Health and disease in Red-crowned Parakeets (Cyanoramphus novaezelandiae) on Tiritiri Matangi Island; causes of feather loss and implications for conservation managers Dr Bethany Jackson BVSc MVS (Con Med) Murdoch University A dissertation submitted to Murdoch University in fulfillment of the requirements of a Doctor of Philosophy Supervisors Assoc Prof Kris Warren BSc, BVMS (Hons), PhD, Dip ECZM (Wildlife Population Health) Dr Richard Jakob-Hoff BSc (Hons), BVMS, MANZCVS (Wildlife Medicine) Dr Arvind Varsani BSc, PhD Dr Carly Holyoake BSc BVMS PhD Prof Ian Robertson BVSc, PhD, MACVSc (Epidemiology) November 2014 “This report, by its very length, defends itself against the risk of being read” Winston Churchill ii I declare that this thesis is my own account of my research and contains as its main content, work which has not been previously submitted for a degree at any tertiary education institution. Dr Bethany Jackson BVSc MVS (Con Med) December 2014 iii ACKNOWLEDGEMENTS Like most achievements in life, this project has come about through the generosity and support of a great many people, professionally and personally. Thank you!!! To Kris Warren, Richard Jakob-Hoff, Arvind Varsani, Carly Holyoake, and Ian Robertson for inspiration, guidance, support, feedback, encouragement, and a collective sense of humour when needed. To the Auckland Zoo and the Auckland Zoo Conservation Fund for their financial, logistical and professional support of this project, as well as me, through the residency program. It was a pleasure to work for an organisation full of passionate staff and with a clear vision of the need to connect zoos, and visitors, with in situ conservation projects and activities. An enormous thank you must go to the very many Auckland Zoo keepers and staff who provided such capable field assistance during the work, as well as some sensational cooking and entertainment packages. Also to the zoo maintenance staff for the plastic nest box extravaganza. To the Supporters of Tiritiri Matangi Island, an incredible and enthusiastic bunch of genuinely lovely people with a passion for conservation of New Zealand species. They provided support in the field, as well as feedback into the design and implementation of the study based on their vast current and historical understanding of the island. Volunteer groups like the Supporters of Tiritiri Matangi Island are fantastic ambassadors for what is achievable in conservation if you have a public that cares, which fortunately New Zealand does. To the Department of Conservation rangers and Warkworth area office staff, for providing substantial support for field logistics on Tiritiri Matangi Island and Hauturu- iv o-Toi/Little Barrier Island, including in kind funding. The project would not have been possible, or as enjoyable, without the assistance from the talented and dedicated DOC rangers and field staff on both islands, especially Dave Jenkins, Daryl Stephens, Jess Clark, Jason Campbell, Nichy Brown and the effervescent Richard, Leigh, Liam and Mahina Walle. To Allen Heath, one of the few remaining experts in morphological identification of parasites in New Zealand, and a really wonderful human being. Thank you for being as (if not more?) excited about the mites, which quite frankly turned me into a rather dull dinner party guest (Mary VA will testify). I feel incredibly fortunate to have had the opportunity to learn from and work with you. Thank you also to the following organisations and individuals for funding and support, and believing in New Zealand species and their conservation: 360 Discovery Ferries, Bivouac Outdoor, Marley Plastics, Forest and Bird New Zealand, New Zealand Veterinary Pathology, Massey University especially Brett Gartrell, Laryssa Howe and Luis Ortiz-Catedral, Long Bay College Students (who so cheerfully made the wooden nest boxes!). There are a few creatures that need to be thanked individually, for friendship and logistical support during the process, recording sighs of despair and lives saved, and enduring the endless talk about mites. They are Natalie Ann Sullivan, Danae Moore, Kate McInnes, Emma Wells, Clio Reid, Mary Van Andel, Stephanie Jervis, Kirsten Derry, Danny White, Peter Fraser, Mikaylie Wilson, Simon Fordham, Morag Fordham, John Stewart, Kay Milton, and Mary Ann Rowland. v ABSTRACT Research into the diseases of free–ranging wildlife requires targeted surveillance for pathogen(s) of interest, however also relies on reference data of general health indicators against which findings can be interpreted. Wildlife reintroductions and translocations in New Zealand introduce specific disease risks related to spread of disease agents from the source site, exposure to novel disease at the destination, or changes in transmission factors for existing diseases at the destination. The discovery of Beak and feather disease virus (BFDV) causing clinical disease in wild Red-crowned Parakeets (RCP, Cyanoramphus novaezelandiae) intended for translocation in 2008 led to an increased interest from conservation managers in the pathogens affecting this species. This study aimed to investigate health and disease in a free-ranging population of RCP experiencing feather loss, with an epidemiological focus to determine temporal trends in disease prevalence, and infer risk factors for disease expression. We captured 229 individuals over 5 sampling sessions between 2011-2013, including 4 surveys on Tiritiri Matangi Island (n=184), and one survey on Hauturu-o-Toi/Little Barrier Island (LBI) (n=45). Normal haematological and biochemical reference ranges were described. The relatively high creatine kinase results highlighted a potential susceptibility to capture myopathy in this species, and warrant further investigation. Comparison of DNA- based sexing results to beak measurements demonstrated high concordance between the two sexing methods. vi We investigated BFDV in the population by PCR of blood and feather, and found a low total prevalence on Tiritiri Matangi Island of 1.09% (0.1-3.9%) for 2011-12, and on Hauturu-o-Toi/LBI of 4.4% (0.5%-15.1%) in 2013. Screening by PCR of opportunistic samples from the Wellington region of the North Island, and phylogenetic analysis of the full viral genome sequences from all positive samples, revealed ongoing evidence of viral flow between RCP and Eastern Rosellas (Platycercus eximius) in the Hauraki Gulf/Auckland region, with separate but closely related strains from the Wellington region. These findings, combined with the first report of seroprevalence data for a New Zealand parrot using the haemagglutination inhibition test, suggest RCP may be a dead-end or spill over host for BFDV, with implications for a downgrading of the conservation threat this pathogen currently poses. The collection of skin biopsies in all birds during the 2012 and 2013 (n=135) following an outbreak of feather loss led to the discovery of a knemidokoptinid mite associated with mange in this species. The mite, Procnemidocoptes janssensi has only been previously described once from a lovebird (Agapornis nigrigenis) in Zambia in 1967. We present the first report of the mite in New Zealand, including histopathological stages of infestation, and the first epidemiological study on mange in a wild parrot globally. Relative mite abundance (number of mites per skin biopsy) was found to be associated with likelihood of feather loss and clinical signs. Findings were also consistent with the presence of a carrier or endemic state, with emergence of clinical disease and epizootics triggered by as yet unknown host, environment or mite factors. Finally, we conducted a nesting study using natural and artificial nests on Tiritiri Matangi Island from 2012-2013, to infer disease risks for nestling and fledgling RCP, and describe baseline health parameters for this group. Overall nesting success was vii low, and likely to be related to the drought experienced that year. Nest mites were detected in 64% (95%CI: 41-83%) of nests, however their presence did not significantly affect fledging success or numbers. Chicks from nest mite positive nests had higher mean absolute heterophil counts (p=0.04), suggesting an inflammatory response to the presence of these mites, and a potential fitness cost that warrants further study. We did not detect BFDV in any nests studied, and therefore cannot infer the impact of this pathogen on this age class, although the study provided further evidence BFDV is present at a low prevalence on Tiritiri Matangi Island. viii Publications from or related to this thesis Peer reviewed: Jackson B, Harvey C, Galbraith J, Robertson M, Warren K, Holyoake C, Julian L, and Varsani A. 2014. Clinical beak and feather disease virus infection in wild juvenile eastern rosellas of New Zealand; biosecurity implications for wildlife care facilities, New Zealand Veterinary Journal, 62(5): 297-301. Jackson B, Lorenzo A, Theuerkauf J, Barnaud A, Duval T, Guichard P, Bloc H, Baouma A, Stainton D, Kraberger S, Murphy S, Clark N, Dillon C, Knight T, and Varsani A. 2014. Preliminary surveillance for beak and feather disease virus in wild parrots of New Caledonia: implications of a reservoir species for Ouvea Parakeets. Emu 114(3): 283- 289. Massaro M, Ortiz-Catedral L, Kurenbach B, Kearvell J, Kemp J, Van Hal J, Elkington E, Galbraith J, Taylor G, McInnes K, Heber S, Steeves T, Walters M, Shaw S, Potter J, Farrant M, Brunton DH, Hauber M, Jackson B, Moorhouse R and Varsani A. 2012. Molecular characterisation of Beak and feather disease virus (BFDV) in New Zealand and its implications for managing an emerging, infectious disease. Archives of Virology 157(9): 1651-63. Julian L, Lorenzo A, Chenuet JP, Borzon M, Marchal C, Vignon L, Collings DA, Walters M, Jackson B, and Varsani A. 2012. Evidence of multiple introductions of beak and feather disease virus into the Pacific islands of Nouvelle-Caledonie (New Caledonia). Journal of General Virology 93(11): 2466-72. ix Jackson B, Heath A, Harvey C, Holyoake C, Jakob-Hoff R, Varsani A, Robertson I, and Warren K. 2014. First report of knemidokoptinid (Epidermoptidae: Knemidokoptinae) mite infestation in wild red-crowned parakeets (Cyanoramphus novaezelandiae); correlations between macroscopic and microscopic findings.