Chytridiomycosis and symbiosis: context-dependency in amphibian disease and conservation

Daskin, Joshua H. (2011) Chytridiomycosis and symbiosis: context-dependency in amphibian disease and conservation. Masters (Research) thesis, James Cook University.

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Symbioses, long-term direct relationships between individuals of multiple species, are well known from many taxa and biomes. Although they are often thought of as static, symbioses are frequently dependent on environmental or ecological context. While there is a substantial amount of information on context-dependence in many symbioses, there little is known of how symbioses important to wildlife disease and conservation vary.

One disease of conservation importance that may be strongly affected by contextdependent symbioses is chytridiomycosis. This amphibian disease is caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd) and has caused population declines and extinctions on several continents. Bd's growth rate depends on environmental context, as evidenced by its distinct in vitro thermal optimum (17-25°C). The majority of Bd-driven declines have occurred in relatively cool climates (at high-elevation and during winter in tropical regions), demonstrating that environmental context affects disease outcome. However, many cool weather declines have occurred at temperatures well below Bd's thermal optimum, where chytridiomycosis might be expected to be less severe. Two possible explanations for this pattern are that Bd in natural environments may adapt to low temperatures by increasing fecundity, or that production of anti-Bd skin peptides, a component of many amphibians' innate immunity, may be down-regulated in cool environments. Still a third possible explanation for the high incidence of Bd-driven declines at temperatures below the fungus's in vitro thermal optimum is that symbiotic bacteria that also inhabit amphibian skin and that can reduce the severity of chytridiomycosis may have severely reduced activity or density at cooler temperatures. However, no information exists on how the composition or antifungal activity of amphibians' anti-Bd bacterial assemblages respond to environmental contexts.

Eventually, antifungal bacterial symbiont populations may be augmented on amphibians' skin for management of chytridiomycosis. Currently, there is no broadly effective treatment or preventative available for wild amphibians at risk of chytridiomycosis, but supplementing amphibians' natural protective microflora, to enhance the protective effect they lend (termed "bioaugmentation,") is being explored. If these bacteria's anti-Bd activity varies with environmental and ecological context, bioaugmentation will require careful selection of robustly antifungal bacteria.

I identified 16 bacterial species previously not known to act as anti-Bd symbionts on the rainforest tree frogs Litoria serrata and L. nannotis. On average, in vitro anti-Bd activity of symbionts (both newly identified and previously known) from all bacterial classes was reduced at cooler temperatures characteristic of areas where declines driven by chytridiomycosis have been most severe. Such context-dependency in anti-Bd activity of amphibian symbionts may partially explain the association of past Bd-driven declines with cool temperatures, especially below the fungus's thermal optimum. It could also affect selection of bacteria for bioaugmentation and disease management.

Bd is a member of the little-studied and phylogenetically-basal Chytridiomycota, which are only distantly related to the better-studied higher fungi. Little is known of chytrids' interactions with bacteria. However, many higher fungi induce or inhibit the antifungal activity of antagonistic bacteria, altering the outcome of microbial symbioses and affecting agricultural biocontrol schemes. If Bd has mechanisms to defend against antifungal bacteria, they might adversely affect the success of bioaugmentation in natural amphibian populations. I found that Bd metabolites can affect the anti-Bd activity of antifungal bacterial symbionts isolated from Litoria serrata, L. rheocola, and L. nannotis. The activity of most symbionts was not affected, suggesting that although bacteria that are candidates for bioaugmentation will need to be screened for responses to Bd metabolites, most will not be affected. Activity of Bd metabolites should therefore not pose a severe problem for the management of chytridiomycosis by bioaugmentation, although Bd may still harbor non-chemical defense mechanisms not yet detected or evaluated.

While many amphibian species have declined due to Bd, some populations persist in an apparent commensal relationship with Bd. For example, in the Australian Wet Tropics, Litoria nannotis declined sharply at high elevation rain forest sites due to Bd in the early 1990s, and has not recovered. However L. nannotis, and one population of L. lorica, the latter previously believed extinct due to Bd, were recently found in high elevation dry forests, apparently healthy, but infected with Bd at high prevalence. One explanation previously suggested for persistence with Bd in dry forests is that exposure to sun-warmed rocks frogs perch on in these habitats may be keeping Bd infections below the lethal threshold attained at cooler rain forest sites. I tested whether short-term exposure to elevated temperatures can hamper in vitro Bd growth. One hour daily at 33°C, but not at 28°C (representing exposure to heavily and more moderately warmed rocks in dry forests, respectively) reduced in vitro Bd growth below that in a constant 15°C regime (representing cool rain forest habitats). The reduction in Bd growth over the fungus's first generation after inoculation was small but may translate into maintenance of Bd infection intensities below a lethal threshold in natural settings over multiple generations of Bd growth.

My work provides early evidence of the role context-dependency may play in determining the outcome of the amphibian-Bd-bacteria symbiosis. If observed reductions in the anti-Bd activity of amphibians' bacterial symbionts at cool temperatures in vitro translate to wild frogs' symbionts, then corresponding losses in amphibian protection from Bd could account for the relatively frequent occurrence of amphibian declines at cool temperatures below Bd’s thermal optimum. In what was, to my knowledge, the first study of a chytrid fungus's effects on antagonistic bacteria, I found that metabolites of Bd were not active against the majority of Litoria spp. bacterial symbionts tested, suggesting that most antagonistic bacteria are not affected by any defenses involving metabolites. In future work based on the present study, chemical methods could be used to measure in situ concentrations of antifungal compounds on amphibian skin, and to identify the composition of Bd's metabolites. Future studies should also clarify the roles of warm microhabitats, amphibian immunity, and animal behavior in driving the apparent commensal nature of the amphibian-Bd symbiosis in tropical Australia’s upland dry forests and elsewhere.

Item ID: 29935
Item Type: Thesis (Masters (Research))
Keywords: Batrachochytrium dendrobatidis; conservation ecology; amphibian disease; frogs; chytrid fungus; bacteria symbiosis; chytridiomycosis
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2. Daskin, Joshua H., and Alford, Ross A. (2012) Context-dependent symbioses and their potential roles in wildlife diseases. Proceedings of the Royal Society of London Series B, Biological Sciences, 279 (1733). pp. 1457-1465.

Chapter 4. Daskin, Joshua H., Alford, Ross A., and Puschendorf, Robert (2011) Short-term exposure to warm microhabitats could explain amphibian persistence with Batrachochytrium dendrobatidis. PLoS ONE, 6 (10). pp. 1-4.

Date Deposited: 25 Oct 2013 05:35
FoR Codes: 06 BIOLOGICAL SCIENCES > 0605 Microbiology > 060502 Infectious Agents @ 34%
05 ENVIRONMENTAL SCIENCES > 0502 Environmental Science and Management > 050202 Conservation and Biodiversity @ 33%
06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060303 Biological Adaptation @ 33%
SEO Codes: 96 ENVIRONMENT > 9604 Control of Pests, Diseases and Exotic Species > 960404 Control of Animal Pests, Diseases and Exotic Species in Forest and Woodlands Environments @ 50%
97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 50%
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