Avian influenza virus dynamics in Australian wild birds by Marta Ferenczi MSc. (Hons) Submitted in fulfilment of the requirements for the degree of Doctor of Philosophy Deakin University May, 2016 Acknowledgements I would like to express my special appreciation and thanks to my principal supervisor Professor Dr. Marcel Klaassen. Marcel, you have been a great mentor for me. I would like to thank you for your continued support throughout my “PhD journey” and for believing that I would grow as a research scientist, even in hard times. I feel lucky that I could spend quite a lot of time with you in the field and I will never forget our desert expeditions. I would also like to thank my fantastic second supervisor Dr. Christa Beckman for her incredible help. Christa, your advice on both research as well as my career have been priceless. You were always there for me if I needed help, either in writing or in statistics. I would like to thank my other supervisors, Dr. David Roshier and Professor Bill Buttemer for their contribution to my thesis. David, if I had not met you in the Prairie in Russia, I probably would have never gotten this fantastic opportunity to do a PhD in Australia. Thank you for all your useful comments on the various chapters too. Bill, I always enjoyed the chats with you about science as well as those not about science. You gave really useful final comments on my thesis. I would especially like to thank my fellow PhD students, Yaara Aharon-Rotman, Simeon Lisovski, Meijuan Zhao and Alice Risely for their amazing support. Yaara, you are the one who broke the ice and gave advice about how to write a confirmation, annual review and a lot more. You also knew how to “handle” a supervisor. As a friend you made my life as PhD student much easier! Simeon, thank you for all your help with statistics, R scripts and graphs. It has been a pleasure getting to know such a talented bloke as yourself. Mei and Alice, you two make me feel as though I do not want to leave the office (however you know how much I don’t like being indoors)! We have had so much fun together and your friendship has made my PhD journey much more enjoyable. Mei, thank you so much for all your help in database handling, R programming and statistics. Your help is priceless. I am extremely lucky that my desk neighbour in the office was such a talented young woman. Alice, I am very glad that you joined our team, you bought lots of laughs and sarcastic humour when you moved into the office. Thank you also for the great times that we spent together outside the office surfing, swing dancing, partying etc. We will continue! I would also like to mention the other smiley faces from the corridor, the members of “Bird Angels”: Eliza Larson, Ondi Crino and Aida Rodrigues, for their amazing emotional support during my PhD. You girls rock! Jacintha van Dijk, while most of the time working on her PhD was far away from our group, the time that she spent here was lot of fun! Jacintha, you gave me really great advice about PhD life. We developed a great friendship in a short period of time and I hope we will meet again soon in some part of the world! I am really glad that Beata Ujvari joined our group. Bea, your kindness, friendship and support means a lot to me. Speaking our mother tongue always warms my heart. Kerry Petterson Fanson and Lee Ann Rollins always have been really helpful for me during the last four years. During our shared car lifts I learned heaps about science, American accents and a lot more. Thanks girls! I would like to thank Peter Biro and Ben Fanson for the great discussions about statistics. Pete, I really enjoyed the sessions with you. You even talk about stats and manage to make it interesting. Ben, thank you for your help in R and introducing me ggplot2. That R package made my graphs much nicer, I think. I would like to thank Andrew Cerasuolo for his fantastic IT help. You have always been there for me if I had problems with different computer programs. I really enjoyed our discussions about birds and rock music too! I would like to thank Natasha Kaukov for her great support and help in administrative tasks. Natasha, it was always very nice to chat to you. Thank you for your kindness and great help. I would like to thank to my mentor, friend and master goose catcher, Gerhard Muskens. Gerhard you always believed in me and stuck up for me. Without you telling me that I should not be afraid to move to the other side of the globe to pursue my dreams, I would not be in my current position. Thank you Gerhard, I cannot wait to visit you in the Netherlands! I would like to thank Kamilla, the person who has been my best friend for 25 years for her endless support. Even being so far from each other in the last few years, our relationship did not change. Thank you for being happy for me when I had success and thank you for crying with me in hard times. It means a lot to me! Last but not least, a huge special thanks to my family. Words cannot express how grateful I am to my mother, Agi and my father, Zoli for all of the sacrifices that you have made on my behalf. I am extremely lucky to have such beautiful, lovely and caring parents. I know that you were very sad when I decided to move to Australia as we have never been away from each other before. But you were there for me when preparing for this huge journey and even came after me when I missed you so much. This PhD thesis is dedicated to you! I also thank my sister Dori and her family (Bali, Bibi and Edi) for their fantastic support over the last few years. The skype chats have helped me a lot to handle being homesick. Your love and smile always helped me to get going! Lastly, I would like to express appreciation to my beloved husband, Gyula. You have not even hesitated for a moment when I told you that I would like to move to the other side to globe to do some crazy science stuff. You just said “let’s go, where ever you are, I’ll go there too!” You are an amazing person, always supportive, kind, understanding, caring and loving. Doing a PhD was a challenging journey for both of us, but you did not doubt for a second that I could do it. This PhD is as much as yours as mine. Documents that have been accepted for publication resulted from this work Marta Ferenczi, Christa Beckmann, Simone Warner, Richard Loyn, Kim O'Riley, Xinlong Wang, Marcel Klaassen: Avian influenza infection dynamics under variable climatic conditions - viral prevalence is rainfall driven in waterfowl from temperate, south-east Australia, Veterinary Research (VETR-D-15-00177) Author’s affiliations Marta Ferenczi ([email protected]) 1 Christa Beckmann ([email protected]) 1 Daniel Ierodiaconou ([email protected]) 1 Marcel Klaassen ([email protected]) 1 Simeon Lisovski ([email protected]) 1 Richard Loyn ([email protected]) 2 Kim O'Riley (Kim.O'[email protected]) 3 David Roshier ([email protected]) 1, 4 Xinlong Wang ([email protected]) 3 Simone Warner ([email protected]) 3 1 Centre for Integrative Ecology, School of Life and Environmental Sciences, Deakin University, Geelong, Locked Bag 20000, Victoria 3220, Australia 2 Arthur Rylah Institute for Environmental Research, Department of Sustainability and Environment, Heidelberg, Victoria, Australia; current address Director, Eco Insights, 4 Roderick Close, Viewbank, Victoria 3084, Australia. 3 Department of Economic Development, Jobs, Transport and Resources, Biosciences Research, AgriBio, Centre for AgriBiosciences, 5 Ring Road, Bundoora, Victoria 3083, Australia 4 Australian Wildlife Conservancy, Adelaide, Halifax Street, PO Box 6621, South Australia 5000, Australia Contents CHAPTER 1 – General introduction ...............................................................................................2 CHAPTER 2 – A description of the avian influenza reservoir community in wild Australian birds and the role of phylogeny, ecology and eco-region ......................................24 CHAPTER 3 – Avian influenza infection dynamics under variable climatic conditions – viral prevalence is rainfall driven in waterfowl from temperate, south-east Australia .................................................................................................................57 CHAPTER 4 – Non-seasonal and long-term avian influenza virus (AIV) dynamics in Australia’s arid interior suggest bird numbers, age structure and immunocompetence influences AIV susceptibility ..............................................100 CHAPTER 5 – Rainfall driven and wild-bird mediated avian influenza virus outbreaks in Australian poultry .................................................................................................133 CHAPTER 6 – Synthesis: Synthesis: Avian influenza virus dynamics in Australian wild birds……………. .................................................................................................159 Curriculum vitae ..........................................................................................................................176 1 CHAPTER 1 General introduction Marta Ferenczi 2 Knowledge of infection dynamics is central to our understanding of zoonotic diseases, their impact on wildlife populations, and their potential to spillover into domestic or human populations (Paull et al. 2012). Pathogen prevalence can fluctuate dramatically and how prevalence is affected by different environmental factors is still poorly researched in some areas (Altizer et al. 2006, Gaidet 2015). Avian influenza virus (AIV) is one of the zoonotic diseases that cause major concern in respect to public and domestic animal health (Gilbert and Pfeiffer 2012, Liu et al. 2013, Gilbert et al. 2014). Since the first outbreaks of highly pathogenic avian influenza H5N1 in 2003 and H5N8 in 2014, these particular subtypes of the virus began to spread rapidly around the globe, resulting in high socio-economic costs (Gilbert and Pfeiffer 2012, Liu et al.