Abstract
Wildlife diseases have become a serious and growing threat to global biodiversity. Among the most devastating is chytridiomycosis, a fungal disease caused by Batrachochytrium dendrobatidis (Bd), which has contributed to widespread population declines and extinctions of amphibian species globally. Bd infects the keratinised parts of the body in amphibians, causing disruptions in osmoregulation, respiration, ion exchange balance, and in susceptible species leads to death. To date, no effective solution exists to reduce its impact in wild populations, except for the use of azole antifungals to locally eradicate Bd in arid climates. The environmental tolerance mismatch hypothesis (ETMH) points to a promising approach to reduce the impact of Bd on amphibian populations. This hypothesis posits that environmental conditions tolerated by a host (i.e., amphibian) but not by a pathogen (i.e., Bd) will reduce disease impacts. While this hypothesis has been supported in amphibians and Bd under high temperature and salinity, there is anecdotal evidence that metal pollution may also protect Bd-susceptible amphibians from Bd infection. However, the ETMH remains unexplored for these organisms and metals.The overall aim of this thesis is to test whether environmentally-relevant concentrations of copper (Cu), zinc (Zn), and their combination (Cu+Zn;hereafter referred to as metals) can suppress Bd without harming frogs, thereby enabling Bd-susceptible frogs to persist in the presence of Bd. To address this overarching aim, the thesis is structured into six chapters. Chapter 1 is a literature review of wildlife diseases across various taxa, introducing chytridiomycosis and its impact on amphibians, and providing examples where the ETMH has been tested for host-pathogen interactions. This chapter further presents evidence for the potential benefits of metal pollution in a metal-contaminated river, where small populations of the green and golden bell frogs (Ranoidea aurea) persisted despite the disappearance of nearby populations at non-contaminated sites because of Bd. Chapter 2 experimentally determines the acute and chronic metal sensitivity of Bd and compares these sensitivities with those of amphibians reported in the literature. Results showed that Bd zoospores were 10 and 8 times more sensitive to Cu and Zn, respectively, in acute exposures, and 2 and 5 times more sensitive to Cu and Zn in chronic exposures, compared with the most metal-sensitive amphibian species reported in the literature, thereby supporting the ETMH.
Chapter 3 examines whether Bd shows different tolerances to metals across three consecutive generations. It also examines the effects of transgenerational plasticity (TGP) when the parental generation is exposed to metals, but the offspring are returned to a metal-free environment. The multigenerational effects of metals on Bd revealed decreased tolerance across three generations, with each generation showing successively lower tolerance than the first generation. TGP effects revealed that the impacts of metal exposure persisted in offspring, even in the absence of metals in the environment. Interestingly, TGP effects explained 45% of the decline in Bd’s population growth rate across generations under continuous metal exposure, highlighting that 55% of the Bd’s response is due to mechanisms other than TGP.
In Chapter 4, a filtration-based method was developed to concentrate Bd zoospores from water samples. This approach was necessary due to the limited understanding of Bd zoospore viability in aquatic environments, particularly the effects of environmental stressors on zoospores after their release into water. The method enabled assessment of both zoospore abundance and viability in water samples. This method proved effective for assessing both the abundance and viability of Bd zoospores, yielding consistent results between expected and counted zoospore numbers, with nearly 100% viability maintained after filtration. This method was then applied in Chapter 5, in which frogs were exposed to Bd in the presence and absence of an environmentally-relevant concentration of Cu. The aim was to experimentally examine whether Cu exposure provides an advantage to frogs (R. aurea), enabling them to persist in the presence of Bd. Results showed that exposure to Cu and Bd reduced infection intensity and mortality, increased feeding rate and weight gain, relative to frogs exposed to Bd in the absence of Cu. Bd zoospores in the water had higher mortality when exposed to Cu compared with zoospores from non-exposed frogs, highlighting the impacts of Cu on Bd zoospores in the water environment. Chapter 6 summarises the work and the contribution of the body of research along with implications and future research opportunities.
This thesis provides strong evidence for the hypothesis that Cu and/or Zn pollution reduces Bd’s performance more than it affects its amphibian hosts, explaining the persistence of Bd-susceptible frogs at metal-polluted sites. Existing metal-polluted sites could also be used as disease refuges, enabling Bd-susceptible frogs to persist in the presence of Bd. This work is the first to contribute to the current body of knowledge regarding the potential of well-supported environmental stressors such as high temperature and salinity and adds sites where existing metal-polluted environments may protect frogs facing Bd. This research has significant implications for conservation strategies, potentially help to relocate or reintroduce Bd-invaded species (such as the green and golden bell frog, R. aurea) to metal-polluted sites as refuges from disease. Future research testing this hypothesis in existing metal-polluted wetlands and/or large-scale mesocosms will enhance our understanding of the complex environmental factors influencing the interactions among Bd, amphibians, and metals. Conducting experiments in these more ecologically-realistic habitats, where multiple biotic and abiotic factors coexist, will provide further support for the hypothesis that metals modulate disease dynamics in amphibian populations.
| Date of Award | 2025 |
|---|---|
| Original language | English |
| Supervisor | Ben KEFFORD (Supervisor), Simon CLULOW (Supervisor), Richard DUNCAN (Supervisor) & MD Tariq EZAZ (Supervisor) |