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Examples from Pathogens and Parasites of Wild Rodents by F Observational and model evidence for and against the dilution effect: examples from pathogens and parasites of wild rodents by Flavia Occhibove A thesis submitted to Aberystwyth University in partial fulfilment of the requirements for the degree of Doctor of Philosophy Institute of Biological, Environmental and Rural Sciences Aberystwyth University September 2018 Word Count of thesis: 70000 DECLARATION This work has not previously been accepted in substance for any degree and is not being concurrently submitted in candidature for any degree. Candidate name Flavia Occhibove Signature: Date 21/09/2018 STATEMENT 1 This thesis is the result of my own investigations, except where otherwise stated. Where *correction services have been used, the extent and nature of the correction is clearly marked in a footnote(s). Other sources are acknowledged by footnotes giving explicit references. A bibliography is appended. Signature: Date 21/09/2018 [*this refers to the extent to which the text has been corrected by others] STATEMENT 2 I hereby give consent for my thesis, if accepted, to be available for photocopying and for inter-library loan, and for the title and summary to be made available to outside organisations. Signature: Date 21/09/2018 NB: Candidates on whose behalf a bar on access (hard copy) has been approved by the University should use the following version of Statement 2: I hereby give consent for my thesis, if accepted, to be available for photocopying and for inter-library loans after expiry of a bar on access approved by Aberystwyth University. Signature: Date 21/09/2018 There is no self-awareness in ecosystems, no language, no consciousness, and no culture; and therefore no justice and democracy; but also no greed or dishonesty. ̶ Fritjof Capra, The web of life These, then, are some of the basic principles of ecology – interdependence, recycling, partnership, flexibility, diversity, and, as a consequence of all those, sustainability. [...] the survival of humanity will depend on our ecological literacy, on our ability to understand these principles of ecology and live accordingly. ̶ Fritjof Capra, The web of life Acknowledgements Firstly, I would like to express my sincere gratitude to my first supervisor Dr Claire Risley and my second supervisor Dr Joe Ironside for their continuous support through my PhD and for their advice, patience, and motivation, especially during the difficult time of the writing up. Additionally, I would like to thank Dr Kim Kenobi, without who I could not have made it through the modelling work (and through these four years). His infinite support and kindness made the impossible possible: I managed to learn how to deal with the terrifying “R”. He is honestly one of the best human being I have ever met, and I am so grateful he dedicated time to my research. Besides my supervisors, I really want to thank all the people in IBERS that provided invaluable help at every stage of my PhD journey. In particular, Dr Jo Hamilton, who gave me essential advice on macroparasite analysis, Dr Joseph Jackson, who provided useful information to design the live-trapping study, and Gareth, Rori, Julie, and Colin who fulfilled all my requests for field and lab work equipment, reducing substantially my stress levels. Outside IBERS, I am profoundly grateful to Dr Michael Kosoy, Dr Richard Wall, Dr Swaid Abdullah, and Dr Stuart Siddell for their suggestions and for providing positive controls for my PCRs. I also have to thank all the people involved in my field and lab work. First of all, Paul Culyer and his staff at the Stackpole Estate: I could not think of nicer, more supportive, and more professional people, and also of a more beautiful place to spend time outdoors. It was a fantastic experience and I am immensely grateful to all of you (especially Jon, Sam, and Alex). Secondly, the Skomer staff, Dr Tim Healing, and all the volunteers who were an invaluable help with the data collection on the island. And finally, I owe a huge thank to all the undergraduates who helped me in the field and in the lab (Aaron, Alice, Alex, Bridget, Emily, Hannah, Jacques, Karolina, Katie H., Katie W., Michaela, Nicole, Peter), and among those a “very special mention” goes to Scarlett, Joe and Tina. vii They were great research assistants, and I could not have accomplished anything without them. So many brilliant people were crucial in these PhD years. In Aberystwyth, I found an amazing community of friends and colleagues. They are all precious to me and I feel we shared so much life. Thanks to Adil, Ally, Amy, Christine, Claire, Gaspare, Lizzy, Marton, Mathilde, Max, Nathan, Paolo, Pippa, Sara, Tamsin, and last but definitely not least the great, old, wise, fatherly Niall (I will always owe you Niall, I hope you won’t ever need an organ or something because I will have to donate it to you considering my life debt!!). Thanks to my two Francesca, I am so grateful to Aberystwyth for meeting you. You are truly wonderful. Thanks to the acroyoga people, especially for meeting Bronya: thank you for the fantastic time spent away from the office. Thanks to all the Aber Organic Food Coop for supporting my ideas and me. Thanks to Julia and Rob for sorting out my living arrangements in a very difficult moment of my PhD journey. Here in Wales, I also found an “adoptive” family who welcomed me and made such a difference in my PhD experience. Thank you Alex, Jenny, Leslie, David, Sam, Jacob, and Isaac. Although they were not in Aberystwyth, I have to thank all my friends spread around the world because they are always by my side, listening, moaning, travelling, dreaming, and partying. Thank you Carmen, Claudia, Cristina, Gianluca, Laura, Ottavia, Mara, Salvatore, Teresa, Anna, Matia (and Gemmina) and so many others for taking care of me and for letting me taking care of you. And thank you my friend for supporting me during the time I was desperately looking for a PhD, and for encouraging me to embark in this one, and for make me regret my decision more than a few times. In conclusion, by far the most important acknowledgement goes to my family, in particular to my parents, to whom I owe everything. They have been the greatest support and inspiration to me, and the best life companions I could have ever desired, and there is no need to add any redundant words. Thank you. viii Abstract In disease ecology, the relationship between biodiversity and pathogen transmission is still under investigation. In particular, the dilution effect, namely that higher biodiversity decreases disease transmission, is currently the most debated eco-epidemiological theory in the context of multi-host pathogen systems. Mechanisms of dilution include transmission and encounter reduction, and susceptible host regulation. This study integrated empirical data and mathematical modelling to investigate the transmission of parasites and pathogens in Welsh wild rodent communities, as rodents are considered an ideal system to study multi-host parasite/pathogen transmission in the eco- epidemiological context. Rodents were live-trapped and faecal samples and ecto-parasites were screened for parasites and pathogens. Field data were used, where relevant, to parameterise models of infection that investigated the effects of parameter variation and community composition on pathogens with different transmission modes. The final aims were to provide additional knowledge on Welsh rodent communities, to identify rodent- borne parasites/pathogens circulating in the sampling area, and to improve understanding of local transmission dynamics, testing the dilution effect through eco-epidemiological modelling. The main results from the parasite and pathogen screening were: a. the observation of host heterogeneity in ecto-parasite and macroparasite prevalence and burden, with different host species contributing in different ways to the transmission pool; b. the isolation of Anaplasma phagocytophilum and Babesia microti in ixodid ticks; c. Bartonella spp. were isolated in fleas, B. rochalimae, notably, for the first time in the UK. The directly transmitted pathogen model outputs confirmed that reduced (or “diluted”) infection prevalence might not represent a true dilution effect to some hosts, since prevalence could decrease simultaneously with the increase of infectious individuals. The model was effective in recognising susceptible host regulation via inter-specific competition and predation as the most important dilution mechanism. Modelling the two similar but different host-tick-pathogen systems showed that the parameters affecting the juvenile stages of the ticks were the ones most affecting pathogen transmission: crucial information to develop targeted control strategies. In the system with the more generalist vector, Ixodes ricinus, dilution effect was more significant and more dilution mechanisms were observed. The key parameters regulating transmission were also different between the two systems, but the dilution was observed only with regards to infectious hosts, as more complex communities led to amplification of infectious nymphs, representing amplified human disease risk. With regards to the flea-borne Bartonella, force of infection and proportion of hosts transmitting vertically were the parameters most affecting transmission and degree of the dilution, which occurred through the mechanism of regulation of susceptible hosts, providing evidence that community composition was crucial to the dynamics of pathogen transmission. The average flea burden of infested hosts was another
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