are likely to move infectious materials around. Some progress has been made on this front with clear protocols now in place for biologists in terms of disinfecting equipment.

Why should people care about amphibians?

They’re such a weird and wonderful group with fantastic individual stories (for example, great examples of parental care) and I think they play a memorable part in the childhoods of many people…dipping for tadpoles and taking them home to rear through metamorphosis. At the same time they play key roles in ecosystems; they’re the “gardener’s best friend” because they eat slugs and other species we consider as pests whilst the dead snake in our paper indicates their role when you travel the opposite direction in a food chain! Then you’ve also got the general arguments for why biodiversity loss matters: the stuff we don’t yet know, the potential for human tech/medical advances, biomimicry, and so on.

Massive thanks to Jaime, Amparo, and the team of PNPE rangers who have compiled an amazing dataset charting demographic change among amphibian communities through their commitment to conservation and research. And also to Cesar Ayres for the hours he’s put in counting carcasses in Galicia!

The PNPE ranger team:
J.J. Alonso, I. Alonso, M.A. Bermejo, S. Casares, M. Dıaz, J.E. Dıez, P. Fernandez, M. Fernandez, S. Gonzalez, S. Marquınez, J.J. Martınez, J.L. Mosquera, C. Obeso, F. Rojo, A. Tejedor, and R. Varona.