Population dynamics, disease and other drivers in a wild snake population

Anthropogenic activities are currently contributing to global wildlife populations declines in what some scientists have named the sixth mass extinction. Reptiles are not exempt from these declines, with species affected by the combined effects of habitat loss, climate change, over-exploitation, disease, and multiple other factors. In recent decades, emerging infectious diseases have become a more urgent concern on the conservation agenda, especially in those species or populations that are already threatened by human-mediated threats or changes. One example of these is ophidiomycosis, which was first detected in wild snake populations in Great Britain in 2016. The barred grass snake (Natrix helvetica) is a widespread species throughout Great Britain that has declined regionally in recent times. This thesis aims to answer: (1) What is the prevalence of skin lesions within the study population and its relationship to ophidiomycosis? (2) How do skin lesions caused by ophidiomycosis vary seasonally in barred grass snakes? (3) How do skin lesions affect the behaviour and survival of snakes? (4) What is the population size and annual survival and detectability of snakes within the population?

A study site comprising an artificial wetland and associated habitats in eastern England measuring approximately 0.5 km2 in size, was monitored for N. helvetica through 264 surveys conducted by five surveyors from 2015 to 2021. A total of 1143 individual snakes were captured and identified by their ventral scale pattern, using Wild-ID. These data were then used to build a capture history to compare annual survival and detectability of snakes with and without skin lesions.

Skin lesions were first identified in the population in 2016, which tested real-time PCR positive for Ophidiomyces ophidiicola DNA. Starting in 2019, targeted monitoring of skin lesions was undertaken to investigate their characteristics and aetiology, with snakes showing clinical signs being swabbed for later rtPCR analysis. Skin lesions were observed in 25.5% of individual snakes captured from 2019 to 2021 inclusive. The lesions occurred mainly on the ventral surface of snakes as discoloured areas of mild crusting on scales, or scale margin erosion. When present, a tailored severity classification system was used to score the severity of skin lesions. A total of 78.7% of the swabs taken from snakes with skin lesions, tested rtPCR positive for O. ophidiicola DNA. These results were reinforced through the use of histopathology of both tissue and slough samples, which supported use of skin lesions as a proxy for ophidiomycosis in later analyses. Skin lesions occurred more frequently in adults than sub-adults or neonates, and a higher occurrence of trauma was observed in snakes with skin lesions, indicating potential changes in behaviour leading to increased conflict with predators.

Jolly-Seber models indicated a population size that fluctuated between 323-780 (SE: 66.15-179.67) snakes per year. Cormack-Jolly-Seber models showed that snakes with skin lesions had approximately half the apparent annual survival through time (φ = 0.224-0.225), than those snakes without skin lesions (φ = 0.531-0.639). Moreover, the detectability of snakes with skin lesions was also significantly higher (p = 0.693-0.721) than those without lesions (p = 0.08-0.163). Ophidiomycosis may therefore lead to changes in behaviour that could potentially expose snakes to higher predation pressure.

Finally, the anti-predator behaviour of snakes was compared between snakes with and without skin lesions. Three anti-predator behaviours were observed, with musking being the most frequent, being recorded in over 75% of snakes upon initial capture. There were significant differences between the observed behaviour of snakes between both the capture and processing phases. The response of snakes to initial capture did not vary according to sex, size class, presence of skin lesions, or slough cycle. Snakes were less likely to feign death on subsequent captures than those encountered for the first time. Snakes with skin lesions also feigned death for a longer duration than those snakes without skin lesions.

Changes in the behaviour of snakes affected by ophidiomycosis may lead to reduced survival rates, posing a threat to populations if recruitment is not high enough to compensate. The findings related to the prevalence of ophidiomycosis in N. helvetica could also have implications on survey design, such as employing a risk based surveillance strategy to improve the efficiency of ophidiomycosis detection.