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This thesis has been submitted in fulfilment of the requirements for a postgraduate degree (e.g. PhD, MPhil, DClinPsychol) at the University of Edinburgh. Please note the following terms and conditions of use: This work is protected by copyright and other intellectual property rights, which are retained by the thesis author, unless otherwise stated. A copy can be downloaded for personal non-commercial research or study, without prior permission or charge. This thesis cannot be reproduced or quoted extensively from without first obtaining permission in writing from the author. The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the author. When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given. Diseases of wild birds of the orders Passeriformes and Columbiformes - a review of conditions reported from the United Kingdom and an analysis of results from wild bird disease surveillance in Scotland 1994-2013 Thomas William Pennycott BVM&S Cert PMP MRCVS Thesis submitted in accordance with the requirements of the University of Edinburgh for the degree of Doctor of Veterinary Medicine and Surgery 2016 i Diseases of wild birds of the orders Passeriformes and Columbiformes - a review of conditions reported from the United Kingdom and an analysis of results from wild bird disease surveillance in Scotland 1994-2013 Declaration I declare that this thesis has been composed by myself, and that my input to the disease investigations was as described in the Materials and Methods. Some of the findings have been previously published in letters, short communications or papers in the scientific press, as referenced in the appropriate sections of the thesis. The body of work presented in this thesis has not been submitted for any other degree or professional qualification. Thomas William Pennycott 29/01/16 ii ABSTRACT There is growing concern about the impact of human activities on wildlife, both at the level of the individual animal and at a global population level, and the need for surveillance of wildlife for evidence of infectious and non-infectious diseases has never been greater. There is also much interest in attempting to help wildlife by treating and rehabilitating sick and injured wild animals and by providing supplementary feeding to garden birds. This thesis reviews the literature describing the diseases found in the United Kingdom (UK) in different birds of the orders Passeriformes and Columbiformes, the orders of birds with which members of the general public and wildlife rehabilitators are most likely to have contact. The thesis then collates and analyses the postmortem findings from wild bird surveillance carried out on 2048 birds of these orders at one diagnostic laboratory in Scotland over a twenty-year period (1994- 2013). The overall aim was to make maximum use of surveillance data already gathered but not previously readily available, to inform those involved with wildlife disease surveillance, wildlife rehabilitation, and members of the public providing supplementary feeding to garden birds. During the 20 years of wild bird disease surveillance, 42 endemic conditions or pathogens were identified, raising awareness and increasing our understanding of these conditions. One re-emerging disease, salmonellosis, came to prominence and then declined during the surveillance period, and was confirmed in approximately 350 garden birds. Two new conditions were described in finches; Escherichia albertii bacteraemia in approximately 150 finches and Trichomonas gallinae infection in approximately 370 finches. The large numbers of birds with salmonellosis, E. albertii bacteraemia or trichomonosis permitted further analysis by species of bird, geographic region, and distribution by age and sex, permitting conclusions to be drawn regarding the epidemiology of these diseases. Two new conditions were diagnosed in choughs (Pyrrhocorax pyrrhocorax), a species of conservation concern in the UK; a developmental abnormality of the eye and sometimes brain of young choughs, most iii likely inherited, and significant helminthosis caused by spirurid gizzard worms and intestinal thorny-headed worms. These findings will influence future attempts to conserve this species in Scotland. Another new condition encountered was enteritis and/or hepatitis associated with schistosome-like eggs, diagnosed in blackbirds (Turdus merula) and a dunnock (Prunella modularis). More specific identification of the causal organism and evaluation of potential zoonotic implications are required. Two conditions were investigated for which no satisfactory aetiological agent could be identified; a non- suppurative encephalitis affecting multiple fledgling starlings (Sturnus vulgaris) and house sparrows (Passer domesticus), and a necrotic oesophagitis of unknown cause detected in five chough nestlings. Three organisms identified in wild birds elsewhere in the world and found for the first time in the UK as part of this surveillance study were the avian gastric yeast Macrorhabdus ornithogaster (“megabacteria”) in greenfinches (Chloris chloris) and a waxwing (Bombycilla garrulus), Mycoplasma sturni in blackbirds, starlings and corvids, and Ornithonyssus sp. mites in corvids. Screening for two zoonotic pathogens exotic to UK wildlife, highly pathogenic avian influenza virus (HPAIV) and West Nile virus (WNV) was carried out on over 600 samples and over 500 samples respectively, but no positive results were obtained. Investigation of novel and re-emerging conditions and screening for exotic pathogens relied heavily on work carried out by other laboratories, underlining the importance of collaboration between multiple laboratories when carrying out disease surveillance. To aid those working in wild bird disease surveillance, diagnosis and treatment, a collection of approximately 700 images of lesions, parasites and their eggs or oocysts is included as an appendix to this thesis, as has a guide to the presumptive identification of some of the internal parasites encountered. This study has demonstrated the ever-changing nature of diseases of wild birds of the orders Passeriformes and Columbiformes, and the same is likely to be true of wild birds in other orders. Continued wild bird disease surveillance is essential, to help safeguard the health of wildlife, livestock, humans, and indeed the environment itself. iv ACKNOWLEDGEMENTS There were two overlapping phases to this work, namely the initial submission and examination of carcases for the purposes of wild bird disease surveillance, followed by the retrospective collation, analysis and interpretation of the results and preparation of this thesis. A vast number of people assisted in the first phase and assistance of a different nature was given in the second phase, and I am extremely grateful to all concerned. The initial investigations were only possible because of funding from a wide range of sources including the Scottish Office Agriculture, Environment and Fisheries Department (SOAEFD); Janssen Animal Health; the Royal Society for the Protection of Birds (RSPB); Bayer Animal Health; Scottish Natural Heritage (SNH); the Dulverton Trust; the Game and Wildlife Conservation Trust; Richard and Margaret Cinderey; the Galloway Wildlife Refuge; CJ Wildbird Foods Ltd; the Scottish Agricultural College (SAC) Trust Fund; the Garden Bird Health initiative and funders; and the Scottish Government as part of its Public Good Veterinary and Advisory Services. My thanks to all the funders, of whom more details can be found in Section 2.2 of the thesis. Without carcases there could not have been wild bird disease surveillance, and the assistance of those members of the general public, wildlife rehabilitators, veterinary surgeons, gamekeepers, local authority employees and others who submitted carcases is gratefully acknowledged. The large number of carcases received is testimony to their enthusiasm and commitment. I was fortunate to have the backing of the Management Team of SAC Consulting Veterinary Services (SACCVS), and of Jesus Gallego, Veterinary Adviser to the Scottish Government, for support in developing wild bird disease surveillance in Scotland over the years. This was much appreciated. At a practical level, the wild bird surveillance carried out at Ayr Disease Surveillance Centre (DSC) was only possible v because of the skills and professionalism of the veterinary, scientific, administrative and support staff. Without their input, the number of confirmed diagnoses would have been substantially reduced, the results of the postmortem examinations would not have reached those submitting the birds, and the appropriate environment for carrying out the postmortem examinations would not have been available. One of the advantages in working for SACCVS was access to scientists at several different laboratories throughout the organisation, each with their own areas of expertise. My thanks to all at Ayr DSC and elsewhere in the organisation for their patience and support, sometimes indulging me when I made unusual requests in my pursuit of a diagnosis. Inevitably, satisfactory disease surveillance requires considerable collaboration with other institutes, and I am most grateful to those people and institutes listed below. Further details of the assistance provided by each organisation can be found in Section 2.5 of the thesis. Alisdair Wood and Cristina Garcia-Rueda, Animal Health and Veterinary

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