Death by fungus?

The Chytrid Fungus Epidemic

Figure 1 - Known incidence of chytrid fungus infection in 2009 (Fisher et al.) Photo credit: http://www.amphibiaweb.org

In 1998, researchers discovered a previously undescribed Chytridiomycota fungus species, subsequently named Batrachochytrium dendrobatidis (henceforth referred to as Bd) was directly responsible for eradicating entire populations of amphibians. To date Bd has been confirmed responsible for amphibian deaths on five continents including: North America, South America, Africa, Australia and Europe (see figure 1). This discovery was paramount as it was the first fungi known to specifically attack a vertebrate species with such devastating effects. Since 1998, numerous studies have been done on Bd to establish its origin, physiology, requirements, its specific effect on amphibians, its ecological consequences and how it is being distributed into new environments. Many scientists have stated that this new pathogen represents the greatest global threat to biodiversity yet discovered.

Frogs killed by the deadly chytrid fungus. Photo credit: http://theworldofrogs.weebly.com/chytrid-fungus.html

Bd feeds solely on keratin and chemotaxis (attraction via chemical cues) may play a role in Bd’s ability to find and attack keratin sources. Studies have indicated Bd can survive in the environment without a keratin food source up to 7-12 weeks in sterile water. The optimal growing conditions that favor Bd’s presence has been studied and four factors seem to play a role: temperature, pH, salinity, and dissolved oxygen concentrations. Bd cannot survive outside the temperature range of 17-25 degrees Celsius. This information is meaningful to understanding why higher elevations are more prone to Bd outbreaks as many areas in higher elevations are warming from global climate change to temperatures that support growth of Bd. This also explains why many outbreaks occur in colder seasons, especially in tropical regions. Bd growth is limited by salinity and is only found in freshwater systems or slightly brackish water. The ideal pH for Bd growth is between 6-7 pH, however it has been shown to be able to survive outside these parameters. Often water pH can shift due to habitat alteration or climate influences and can encourage and sustain Bd epidemics. However, Bd growth is extremely limited by dissolved oxygen concentration. Increased nitrogen levels have a positive correlation on growth of Bd, this is significant as pollution has created higher nitrogen levels in aquatic systems near and far from human populations. Having a basic understanding of what conditions contribute to the growth of Bd can help explain why it has made such a sudden emergence and possible environmental factors that have allowed it to spread into so many new areas. 

The chytrid fungus. Photo credit: http://bama.ua.edu/~chytrid/

The first evidence of Bd infection on an amphibian was a Xenopus laevis (African clawed frog) museum specimen from the 1930’s collected in Africa. Molecular analysis of this specimen and analysis of other Bd specimens from around the globe point to a possible origin in Africa. Other studies have suggested a possible origin in Japan. Many questions arise of what vectors are responsible for its transmission and if specific environmental factors help encourage the spread of Bd into new areas. For both of these questions, one of the key components to consider is that pristine areas are being infected. Cascading anthropogenic affects are quite possibly part of the environmental and climatic shifts that could play a major role in Bd frequency, even in these pristine areas. Habitat, pollution and climate change are known environmental stressors and impact even remote areas. Habitat degradation can upset the balance of parasite and host dynamics and increase the virulence of pathogens. Microorganisms can acclimate and evolve at a faster rate than macro organisms to climate change, habitat modifications and chemical alterations in the environment. These aspects can impact the population size and diversity of pathogens like Bd. At the same time, host susceptibility can increase rates of infection as amphibian physiology can be altered and resistance to pathogens may be lowered in these same changing environmental conditions.

Studies indicate amphibians have decreased immune function in colder weather, when Bd is at its ideal growth parameters and when temperature and precipitation levels are unpredictable. Lower water levels and desiccation of water sources increases the density of amphibian populations creating additional stress on amphibian health and exposure to pathogens. Co-evolution is a dynamic that usually stabilizes parasite and host equilibrium. However if an amphibian species has not had previous exposure to Bd, it does not have the ability to adapt fast enough to prevent infection of the entire population. Isolated amphibian species can either be wiped out entirely or enough of the population can be reduced to create a genetic bottleneck that can ultimately lead to the demise of the population.

Frogs congregating after a heavy rain Credit: love in the ruins

Amphibians congregate in large numbers during breeding seasons, which can expose an entire population from one infected amphibian or an infected Bd water source. Although amphibians that reproduce in permanent water sources seem to be primarily affected, terrestrial amphibians can carry Bd to previously uninfected water systems. Amphibian larvae may also expedite transmission. Some amphibian larvae are known to take up to 4-5 years to complete metamorphosis and since they do not die from the infection, can keep Bd in local water sources for an extended time. Other adult amphibians are known to feed on them and have shown no discrimination to feeding on infected versus uninfected larvae which can spread Bd to the predatory amphibian species. High mortality rates are also associated with recent metamorphosed individuals that have been infected as larvae, possibly due to detrimental development or immunosuppression from Bd exposure (see figure 3).

Figure 2 - created by Heidi Rockney showing possible vectors compiled from references below

Several possible Bd vectors have been studied (figure 2). One of the most obvious and relevant is humans. There is a positive correlation to Bd ubiquity and human density, meaning that humans themselves probably carry Bd on their shoes, clothes, vehicles or other equipment between locations. The African clawed frog, an amphibian from Africa where Bd possibly originated are known vectors and have historically been distributed worldwide. In the 1940’s-1950’s; they were used as a way to determine pregnancy in humans. Bullfrogs are also carriers of Bd and are farmed in Africa where they could have picked it up and spread it across the globe via human introduction. Other vectors that have been researched are: migratory fish, waterfowl (carried on feet and feathers) and insects (possibly residing in their gut). In 2005, a study discovered that Bd can survive in moist sand and soil and  if infected dirt is tracked into a new environment, it could possibly infect new areas. Dead algae and insect exoskeletons have also been shown to be able to sustain Bd populations. Wind has been hypothesized as a possible vector, although Bd does not survive desiccation for more than 1-2 hours. It is highly possible that some if not all of these vectors are working in concert in the rapid global invasion of Bd. 

Figure 3 - created by Heidi Rockney illustrating how Bd kills amphibians

An important aspect of the Bd epidemic is how it causes amphibian death. Amphibians have permeable skin, which is a vital organ essential to their survival; as it is used as a means of water and oxygen absorption. Even small amounts of exposure to Bd can cause widespread infection. Bd attacks keratinized cells on amphibian skin, it thrives in the mouthparts of tadpoles, and the digits and ventral area of adults known as the “drinking patch." The drinking patch is where water absorption takes place and is critical in maintaining proper electrolyte balance. When Bd infects the drinking patch it disables the body’s ability to maintain proper electrolyte balance and infected amphibians show signs of severe dehydration. The exact cause of death in infected individuals is not certain, but currently it is thought that Bd affects cutaneous transport and might disable sodium transport channels on cell membranes. Improper osmotic homeostasis and disruption to vital membrane channels affect and control membrane potentials that regulate smooth cardiac muscles and other organ functions that if upset can lead to death (see figure 3 - created using data from scientific literature listed at bottom of page).

Interestingly, some amphibians do not show a strong immune response to Bd when infected. It is not yet understood if their bodies are not able to recognize the pathogen as a threat or whether they have decreased immune function from other factors, such as environmental stress. A few amphibians (bullfrogs, tiger salamanders, African clawed frogs) do show the ability to carry the pathogen but not succumb to infection as frequently as other species. It is still unknown whether they have an innate immune response that defends against infection or if they have had time to co-evolve an immune response. Future studies on amphibian immunology could help scientists understand the differences in amphibians that die from Bd and those that survive.

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References:

Carey, Cynthia. 2000. Infectious disease and worldwide declines of amphibian populations, with comments on emerging diseases in coral reef organisms and in humans. Environmental health perspective. 108 pp 143-150.

Fisher, M. P., Garner, T. W. J., and Walker, S. F. 2009. Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annual Review of Microbiology 63: 291–310.

Garmyn, An, Van Rooij, Pasmans, Frank, Hellebuyck, Van Den Boreck, Wim, Haesebrouck, Freddy, Martel, An. 2012. Waterfowl: Potential environmental reservoirs of the chytrid fungus Batrachochytrium dendrobatidis. PLoS One. 7(4).

Garner, Trenton W.J., Walker, Susan, Bosch, Jaime, Leech, Stacey, Rowcliffe, J. Marcus, Cunningham, Andrew A., Fisher, Matthew C. 2009. Life history tradeoffs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis.Oikos. 118 pp783-791.

Gerry, Parkes, Helen. 1998. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Population Biology. 95 pp 9031-9036.

Han, Barbara A., Searle, Chatherin L., Blaustein, Andrew R. 2001. Effects of an infectious fungus, Batrachochytrium dendrobatidis on amphibian predator-prey interactions. PLos One. 6(2)

Johnson, Megan L., Speare. Ricjard. 2005. Possible modes of dissemination of the amphibian chytrid Batrachochytrium dendrobatidis in the environment. Disease of Aquatic Organisms. 65 pp 181- 186.

Piotrowski, Jeffrey S., Annis, Seanna L., Longcore, Joyce. 2004. Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia. 96(1) pp 9-15.

Rachowicz, L., Vredenburg, V. (August 6, 2008) Overview of Amphibian Diseases [online]. Amphibiaweb.com [online] available: http://www.amphibiaweb.org/declines/diseases.html [2/21/2013]

Rosenblum, Erica Bree, Fisher, Matthew C., James, Timothy Y., Stajich, Jason E., Longcore, Joyce, E., Gentry, Lydia R., Poorten, Thomas J. 2010. A molecular perspective: biology of the emerging pathogen Batrachochytrium dendrobatidis. Disease of aquatic organisms. 92 pp 131-147.

Rohr, Jason R., Halstead, Neal T., Raffel, Thomas R. 2011. Modeling the future distribution of the amphibian chytrid fungus: the influence of climate and human-associated factors. Journal of applied ecology. 48 pp 174-176.

Voyles, Janie, Berger, Lee, Young, Sam, Speare, Rick, Webb, Rebecca, Warner, Jeffrey, Rudd, Donna, Campbell, Ruth, Skerratt, Lee F. 2007. Electrolyte depletion and osmotic imbalance in amphibians with chytridiomycosis. Diseases of Aquatic Organisms. 77 pp 113-118.