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Impact and mitigation of the emerging infectious disease chytridiomycosis on the endangered green and golden bell frog

By Michelle Stockwell

Abstract

Research Doctorate - Doctor of Philosophy (PhD)Over the past 50 years dramatic declines in the world’s amphibian fauna have resulted in the possible extinction of up to 159 species and the emerging infectious disease chytridiomycosis has been implicated as a causal agent. Chytridiomycosis is caused by the newly described amphibian chytrid fungus Batrachochytrium dendrobatidis which infects keratinised cells in the outer epidermal layers of post-metamorphic amphibians that impair the osmoregulatory function of the skin, leading to circulatory collapse and death in susceptible species. The chytrid fungus also infects the keratinised mouthparts of tadpoles but this is rarely reported to be fatal. The existence of reservoir hosts, in the form of tadpoles and less susceptible species allows the pathogen load to remain high in an area, driving susceptible species to extinction. As a result, population declines and extinctions caused by chytridiomycosis are often rapid and occur alongside a suite of non-declining species. The green and golden bell frog Litoria aurea is an endangered Australian anuran that was once widespread throughout eastern NSW and Victoria but underwent a dramatic range contraction in the 1980s. This species currently persists in less than 10% of its former range in a series of highly isolated and disturbed sites along the coastline. Historically, the decline of the green and golden bell frog has been attributed to the effects of habitat loss and predation by the introduced mosquito fish Gambusia holbrooki. However, at the landscape level, the distribution of these threats is inconsistent with the bell frog’s pattern of decline. Green and golden bell frogs are highly tolerant of disturbance and appear to have disappeared from apparently suitable areas only to persist in highly modified sites, often in the presence of mosquito fish and other non-declining frog species. These observations suggest another agent may be operating. The decline pattern of the green and golden bell frog has a number of consistencies with global disease-induced declines but the potential role of chytridiomycosis in the bell frog has not been established. Several small mortality events of infected bell frogs have been observed, indicating susceptibility, but nothing is known about infection and disease dynamics. There has also been some speculation that the persistence of bell frogs in coastal and often contaminated sites may be due to the antifungal properties of water solutes in those environments but this has not been investigated in detail. The overall objective of this thesis was to establish the susceptibility of bell frogs to chytridiomycosis and to model this impact on population dynamics. It also investigated the role of environmental inhibitors of chytrid in allowing bell frog populations to persist in their current range and the potential for these inhibitors to be used as a mitigation tool. This was done by addressing four primary aims. The first primary aim of this thesis was to determine whether bell frogs were susceptible to chytridiomycosis upon exposure to the chytrid fungus and this was investigated in both captive and free-living animals. An infection experiment exposing green and golden bell frogs to a chytrid isolate in captivity monitored infection loads and signs of disease over time (Chapter 2). All exposed bell frogs were found to become infected and infection loads increased significantly over time. Within 100 days all infected bell frogs showed terminal signs of chytridiomycosis. In free-living bell frogs, mark-recapture surveys and radiotracking were used to determine infection status over a 12 month period to estimate the impact of infection on survival probability (Chapter 3). Infection was found to impact survival over the colder non-breeding season with significantly lower survival probabilities found in infected bell frogs (0.1), compared to uninfected (0.56). The second primary aim of this thesis was to determine the impact of infection on population dynamics. This was investigated using the survival and infection transition probabilities from multistate models and comparing population size scenarios when chytrid was present or absent (Chapter 3). The results reveal that an infected population would decline at twice the rate of an uninfected population. The ability of the chytrid fungus to cause population decline and extinction in bell frogs was further supported by the unintentional exposure of a reintroduced population at the Hunter Wetland Centre and the resulting chytridiomycosis epidemic observed (Chapter 4). The third primary aim of this study was to determine whether inhibitors of chytrid survival, growth or transmission occur in current bell frog habitat. Infection levels in the dwarf green tree frog Litoria fallax were compared between sites formerly and currently occupied by bell frogs in the Lower Hunter Region of NSW, where bell frogs have undergone a directional range contraction that echoes the species decline (Chapter 5). Infection loads were found to be higher in sites where bell frogs have disappeared and were correlated with the abundance of fish (positive relationship), the degree to which the water body dried, water temperature and salinity (negative relationships). A series of controlled and replicated experiments were then conducted to test for causation and an inhibitory effect of water temperature and salinity on infection load was confirmed. The fourth primary aim of this thesis was to determine whether inhibitors of the chytrid fungus can be used to mitigate the impact of chytridiomycosis on bell frog populations. The antifungal effect of dissolved sodium chloride in aquatic habitat was investigated in controlled experiments conducted in the laboratory and then in the field. When grown in culture media with 4 and 5 ppt sodium chloride, chytrid growth, zoospore density and zoospore motility were significantly inhibited compared to 0 ppt (Chapter 6). Given that chytrid fungi are generally adapted to freshwater habitats and are have low sensitivities to desiccation, this effect is likely the result of energy investment into osmoregulation rather than growth and motility. To investigate the impact of this on infection outcomes, an infection experiment was conducted and found that hosts housed in water bodies with 3 or 4 ppt sodium chloride had significantly lower infection loads relative to those housed in 0 ppt and had significantly higher survival rates (Chapter 6). These results confirmed the antifungal effect of dissolved sodium chloride at environmentally available concentrations. A field based experimental reintroduction was then used to trial the practicality and effectiveness of elevating dissolved sodium chloride concentrations in ponds as a mitigation tool for the chytrid fungus (Chapter 7). Naturally derived sodium chloride was added to eight water bodies to equal a maximum of either 2 or 4 ppt. An additional four water bodies were left at close to 0 ppt to act as controls. Captively bred green and golden bell frog tadpoles were released into each independent water body and monitored for body size, infection levels and survival. A negative effect of exposure to 4 ppt was found on the body length of tadpoles but a positive effect was found for the outcome of infection, with significantly lower prevalences and higher survival rates post-metamorphosis. Monitoring of non-target amphibians and macro-invertebrates found a negative effect of 4 ppt on the relative abundance of several species. These results support the role of sodium chloride manipulations in natural amphibian habitat as a potential mitigation strategy but cautions that these effects must be weighed against any negative effects on co-occurring species. In the process of addressing the four primary aims of this thesis, a number of additional secondary aims were also investigated that, although not the focus of this thesis, still contributed to our understanding of chytridiomycosis and the green and golden bell frog. The first of these secondary aims was to determine the dynamics that drive infection outcomes for both the individual host and the host population. In determining the susceptibility of bell frogs to chytridiomycosis following exposure to the chytrid fungus, it was found that the terminal stages of chytridiomycosis were determined by infection loads crossing a threshold, representative of the point at which epidermal function is irreversibly impaired (Chapter 2). In host populations, it was the survival rate of infected individuals as well as the transition probabilities between infected and uninfected states, both of which were driven by seasonal variability in temperature, that determined the impact on population size (Chapter 3). The second secondary aim was to determine whether non-declining amphibian species that co-occur with bell frogs are less susceptible to chytridiomycosis and was investigated in a comparative infection experiment (Chapter 2). The comparison of infection outcomes when exposing both green and golden bell frogs and the non-declining co-occurring striped marsh frog Limnodynastes peronii to the chytrid fungus revealed significantly different outcomes. Infection loads in striped marsh frogs did not increase over time and did not result in the mortalities seen in bell frogs. Rather, infection loads remained the same or declined over time and survival rates did not differ from uninfected controls. This suggested that this species has a mechanism of maintaining infection loads below the disease causing threshold. These susceptibilities also correlate with the decline patterns and threat status of these two species. Further evidence that bell frogs are more susceptible to chytridiomycosis than co-occurring species was obtained through observations of a reintroduced bell frog population extinction alongside populations of three other species that did not disappear (Chapter 4). Finally, the third secondary aim was to determine the most effective vital rate to target to manage the negative effect of chytridiomycosis on population persistence. This was done by comparing scenarios of population persistence models when the probability of acquiring infection, the probability of losing infection, the recruitment rate or the survival probabilities of infected and uninfected hosts were improved by a relative measure (Chapter 3). Comparisons revealed that when the degree of ‘improvement’ is kept constants across rates, an increase in the recruitment rate or survival probability of uninfected individuals resulted in the greatest benefit for population persistence. These results suggest that even if methods to control the chytrid fungus were available, counteracting its effects may be the most effective management strategy

Topics: Batrachochytrium dendrobatidis, amphibian chytrid fungus, chytridiomycosis, Litoria aurea, bell frog, disease mitigation
Year: 2011
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