Factors influencing the epidemiology of Rabbit haemorrhagic disease virus in New Zealand A thesis presented in partial fulfilment of the requirements for the degree of Doctor of Philosophy at Massey University, Palmerston North, New Zealand Jörg Henning 2003 ii iii Abstract The European rabbit (Oryctolagus cuniculus) is a major pest species in New Zealand. The illegal introduction of Rabbit haemorrhagic disease virus (RHDV) in 1997, for purposes of biological control of pest rabbit populations, was a controversial event due to uncertainties about the impact of the disease on both rabbit populations and other potential host species. This thesis presents a series of studies conducted to investigate several aspects of the epidemiology and biology of RHDV in New Zealand, and to assess the opinions of farmers about the usefulness of RHDV for rabbit control. A longitudinal study was conducted in an area of low rabbit density near Himatangi in the lower North Island of New Zealand. Rabbits were trapped at weekly intervals over 37 months using a capture-mark-recapture approach. The study was initiated shortly after the first rabbit haemorrhagic disease (RHD) epidemic occurred in the area, and focused on evaluating the relationships between the occurrence of RHD and the dynamics of the rabbit population. Over the course of the study, predation, particularly by cats, was the principal cause of rabbit mortality. RHDV was present every year in the late summer-autumn period, but caused discernible outbreaks with high mortality only in the first and third years. Fluctuations in population immunity due to population turnover and influx of susceptible immigrants appeared to be key factors contributing to the intermittent occurrence of the disease. Infected migrant rabbits may also be a source of reintroduction of virus and new disease outbreaks. Rabbit deaths due to RHD were clustered in time and space, and RHD affected animals died closer to their home range centroid than rabbits dying of other causes. In cats, ferrets, stoats and hedgehogs that were trapped at the site, seropositivity to RHDV was detected up to several months before and after RHDV infections in wild rabbits. These predatory and scavenging species may act as vectors causing localized spread of the disease. During the course of the study, the abundance of six fly species identified as potential RHD vectors was also determined. The influence of climatic factors on fly abundance varied between species, and peaks in fly abundance in late summer and autumn coincided with RHD outbreaks. iv Two aspects of the survival of RHDV in the environment were investigated using experimental exposure of laboratory rabbits to determine viral infectivity. The survival of RHDV on two matrices (liver and cotton) exposed to environmental conditions on open pasture was evaluated. RHDV in bovine liver tissue, used to emulate a rabbit carcass, remained infective for up to three months under field environmental conditions. RHDV on cotton, which was used to emulate excreted RHDV on an inanimate substrate, remained infective for less than half that time. These observations suggest that RHDV in decomposing rabbit carcasses could be a relatively persistent reservoir of the virus. RHDV that was inactivated with UV-light failed to induce protective immunity in rabbits following oral or parenteral injection, indicating that inactivated virus on baits is unlikely to induce protective immunity in wild rabbits and thereby jeopardise the effectiveness of RHDV use. Using a multistage sampling frame, the attitudes and practices of farmers regarding rabbit control, and particularly RHDV, were evaluated using a mail questionnaire. Shooting remains the predominant method that farmers use to control rabbits, although 10% of farmers used RHDV baiting. The use of poisoning and trapping for rabbit control has declined since the introduction of RHDV. Most farmers considered that the introduction of RHDV has been beneficial. The impact of RHDV on rabbit populations appears to be highly variable. These studies have provided detailed documentation on the occurrence of RHDV and its relationship to rabbit population dynamics in an area of low rabbit density. Overall, the findings suggest that both the expected benefits and the potential ecological risks from introducing RHD to New Zealand, were overstated. While the disease certainly had a marked impact on the population at Himatangi at certain times, outbreaks were intermittent and other 'natural' causes of mortality may exert greater constraints on rabbit populations. Better understanding of the factors that contribute to the variability in frequency and severity of RHD outbreaks may enable more efficient use of this method in the future. RHDV is likely to remain a useful option for rabbit control, particularly in areas of severe rabbit proneness, and will likely prove most effective when used in conjunction with other methods. v Acknowledgements If I had not started this PhD, I might have never visited Aotearoa, New Zealand. But I came to this country and spent more then five years not only researching, but also falling in love with this ‘Land of the Long White Cloud’. This was a wonderful opportunity to learn and to live in this country, from which I will move on, like most of my supervisors did. Firstly I want to thank Dirk Pfeiffer, who sent me an e-mail from Malawi and described this project and changed my plans for the future. I never started the anticipated PhD in the Rift valley and went to Palmerston North instead where I met one of the most passionate data-analysts. I thank Dirk for his consistent exposure to all the new statistical and epidemiological tools, which make life both easy and complicated, even after his departure to England. I am so grateful to Joanne Meers, for her enthusiasm and friendship during all these years. I acknowledge gratefully her help and guidance in all aspects of virology. Joanne’s tremendous support still remained vibrant after her move to Australia. Peter Davies was another exceptional supervisor, with great wisdom and an ability to refine my many pages to the heart of the matter. I acknowledge Peter’s help in reviewing my work and I was lucky to finish most of it before he left for America. I also thank John Parkes, whose immediate reply from the South Island and help in all technical issues of the project was outstanding. I finally want to thank, my fifth supervisor, Roger Morris, who guided with his good judgment the overall progress of the work. The project involved intensive fieldwork and I thank the farmers, who allowed me to ‘chase rabbits’ on their properties. I thank the local Regional Council field staff for their encouragement from the beginning (‘…there is no way to catch a rabbit alive, the only way to get them is to shoot or poison them’) and their assistance in all ‘rabbit issues’ from night counts to night shooting. I also would like to acknowledge all the help I received from so many people from the EpiCentre, Nigel Perkins’ logical explanations, Mark Stevenson’s Aussie spirit, Cord Heuer’s unlimited experience and Ron Jackson’s philosophical approach, Deb’s and Julie’s budgeting, Fiona’s and Colleen’s secretarial assistance, and Solis Norton’s vi and Daniel Russell’s technical support. I thank all students from so many countries, who crossed my path during my time in the EpiCentre, but I am especially grateful to the German contingent, who always gave some native language support; thank you Dirk, Carola, Klim and Cord. I would like to thank all those friends I met over the years in Palmerston North and New Zealand, and the list would be too long to name all of them, but I would like to especially thank Sylvia, Delwyn, Peter, Petra, Steffen, Bruce and Joanna. I thank my partner Sonja, who came to live with me in New Zealand, and I appreciate her help with radio-tracking rabbits through thorny gorse bushes and her patience for waiting until everything was written up. Finally I want to thank my family in Germany. Thank you Kerstin, my sister, for the parcels with items from our former ‘Heimat’. I thank my parents for their endless support. They visited me and I saw them a few times back home, but I can only imagine how difficult it must have been for them to see me always flying back to the other side of the planet. ‘Writing in the speed of thoughts remains the dream of an author’ (Heiner Müller, East-German play writer in ‘Krieg ohne Schlacht’, 1999, Kiepenheuer and Witsch, Köln, Germany), and thoughts need nutrients to flourish. I also found strength and joy for my research in the hours I spent away from it, on the top of some mountains or in remote rugged patches of native bush, and must therefore somehow acknowledge the New Zealand wilderness. Jörg Henning EpiCentre, Institute of Veterinary, Animal and Biomedical Sciences Massey University, Palmerston North, New Zealand 26th June 2003 vii Table of Contents ABSTRACT.................................................................................................................iii ACKNOWLEDGEMENTS.......................................................................................... v TABLE OF CONTENTS............................................................................................vii LIST OF FIGURES ...................................................................................................xiii LIST OF TABLES.....................................................................................................xvi LIST OF APPENDICES............................................................................................xix