Investigating the host-parasite dynamics of a novel amphibian dermocystid disease in an isolated population of palmate newts in the UK
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Date
01/12/2017Author
Clarke, Charlotte Louise
Metadata
Abstract
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.