Investigating the host-parasite dynamics of a novel amphibian dermocystid disease in an isolated population of palmate newts in the UK
Clarke, Charlotte Louise
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Emerging infectious diseases (EIDs) have been identified as a key factor in significant amphibian mortalities and global declines. Disease has been largely attributed to just two pathogens, Batrachochytrium dendrobatidis (Chytrid) and Ranavirus, however, an increasing number of amphibian disease cases across Europe are being attributed to a group of unusual fungal-like pathogens of the order Dermocystida. Despite representing an old lineage of amphibian pathogens first described in 1903, very little is known about amphibian- Dermocystids. In 2006, diseased palmate newts on the Isle of Rum, Scotland were reported. Clinical signs appeared consistent with heavy infestations of Dermocystid disease, however oedematous pathologies not previously described in the literature were also observed, suggesting a severe case of disease. This thesis develops the first comprehensive pathogen profile of a novel amphibian-infecting Dermocystid causing severe disease in an isolated population of palmate newts (Lissotriton helveticus) on the Isle of Rum, Scotland. Molecular phylogenetics and histopathology techniques were used to characterise the pathogen, confirming its affiliation to the Dermocystids and identifying it as the second formally described species in the genus Amphibiothecum (meredithae). By incorporating histopathology, field observations and study trials a broader understanding of disease dynamics was achieved. Pathogen cyst developmental stages were assigned to distinct gross pathologies, determining a putative disease cycle. In addition, a large disparity in disease outcome was evident, with cases suggesting involvement of innate immune systems with apparent host recovery, alongside cases with severe morbidity and mortality. Following the development of a pathogen profile, the spatio-temporal dynamics of disease were explored across three consecutive years, from 2014 to 2016. The temporal patterns observed within a single season were first examined across a small sub-set of sites, highlighting a degree of stability in disease prevalence and environmental variables. This within-season survey also provided a temporal dataset of disease presentation, allowing for disease progression to be assessed at the population level, investigating the impact of time on disease presentation and morbidity. For example, an overall linear trend in disease progression was observed where the burden of discrete cysts, thought to represent an initial stage of infection was highest at the beginning of the season, appearing to be ‘replaced’ by larger lesions representing later stage pathologies. Finally, ulcerations that facilitate the release of mature pathogen spores (or sporangia) occurred in the highest abundance towards the end of the season. However the prevalence of the most severe oedematous stages did not always fit with this linear progression of disease and may be driven by other factors. Understanding the within-season dynamics, and confirming a temporal stability in disease prevalence, allowed for broader spatial analysis to be performed without the need to account for samples taken at different points in time. Data collected from a broad spatial survey conducted in 2014 was explored to determine the spatial distribution of infection on Rum, and to investigate the relationships between the incidence, prevalence and severity of disease to environmental conditions and host population structure (e.g. sex ratios). Disease was widespread but heterogeneously distributed across Rum, with site-to-site variation in the incidence and prevalence linked to water pH where low pH environments were associated with low disease prevalence. An apparent sex-linked bias in disease was determined where males were more susceptible, but this does not appear to impact the host population structure of infected sites. The observed relationships between disease prevalence and environmental conditions were further utilised to test the use of disease prediction maps as a means to estimate disease across unsampled locations on the Island. Spatial surveys were subsequently conducted in 2015 and 2016, providing annual data on the distribution and prevalence of disease. Interannual variation at the site level was used to explore key factors influencing the stability of disease, identifying an association between changes in host population structure and increasing disease levels. Spatio-temporal fluctuations at the island level alluded to the overall state of disease on the island and changes to disease risk overtime. Whilst spatial clusters of changing disease prevalence were identified, which could indicate unusual patterns of epidemic spread, these conclusions would be speculative and as no consistent, significant increase in disease was determined or expansion in range, disease likely represents an endemic infection dictated heavily by etiological factors. In order to facilitate future studies and nation-wide surveys such as those conducted for Chytridiomycosis and Ranavirosis, this thesis concludes by trialling non-invasive diagnostic techniques. Environmental DNA and dermal swabbing provides the basis for the development of alternative sampling protocols to improve large-scale survey potential, and lead to a deeper understanding of these pathogens. This study represents the first formally described case of Dermocystid in the UK as well as providing the first detailed spatio-temporal study of an amphibian- Dermocystid. Identifying significant predictors of disease alongside disease prediction maps and potential methods for quick disease diagnosis, provides the tools for future, large-scale analyses to understand the distribution of disease across mainland UK, host range and the risk to native amphibian species.