Amphibian Chytrid Crisis: A Deep Dive into a Deadly Disease

Guest post by Tristan Williams, MEnvSc Candidate at the University of Toronto-Scarborough

We currently live in an era of mass extinction, where many species around the world are at high risk of being lost forever, and among these species, amphibians are at much higher risk of extinction than any other (Wake and Vrendenburg, 2008). This comes from a combination of many factors, including climate change, habitat destruction and human land use, the presence of invasive species, and as we’ll be looking at here: the fungal infection chytridiomycosis.

Chytridiomycosis is a skin disease caused by a chytrid fungus, either Batrachochytrium dendrobatidis (Bd), or Batrachochytrium salamandrivorans (Bsal). Though these fungi may be small, they are a big deal when it comes to the health and stability of amphibian populations. They have been implicated for the heavy decline or even outright extinction of a large number of amphibian species, making it potentially the most impactful wildlife disease known (Scheele et al., 2014). These fungi have a number of traits that make it easy for them to spread to amphibians. One such trait is the ability to reside within a host without causing infection, using it as a reservoir from which it can spread to more vulnerable species (Fisher, 2017). This can be seen in the example of the midwife toad and alpine newt, which are carriers for Bsal, and can lead to infection of fire salamander populations.

Figure 1: Potential pathways for the spread of Bsal in Europe, from Fisher 2017.

The zoospores of these fungi also have two forms which contribute to their spread among amphibian population. The first is the motile aquatic form, which allows them to establish infection during the tadpole stage (Fisher, 2017). The second is the non-motile form, called an encysted spore, which has a thick cell wall, and are highly resilient. These encysted spores are capable of persisting in the environment while retaining their infectiousness, without needing a host at all for a long period of time. And if that wasn’t enough, it could be the case that birds can act as carriers for these encysted spores, bringing the fungus to new locations and further contributing to the spread of disease over larger distances. As noted by Fisher et al. (2017), it really does seem like amphibians really are in peril from a perfect pathogen. But what exactly do these fungal infections do to amphibians that make it such a problem?

Amphibians are cutaneous respirators. They “breathe” through their skin, allowing them to maintain the correct osmotic balance of electrolytes and water within the body. This is what makes chytrid fungi such a unique threat to amphibians. To other organisms the development of a cutaneous chytrid infection is usually not a big deal, but to amphibians it can directly interfere with their ability to respire (Voyles et al., 2009). The ensuing loss of electrolytes impairs the ability of the heart to function, blood flow to the rest of the body is reduced, and cardiac arrest leads to death as a result of complete collapse of the circulatory system. However, even before that occurs, the now physically impaired and lethargic individual is likely to become a victim of predation or a combination of other stressors as well. As an example of the potential severity of this disease, fire salamanders in the Netherlands that were infected with Bsal experienced a mortality rate of over 96% (Fisher, 2017). A very morbid and unfortunate situation our amphibian friends find themselves in.

Normally, the mucus layer present on the skin of amphibians contains a number of antimicrobial peptides and lysozymes, as well as symbiotic bacteria which all contribute to innate defenses against invading pathogens (Rollins-Smith et al., 2011). Amphibians have also shown to be capable of developing an acquired immune response to chytrid fungi after exposure, with some even developing Bd specific antibodies. So then why is chytridiomycosis such a problem for amphibians? The answer appears to be because chytrid fungi are capable of suppressing immune responses in many species before these defenses are capable of protecting against infection (Ellison et al., 2014). Other environmental stressors can also interfere with the ability of amphibians to mount an appropriate immune defense. Lack of food resources, temperature stress, or exposure to chemicals like pesticides can all increase the likelihood of fungal infection (Rollins-Smith et al., 2011). Furthermore, the amphibian life cycle itself can impair the ability of an individual to resist infection. When a tadpole undergoes metamorphosis into an adult, the immune system also goes through a drastic transition to maturity. This period of time provides an opening for infection to develop while the defenses of the amphibian aren’t at full capacity. Ultimately, this means that the ability for a species of amphibian to defend against chytrid fungi varies heavily based on the level of innate and acquired defenses mounted, the health of the habitat, the climate, and what part of the life cycle the species in question is in.

 It is abundantly clear that amphibian populations are in great danger as a result of this disease outbreak, so the obvious follow-up question is what can we do about this ongoing threat? While there is no silver bullet for stopping chytridiomycosis outright, there are a number of potentially promising forms of intervention that could help to bring mortality rates down to less extreme levels. In short-term or small scales, the direct treatment of individuals with antifungals is shown to be an effective method of temporarily controlling an outbreak, but more long-term measures are needed to ensure success in restoring populations (Garner et al., 2016). Scheele et al. (2014) provide a framework of three potential classes of action to protect amphibians from fungal infection. The first class is Environmental Manipulation. As mentioned previously, there are a number of environmental factors that influence the chance of successful infection. Reducing the presence chemical pollutants can reduce stress on amphibian populations are lower infection rates. The creation of warm regions in the habitat, such as warm pools of water, areas of high sun exposure to bask in, or the introduction of artificial heat sources can also allow species to initiate behavioural fever, raising their body temperature to levels that are no longer ideal for chytrid fungi to survive. Finally, methods such as bio-augmentation, which involves introducing microbes with the ability to inhibit chytrid fungi to the environment, can potentially provide an ecosystem-wide treatment, so long as proper testing is done to ensure that this will not negatively impact the environment in any way. 

Artificial ponds for the captive breeding of the endangered Pseudophryne corroboree.

(Figure 2 from Scheele et al., 2014)

When manipulation is not a reasonable solution, the Amphibian Introduction class is next in line. This involves the translocation of amphibian populations to refugia: environments that are ideal for the species, but poor for chytrid fungus. This method does require that it is ensured that this translocation will not cause any impacts in the new environment. Alternatively, captive bred amphibians can be added to wild populations in order to increase the buffering capacity of the ecosystem, allowing higher likelihood of survival for a population even after an chytrid epidemic. Finally, failing the previous two classes, the last class is Ex-Situ Conservation, which involves keeping colonies in captivity. Infected individuals are treated with chemicals or heat to kill the fungus, and individuals are bred in order to improve resistance among the population while maintaining genetic diversity (Scheele et al. 2014).

While these treatments are still in development and have not been used in proper field tests yet, they definitely have the potential to rescue amphibian populations. However, the fact remains that many amphibians around the world are critically imperilled, so there is clear need for feasibility research as soon as possible if we want to prevent any more extinctions. The loss of mass amounts of amphibians could lead to huge impacts on many ecosystems around the world, and it is all but guaranteed to happen unless we take action.

Literature Cited:

Ellison AR et al. 2014. Fighting a Losing Battle: Vigorous Immune Response Countered by Pathogen Suppression of Host Defenses in the Chytridiomycosis-Susceptible Frog Atelopus zeteki. G3-Genes Genom Genet 4(7): 1275-1289.

Fisher MC. 2017. Ecology: In peril from a perfect pathogen. Nature 544(7650): 300-301.

Garner TWJ et al. 2016. Mitigating amphibian chytridiomycoses in nature. Philos T Roy Soc B 371(1709).

Rollins-Smith LA et al. 2011. Amphibian Immune Defenses against Chytridiomycosis: Impacts of Changing Environments. Integr Comp Biol 51(4): 552-562.

Scheele BC et al. 2014. Interventions for Reducing Extinction Risk in Chytridiomycosis-Threatened Amphibians. Conserv Biol 28(5): 1195-1205.

Voyles J, et al. 2009. Pathogenesis of Chytridiomycosis, a Cause of Catastrophic Amphibian Declines. Science 326(5952): 582-585.

Wake DB and Vredenburg VT. 2008. Are we in the midst of the sixth mass extinction? A view from the world of amphibians. P Natl Acad Sci USA 105(1): 1466-1473.

Carbon sequestration in boreal forests: below-ground interactions matter

K. E. Clemmensen, A. Bahr, O. Ovaskainen, A. Dahlberg, A. Ekblad, H. Wallander, J. Stenlid, R. D. Finlay, D. A. Wardle, B. D. Lindahl. Roots and Associated Fungi Drive Long-Term Carbon Sequestration in Boreal Forest. 2013. Science. Vol. 339 no. 6127 pp. 1615-1618. DOI:10.1126/science.1231923 

One of the most important developments in plant ecology over the last 20 or so years is the inclusion of belowground interactions with fungi into traditional studies of plant diversity, productivity, and ecosystem functions. Results like those from van der Heijden (1998)--which showed experimentally that the assumed link between ecosystem function and plant diversity was actually driven by arbuscular mycorrhizal fungal diversity (through their effects on plant communities)—must alter how we see plant community dynamics. Not only does this reinforce the importance of complexity in ecology, but more specifically it suggests that if fungi are a necessary component of plant community identity and function, they must be explicitly considered in management and conservation plans.

For example, an important current issue is the question of which ecosystems will be carbon sinks as part of a focus on atmospheric CO2 levels. Understanding the mechanisms by which carbon is stored is therefore an important topic. Boreal forests sequester net amounts of carbon in soil and it is generally assumed that this is as a result of plant litter and organic matter accumulating in soil. Clemmensen et al. (2013) examined soil chronosequences for forested islands in Sweden to test whether this hypothesis held. These islands differed in the frequency of fire occurrences, between large and frequently burnt islands and smaller, infrequently burnt islands.

The authors identified the age since fixation of C found in the chronosequences and used models of C source to look at the relative contribution of the two possible processes: either fixation of C through aboveground plant litter or below-ground inputs through root-associated fungi. Carbon input tended to be higher on the small islands that were burnt less often, and this was associated entirely with root-derived input. Further, DNA barcoding showed that on these small islands, there were mycorrhizal fungi associated with the soil depths where the root-derived inputs were occurring. On islands which burned more frequently, and had lower carbon input, fungi were absent at these depths (figure below). This difference in fungal profile was related to the fact that infrequently burnt islands had older mycelium with low turnover, hence greater carbon sequestration.

From Clemmensen et al (2013). A) Fungal functional groups associated with soil depths on large, frequently burnt islands (panel 1) and small, infrequently burnt islands (panel 2).

The authors convincingly show that, at least in some ecosystems, the view that decomposition of litter primarily drives humus accumulation (and the accompanying carbon sequestration) must be tempered with the knowledge that organic layers also accumulate from below by roots and root-associated fungi. This suggests that there is a need to consider fungal communities as well as plant communities for when managing forests and making inventories of global carbon stores. And probably a need to consider fungi much more often in general.

Biodiversity and ecosystem functioning - only with fungi

Once again scientists have come to an age-old conclusion: fungus is behind all of life’s great mysteries. It's responsible for curing strep throat, delicious veggie burgers, that unique musk emanating from your gym bag, the colour-morphing walls at last night’s party and now, biodiversity and ecosystem functioning.

The world of biodiversity and ecosystem functioning (BEF), like many other high-profile disciplines of science, has often been bogged down by controversy. In such situations, we often spend a disproportionate amount of time focusing on the controversy instead of actually advancing the science itself (sound familiar?)

There have been several posts about BEF on this blog in the last few months, but briefly and oversimplified, here's how it works. Ecosystem functions are things like productivity, nutrient cycling and decomposition. Ecosystems that contain many species produce higher levels of these functions than monocultures do. The controversy here surrounds the cause of this phenomenon. In the 1990s, researchers originally disagreed over whether the relationship they observed was due to complementarity (different species partitioning resources) or selection effects (the higher chance of a really productive species being included in a community with many species). The question was largely settled a few years ago; selection effects do exist, but most of the relationship is driven by complementarity. Nonetheless, many biologists who are only tangentially familiar with this area of research are unaware of the consensus and continue to believe that the issue remains unresolved. Some still dismiss the whole field of BEF because of selection effects. I guess people just love a controversy.

The result of all this is that the ecologists studying these relationships have had to spend an undue amount of time parsing their results into selection and complementarity and discussing the two phenomena. They have even come to refer to these as the “mechanisms” behind BEF. And this is where we start to have a problem. Selection and complementarity are not mechanisms - they are symptoms of mechanisms. They do not tell us what is actually causing the positive effect that biodiversity has on ecosystem functioning, only what the shape of the relationship is. In fact, very few studies have actually looked for true mechanisms that explain the effects that we have repeatedly observed.

But this week I read a new paper in Ecology Letters that actually did find a mechanism, and it wasn’t one that we expected. John Maron and his coauthors at the universities of Montana and British Columbia found that belowground fungi were causing plant productivity to increase with diversity.

In an impressively complete experiment, Maron et al. put together a classic BEF setup of many plots containing varying levels of plant diversity and then measured plant biomass. But this time they added a twist; they applied fungicide to the soil in some of these plots. The result was that in the absence of fungi, the common BEF relationship disappeared. The low diversity plots became much more productive, while productivity at high diversity only increased slightly. The authors explained their results by the fact that fungi can be both species-specific and density-dependent, so as plant diversity increases, the fungi’s negative impact on plant productivity diminishes. And for good measure, they of course also ruled out a significant selection effect in their results.

So what does this all mean? Well for one thing, it means that we now have at least one good mechanistic explanation for that black box that we’ve been calling “complementarity” for years. But perhaps more importantly, it means that the link between biodiversity and ecosystem functioning is now more real than ever. If plant species go extinct, the remaining ones will be more susceptible to fungal pathogens and productivity will decline. So let’s try to not let that happen, k?

Maron, J. L., Marler, M., Klironomos, J. N. and Cleveland, C. C. , Soil fungal pathogens and the relationship between plant diversity and productivity. Ecology Letters, DOI: 10.1111/j.1461-0248.2010.01547.x

Mycorrhizal Networks: Socialists, capitalists or superorganisms?

Mycorrhizal networks – fungal mycelium that colonize and connect roots of one or more plant species – are a very intriguing type of fungal-plant association. There is evidence of substantial facilitation between plant individuals via these fungal networks. This can have drastic implications for our understanding of nature, given that the common perception is that other mechanisms, like competition, herbivory or dispersal, are the main drivers of plant community associations. This may be far from reality if the existence of “socialist” networks is widespread (e.g. the ability to connect and profit from a network may be more important than competitive abilities). In the last issue of the Journal of Ecology ( that has a very interesting special feature on facilitation in plant communities), Marcel Van der Heijden and Tom Horton conducted a review of the topic. They found a general positive effect of mycorrhizal networks on seedlings and large plants (i.e. plants tend to grow better if they are associated with a network). However, the reviewers also found some networks can have a neutral or even a negative effect on plants. The plant responses were highly variable depending on other variables including fungal species, nutrients availability, and plant identity. The positive effect of some fungal networks on seedlings growing nearby adult trees of its same species is somehow opposite to the predictions of the Janzen-Connell hypothesis. We need further studies to understand the overall importance of mycorrhizal networks in relation to other better understood mechanisms.

van der Heijden, M., & Horton, T. (2009). Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems Journal of Ecology, 97 (6), 1139-1150 DOI: 10.1111/j.1365-2745.2009.01570.x

How to plan an experiment that could last 99 years

For a number of reasons, including the fact that most grants only allow for research over a time span of 1-3 years, ecologists and evolutionary biologists usually plan experiments that last few years (with notable exceptions, such as the LTER). A usual approach to study long term phenomena is to take advantage of “natural” experiments. This allows us to understand about processes over long time periods, but usually with limited control on the initial conditions.

In a recent paper by Thomas Bruns and collaborators I learned about another way. They study spores viability of an important genus of ectomycorrhizal fungi, symbiont of Pinaceae: Rhizopogon. Pinaceae (the family of pines and other conifers) need ectomycorrhizal fungi to survive and usually spores and seeds are dispersed independently. It was not known how long their spores can last, which has very important implications, for example for colonization of areas not previously colonized by Pinaceae, or colonization after large scale disturbances, since if seeds cannot find mycorrhizae they have really few chances of survival. Now we know, based on this research that spore banks can be build and last probably decades.

What they did is really interesting, and was inspired on a previous study on seeds. They planted known number of spores of several species of Rhizopogon in terracotta pots, that were later planted into the ground (to mimic natural conditions). They planted 16 replicates, and they plan to open and analyze them later in the century based on the spore viability (for example, if in a few years most spores seem to be not viable that may reduce the expected length of the experiment to increase resolution). This paper found that after 4 years the inoculum potential of these spores seems to be increasing with time. I found the approach used in this experiment really fascinating and I look forward to see what happens in the next years!

Thomas D. Bruns, Kabir G. Peay, Primrose J. Boynton, Lisa C. Grubisha, Nicole A. Hynson, Nhu H. Nguyen, Nicholas P. Rosenstock (2009). Inoculum potential of
spores increases with time over the first 4 yr of a 99-yr spore burial experiment
New Phytologist, 181 (2), 463-470 DOI: 10.1111/j.1469-8137.2008.02652.x