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Copyright Statement University of Plymouth PEARL https://pearl.plymouth.ac.uk 04 University of Plymouth Research Theses 01 Research Theses Main Collection 2019 Disease Ecology of Two Emerging Amphibian Pathogens in Costa Rica Wynne, Felicity Jennifer http://hdl.handle.net/10026.1/13665 University of Plymouth All content in PEARL is protected by copyright law. Author manuscripts are made available in accordance with publisher policies. Please cite only the published version using the details provided on the item record or document. In the absence of an open licence (e.g. Creative Commons), permissions for further reuse of content should be sought from the publisher or author. Copyright statement This copy of the thesis has been supplied on condition that anyone who consults it is understood to recognise that its copyright rests with its author and that no quotation from the thesis and no information derived from it may be published without the author's prior consent. DISEASE ECOLOGY OF TWO EMERGING AMPHIBIAN PATHOGENS IN COSTA RICA by FELICITY JENNIFER WYNNE A thesis submitted to the University of Plymouth in partial fulfilment for the degree of DOCTOR OF PHILOSOPHY School of Biological and Marine Sciences February 2019 ii Acknowledgements Firstly, I would like to thank my supervisor Robert Puschendorf for his guidance, advice and support, for which I am truly grateful. Rob, thank you for your encouragement and inspiration and thank you for introducing me to the beauty of Costa Rica. I would also like to thank my supervisors Mairi Knight and Stephen Price for their contributions. I feel privileged to have spent so much time in the field with Cheska Servini, it is cliché, but I could not have done it without you and the positive attitude and genuine enthusiasm you bring to your work. Reading through the theses of others, the significant supportive role played by family during the PhD journey becomes apparent. Through literal hurricanes, earthquakes, tsunami warnings and volcanic eruptions mine have been no exception. Dad, thank you for being my field assistant, thank you for learning how to swab frogs and most importantly, thank you for not stepping on that fer-de-lance. Mum, thank you for your endless encouragement and thank you for supporting me through proof-reading large parts of this thesis – I hope this acknowledgements page is okay! I am truly grateful for the support provided by Maria Marta Chavarria Diaz, Dan Janzen, Winnie Hallwachs and Roger Blanco from the Área de Conservación Guanacaste. Pero tambien a los padres de Robert, muchas gracias por todo – ¡estoy intentando con el Español, espero ser fluido algún día! I would like to thank the many staff and students who supported me whilst I undertook work at the Institute of Zoology. In particular thank you to Will iii Leung for his qPCR advice, Edmund Flach for road kill dissection guidance and Andrew Cunningham for the use of ranavirus isolates. I would like to extend my sincere gratitude to Conrad Hoskin, Lorenzo Bertola and Stephen Zozaya for logistical support with sample transport from Australia and to the UC Berkeley Museum of Vertebrate Zoology staff for painstakingly fulfilling my large sample request. A special acknowledgement must be made to my friends at the University of Plymouth, especially to Nick Berkeley, Kathy Redfern, Emmie Vernon and Nicola Mansfield, who have always supported me and filled me with chocolate during challenging times. Last, but by no means least, Matt – I don’t even know where to begin. Thank you for having unfaltering faith in my abilities, for pushing me, riding through both the highs and the lows with me. Thank you for conceptualising and financing our Wednesday lunch breaks, which always seemed to come at just the right time. Thank you for gecko- and newt-sitting when I was on fieldwork. Thank you for always helping me find a solution and thank you for understanding what a PhD entails. iv Author’s declaration At no time during the registration for the degree of Doctor of Philosophy has the author been registered for any other University award without prior agreement of the Doctoral College Quality Sub-Committee. Work submitted for this research degree at the University of Plymouth has not formed part of any other degree either at the University of Plymouth or at another establishment. This study was financed with the aid of a studentship from the Natural Environment Research Council and the University of Plymouth. The following external institutions were visited for consultation purposes: The Institute of Zoology, Zoological Society of London, University College London. Presentations at conferences: Plymouth University Biological and Marine Sciences Poster Event (2017), The British Ecological Society Annual Meeting (2016), Plymouth University Biological Sciences Research Day (2016). Attendance to other conferences: Tackling emerging fungal threats to animal health, food, security and ecosystem resilience (2016), Institute of Zoology student research day (2015), British Herpetological Society and Amphibian and Reptile Conservation joint meeting (2014), Garden Wildlife Health annual meeting (2014), The devourer of newts: a novel chytrid fungus on Britain’s doorstep (2014). Courses attended: Introduction to Applying for Research Funding (2018), Data Management and Manipulation (2018), Introduction to Teaching and Learning (PDAP 701) (2017), Phylogenetic Analysis using R (2015), Home Office Licensee Training Course Modules 1-3 (2014) and Amphibia Supplementary Modules 2-3 (2014), GIS – Users Workshop (2014), GIS – An Introduction (2014), Introduction to R (2014). Word count of thesis: 43,640 Signed ………………………………… Date ………17/09/2018…………… v Abstract Disease ecology of two emerging amphibian pathogens in Costa Rica Felicity Wynne The emergence of infectious diseases is increasing globally, whilst biodiversity is being lost at an unprecedented rate. The amphibian chytrid fungus (Batrachochytrium dendrobatidis) has driven the extinction of more species than any other known pathogen. This loss was particularly severe among Neotropical amphibians, with several infamous extinctions from Costa Rica. Although chytrid has been attributed to all enigmatic population declines in Costa Rica, its presence has only been investigated from a few populations. Alongside chytrid, another pathogen, ranavirus (Ranavirus spp.), is considered a significant threat to amphibian populations. Very little is known about ranaviruses outside of temperate regions, but its recent confirmation from Costa Rica has provided an opportunity to investigate both pathogens amongst declining amphibian populations. The aim of this thesis was to improve the knowledgebase of chytrid and ranaviruses in the tropics, using Costa Rica as a model system, investigate cryptic diversity among local amphibian hosts and to optimise and determine suitable diagnostics that could be used to aid ranavirus research globally. The Área de Conservación Guanacaste (ACG), northern Costa Rica was chosen as my main study location for the investigation of hosts and pathogens. The ACG is comprised of high habitat diversity that is representative of multiple tropical habitats. Samples from the ACG were used to compare four ranavirus assays to determine appropriate diagnostics. Museum specimens collected between 1976 and 1989 were used to examine how long ranaviruses have been present in northern and central Costa Rica and whether they were present during outbreaks of chytrid. The presence of ranavirus was also vi examined amongst highly threatened amphibian populations in tropical regions of Australia. I identified six candidate species of amphibian, indicating current inventories of Neotropical amphibians to be incomplete. Among the populations of these candidate species, ranavirus and chytrid are present. Chytrid was commonly found in wet forest habitats, whereas ranavirus was detected among all habitat types. However, ranavirus prevalence increased with temperature. Both pathogens were non-randomly distributed among host taxonomic families and ranavirus was detected in Costa Rican reptile species, representing the first detection of this pathogen from this group in Central America. Comparisons of ranavirus diagnostics indicated some assays to exhibit poor sensitivity and generate false positives. Using this information and a highly sensitive assay I detected ranavirus from populations sampled from prior to and during amphibian declines. Infected individuals included extinct and severely declined species. I also detected this pathogen from the order Gymnophiona, which, to my knowledge, has not been found infected with ranavirus previously. Additionally, I detected ranavirus from highly threatened Australian amphibian populations. Future research priorities should include the description of candidate species identified here using morphometrics, bioacoustics and nuclear DNA. If confirmed as true species, their conservation status should be assessed. The results of pathogen surveys among Costa Rican populations will allow researchers to identify areas and taxa more likely to be infected within the tropics. My findings from comparing ranavirus assays will facilitate the generation of highly accurate results, hence improve estimates of distribution and impacts of ranavirus. My thesis has improved the knowledge of both hosts and ranaviruses in Costa Rica, but also in tropical systems more generally, and will help guide future researchers with the effective detection of ranaviruses from these under- studied systems. vii
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