The Amphibian Chytrid fungus

Chytridiomycosis is a skin disease currently devastating amphibians worldwide. The fungus that causes the disease, Batrachochytrium dendrobatidis (BD), operates by infecting keratinized cells of the amphibian epidermis (skin)(Ouellet et al. 2005). The disease was first described in 1998 in amphibian populations in Australia and South America(Berger et al. 1998). Since then, the disease has been reported on every continent except Antarctica and is estimated to have played a part in the decline of at least 500 species and the presumed extinction of 90 species(Scheele et al. 2019). Chytridiomycosis is arguable the greatest threat to biodiversity caused by a pathogen, and as such has warranted in-depth research and intense conservation efforts. Here, I will briefly describe the history, biology, and ecology of chytrid, and current conservation efforts to combat its spread.

Although it was first described in 1999, samples taken from museum specimens indicate that the earliest records of chytrid date back to the 1930’s (Schloegel et al. 2012; Rodriguez et al. 2014). While the chytrid fungus went undetected for decades at minimum, researchers were able to record a sharp decline of amphibian populations worldwide beginning in the 1960s. Interestingly, some researchers even hypothesized that this decline was being caused by a pathogen, although at the time they were unable to identify the causative agent(McCallum 2005). When Berger et al(1998) described chytridiomycosis and Longecore et al(1999) described the causative agent (B. dendrobatidis), they provided the missing pieces for a hypothesis put forward by others. However, the history regarding the spread of chytrid remains unclear. The most popular idea is that chytrid originates from Africa, and was a pathogen of the African Clawed Frog, Xenopus laevis. X. laevis is a popular study organism, and was used in earlier versions of pregnancy tests, and so was traded globally in the 1930s and onward(Longcore et al. 2007). Following this logic, Weldon et al. suggested that X. laevis acted as a vector of chytrid, and that when humans began trading X. laevis internationally, they unknowingly aided in the global spread of chytrid(Weldon et al. 2004). While this is the most popular idea, some have suggested alternative origins for chytrid, and recent work in population genetics have provided evidence for different origins of chytrid. First, Rodriquez et al. provided evidence that strains of BD found in the Brazilian Atlantic Forest were in fact endemic, meaning that it was not introduced recently by humans, with no evidence of regional spread in over 100 years(Rodriguez et al. 2014). Additionally, research by Schloegel et al. not only provided further evidence for a variety of endemic strains of chytrid globally, but also suggested that a singular strain known as BD-GPL is actually epidemic in nature and largely responsible for the declines currently being experienced by amphibians globally(Schloegel et al. 2012). However, their findings also suggested that BD has infected amphibians globally since long before the beginning of global amphibian declines was recorded. Furthermore, Schloegel et al provide the first evidence of sexual reproduction, in the form of a hybrid between two different BD strains. This last piece of evidence is especially worrying, as the ability to sexually reproduce between and epidemic and endemic strain may create further issues for at risk species(Schloegel et al. 2012). Together, this varying research provides a complicated and often contradictory history of the chytrid fungus.

As for its biology, BD is a member of the fungal division chytridiomycota(Longcore et al. 1999). BD and the recently discovered relative B. salamandrivorans are the only two members of Chytridiomycota known to parasitize vertebrates(Longcore et al. 1999; Van Rooij et al. 2015; Stegen et al. 2017). BD has two major life stages: first it lives as a mobile zoospore. BD zoospores colonize the keratinized skin of amphibians, mainly anurans (frogs). Once there, the fungus begins to develop in the second life stage: a zoosporangia. On the skin, the zoospore develops rhizoids (similar to roots) which then invade skin cells and take in nutrients from the cells’ cytoplasm. Finally, the zoospore develops into a sporangium (or zoosporangium), within which new zoospores are grown and later released into the environment via a discharge tube. This description is taken from a more in-depth description of BD and BSal from Van Rooij et al. (2015).

In terms of ecology, I will focus mostly on the habitat factors BD requires in order to persist. First and foremost, BD is most persistent in semi-permanent to permanent wetlands(Scheele et al. 2019). BD requires an aquatic environment in order for its free living zoospore life stage to persist in dry environments(Scheele et al. 2019). BD also tends to be positively associated with areas with higher vegetation and greater temperature range, although vegetation is thought to just be a proxy for moisture levels and temperature variation(Liu et al. 2013). The effects of temperature and temperature variation on BD are particularly interesting because they almost seem contradictory. BD can reproduce over a range of temperatures from 4-25[^o]C, but above the 25[^o]C threshold infection loads in amphibians decrease(Brannelly et al. 2021). In fact, exposing captive amphibians to higher temperatures has become a common method for treating infected individuals(Brannelly et al. 2021). So, one might think that the increasing predicted temperatures associated with global climate change could actually be good for amphibians, since it will allow them to better resist BD. However, BD-associated amphibian declines in the neotropics were actually positively correlated with temperature (high temperature year = higher chance of BD declines)(Venesky et al. 2014b). Why is this? Increased maximum temperatures are positively associated with higher temperature variability(Raffel et al. 2013). In turn, while amphibian immune systems may work better at higher temperatures, increased temperature variability (the range of temperatures within a given period) in conjunction with BD can actually negatively impact amphibian populations(Raffel et al. 2006, 2013; Hamilton et al. 2012). The exact mechanisms of this interaction aren’t entirely clear, but it is possible and likely the higher temperature variability both improves BD function and transmission while decreasing amphibian immune function. Prior research has shown that drops in temperature trigger a release of zoospores by BD(Venesky et al. 2014b), so increased temperature variation would lead to more frequent temperature drops and thus more frequent release of zoospores. Additionally, increases in temperature variation are associated with decreases in amphibian immunocompetency (measured by stomach lysozyme activity)(Raffel et al. 2006).

In addition to abiotic factors such as moisture and temperature, the presence of BD within a system can also be impacted by biotic factors. The most important biological factors impacting BD are the presence of reservoir species, and the amphibian biodiversity of a given system. A reservoir host is a species that can harbor a pathogen by transmitting it among themselves and others, and is relatively unaffected by the disease (i.e. low mortality rate), allowing the disease to persist even when other, more susceptible species are absent or at low densities (Brannelly et al. 2018). Because BD is usually a density dependent disease (i.e. it’s transmission rate depends on the density of hosts) one would expect that as density decreases due to BD-related mortality, transmission of the disease should go down. If this were the case, then BD would not be able to cause the extinction of species and would not be nearly as problematic as it is. The issue arises with the fact the diseases do not live in a vacuum with a singular host species. BD has a broad host range, meaning that it can infect a wide variety of species(Van Rooij et al. 2015). Given that species can vary in their ability to tolerate BD, some species in a system will decline rapidly while others will remain stable (reservoir hosts). These reservoir hosts will then continue to shed BD zoospores, allowing BD to persist in the environment and continue infecting and killing more susceptible hosts’ until their populations are extirpated. However, a higher variety of species within a system can also actually decrease the prevalence of BD, if the proper conditions are met. This is known as a dilution effect(Venesky et al. 2014a). The essence of the dilution effect is that if there is an increase in biodiversity this will decrease transmission of a disease/parasite by a variety of mechanisms, most notably by decreasing the relative abundance of reservoir hosts and/or decreasing the chances of BD zoospores interacting with a competent reservoirs(Ostfeld and Keesing 2012; Venesky et al. 2014a). There are a few key assumptions that a system must meet for a dilution effect to occur. First, the disease/parasite must be a generalist (meaning that it has multiple host species). Second, there must be variation in host species in reservoir competency (meaning how well they act as a reservoir species). Finally, there must be a positive correlation between reservoir competence and numerical dominance in community such that most competent species tend to be present in both species-poor and species-rich communities. What this final assumption means is that the best reservoirs are also the best survivors. These species should be the most common species across all communities within the system and be the dominant species in low-diversity communities. These assumptions are adapted from Begon et al. (2008).

Now that we have a fuller picture of how and why chytridiomycosis is affecting global amphibian populations, the question remains: what is being done about it? The best way to combat declines due to BD is to stop its spread in to naïve populations by properly disinfecting gear between wetlands (for researchers as well as outdoorsmen), understanding transmission pathways in the amphibian pet trade, and implementing quarantine and screening protocols for the amphibian trade (Longcore et al. 2007; Skerratt et al. 2007; Olson et al. 2013). Additionally, with knowledge of BD, we can improve strategies for re-introduction of at risk species; namely, re-introduction efforts should target high biodiversity areas and/or areas where known reservoir species are not present(Brannelly et al. 2018). Additionally, there has been some research in to the antifungal peptides often found on amphibian skin, as well as acquired immunity in response to infection (the basis on which vaccines are developed)(Venesky et al. 2014b). However, research on these topics is limited, and implementing a worldwide vaccination regime for hundreds, if not thousands, of amphibian species would be incredibly difficult.

Species worldwide are currently at risk of facing major extinction risks. As we have outlined here, in addition to facing threats shared with other species such as climate change, habitat loss, habitat fragmentation, and overexploitation, many amphibians face the unique threat of extinction via disease. While the task ahead is daunting, we should not be dismayed; with continued research and active conservation efforts we can reverse many of the effects we ourselves have caused.

Works cited

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