The ecology and host-parasite dynamics of a fauna translocation in Australia Judy Dunlop BSc (Hons) A dissertation submitted to Murdoch University in fulfillment of the requirements for a Doctor of Philosophy March 2015 Supervisors: Professor R. C. Andrew Thompson, Murdoch University Mr Keith D. Morris, Department of Parks and Wildlife Dr. Stephanie S. Godfrey, Murdoch University - 1 - - 2 - [The naturalist] looks upon every species of animal and plant now living as the individual letters which go to make up one of the volumes of our earth's history; and, as a few lost letters may make a sentence unintelligible, so the extinction of the numerous forms of life which the progress of cultivation invariably entails will necessarily render obscure this invaluable record of the past. It is, therefore, an important object [to preserve them]. If this is not done, future ages will certainly look back upon us as a people so immersed in the pursuit of wealth as to be blind to higher considerations. Alfred Russel Wallace, Journal of the Royal Geographical Society 1863 - 3 - - 4 - Declaration I declare that this thesis is my own account of my research and contains as its main content work that has not been previously submitted for a degree at any other tertiary education institution. Judy Dunlop BSc (Hons) March 2015 - 5 - - 6 - Acknowledgements My sincere thanks and gratitude to my supervisors, Professor Andrew Thompson, Mr Keith Morris and Dr Stephanie Godfrey for their support, direction and patience during the undertaking of this degree. This project received funding as part of Environmental Offset Conditions of the Barrow Island Act 2003 in an attempt to ameliorate the impact of the Gorgon Gas Development on Barrow Island fauna. This work was carried out under the Department of Environment and Conservation animal ethics permit DEC AEC 2010 / 01, and Murdoch University animal ethics permit W2337/10. I am very grateful to Louise Pallant, Adriana Botero-Gomez, Aileen Elliott and Angela Reeves at Murdoch University for their guidance in the SABC and PCR problem-solving wizardry. Without them I would have been evicted from the SABC very early on. To Emily Miller for so much good advice, teaching me how to take blood like a pro and making tedious field times enjoyable. To Craig Thompson for sharing his joy of parasites and always a willing accomplice when we needed a break – I would have quit by year two had you not been there. To the great number of volunteers who assisted with my fieldwork, and trusted me to take them a long way from civilisation on the promise of free food and catching animals. And Grace, Trent and Maynard, who were always there for me. I am very grateful to Ian Abbott, Wes Bancroft, Simon Cherriman, Zoe Davies, Tim Doherty, Mark Eldridge, Manda Page, Andy Smith, David Watson, Adrian Wayne and Matt Williams for their editorial, statistical and cartographical assistance. Your knowledge and expertise was invaluable, thankyou. Finally, I wish to thank my wonderful family and friends who stood by me and encouraged me throughout. I owe you a lot. - 7 - - 8 - Abstract Despite the frequency of fauna translocations as a technique to improve the conservation status of threatened species, new populations frequently fail to establish. Translocations often lack experimental manipulation to determine ‘best practice’ methods to improve success. One poorly understood element of translocation science is the impact of parasites and disease-causing pathogens on the animals moved and the ecosystem they are moved into. Of 58 published Australian translocations in the last 40 years, only 20 (35%) employed any level of parasite management, despite potential contribution of disease to initial fauna declines. I closely investigated a translocation of boodies (Bettongia lesueur) from Barrow Island and Dryandra to Lorna Glen, and ‘island dwarf’ golden bandicoots (Isoodon auratus) from Barrow Island to Lorna Glen and Hermite Island. Bandicoots born into the new populations showed an increased skeletal size and body mass (males) and reproductive output in the number and average size of young (females). These changes occurred within 18 months of release, suggesting that responses were due to phenotypic plasticity, rather than selective pressure occurring over many generations. I conclude that the small size of bandicoots on Barrow Island is a response to resource limitation, rather than true island dwarfism. I determined the impact on parasite load and survivorship of translocated animals by treating half the population with a topical antiparasitic. Despite frequent trapping (six- weekly) and very high recapture rate (64–99%), repeated dosage did not significantly impact ectoparasite or haemoparasite infection, or survival of the marsupials. I observed transmission of parasites between animals of different origin and to offspring, and a - 9 - decline in species diversity present in the translocated population due to the failure of some species to persist. This thesis identified knowledge gaps in the translocation literature and addressed some key concepts of species ecology, population dynamics and parasitology via post- translocation monitoring. - 10 - DECLARATION 5 ACKNOWLEDGEMENTS 7 ABSTRACT 9 LIST OF FIGURES 17 LIST OF TABLES 19 THESIS LAYOUT 21 CHAPTER 1. INTRODUCTION THE HITCHHIKER’S GUIDE TO AUSTRALIA: A PARASITOLOGICAL PERSPECTIVE ON NATIVE AND EXOTIC FAUNA TRANSLOCATIONS 23 ABSTRACT 25 INTRODUCTION 27 DATA COLLATION AND SCOPE OF REVIEW 29 RECENT FAUNAL MOVEMENTS IN AUSTRALIA 30 FAUNAL MOVEMENTS FOR CONSERVATION 30 AUSTRALIAN FAUNA TRANSLOCATIONS SINCE 1970 32 EARLY FAUNA INTRODUCTIONS 42 DELIBERATE INTRODUCTIONS LINKED TO AGRICULTURAL AND PASTORAL ENTERPRISE 42 INTRODUCTION FOR BIOLOGICAL CONTROL 44 INTRODUCTION OF COMPANION ANIMALS AND PEST SPECIES 46 HISTORICAL FAUNAL DECLINES ASSOCIATED WITH PARASITES 47 MANAGEMENT IMPLICATIONS 50 CONCLUSIONS AND OBJECTIVES OF THIS THESIS 53 CHAPTER 2. GENERAL METHODS: TRANSLOCATION STUDY SITE AND SPECIES 57 LORNA GLEN 59 CLIMATE AND RAINFALL 60 SPECIES DIVERSITY 61 FAUNAL DECLINES IN AUSTRALIA 63 - 11 - FERAL CAT CONTROL 64 MAMMAL REINTRODUCTIONS 65 STUDY SPECIES 71 BOODIES 71 GOLDEN BANDICOOTS 76 TRANSLOCATIONS 79 CHAPTER 3. SENSITIVITY TESTING OF TRYPANOSOME DETECTION BY PCR FROM WHOLE BLOOD SAMPLES, USING MANUAL AND AUTOMATED DNA EXTRACTION METHODS 83 ABSTRACT 85 INTRODUCTION 86 METHODS 89 TRYPANOSOME SAMPLE PREPARATION 89 EXPERIMENTAL DESIGN 89 DNA EXTRACTION 90 PCR PRIMERS AND METHODS 91 DATA ANALYSIS 93 RESULTS 93 DISCUSSION 98 CHAPTER 4. HOST-PARASITE DYNAMICS OF TRYPANOSOMES AND ECTOPARASITES ON A TRANSLOCATED POPULATION OF AUSTRALIAN MARSUPIALS 103 ABSTRACT 105 INTRODUCTION 106 METHODS 110 STUDY SPECIES 110 TRANSLOCATIONS AND MONITORING 111 SAMPLE COLLECTION 112 - 12 - SAMPLE ANALYSIS 113 DATA ANALYSIS 114 RESULTS 116 TRAPPING DATA 116 ECTOPARASITE PREVALENCE AND SPECIES RICHNESS 117 FACTORS ASSOCIATED WITH PARASITE PREVALENCE 123 POST-RELEASE SURVIVAL 127 DISCUSSION 128 ECTOPARASITE SPECIES DIVERSITY 131 IMPACT OF TRANSLOCATION ON TRYPANOSOME DYNAMICS 132 TRYPANOSOME VECTOR CORRELATION 134 INTERACTION BETWEEN ECTOPARASITES, SEASON AND TRYPANOSOME INFECTION 135 MANAGEMENT IMPLICATIONS 136 CHAPTER 5. ENVIRONMENTAL DETERMINATION OF BODY SIZE IN MAMMALS: RETHINKING ‘ISLAND DWARFISM’ IN THE GOLDEN BANDICOOT 139 ABSTRACT 141 INTRODUCTION 142 METHODS 144 STUDY SPECIES 144 STUDY SITES AND RELEASE PROTOCOL 146 MONITORING AND TRAPPING 149 BODY CONDITION INDEX (BCI) 150 STATISTICAL ANALYSES 151 RESULTS 152 COMPARISONS BETWEEN RECRUITED (HI, LG) AND SOURCE (BI) BANDICOOTS 152 EFFECT OF TRANSLOCATION ON FOUNDER INDIVIDUALS 158 DISCUSSION 160 - 13 - RESPONSE OF FOUNDER INDIVIDUALS 161 RESPONSE OF RECRUITED INDIVIDUALS 161 RELEVANCE TO THE ISLAND RULE 162 CHAPTER 6. GETTING CLOSE TO THE MARK: AN EMPIRICAL TEST USING CAPTIVE POPULATIONS OF BOODIES AND GOLDEN BANDICOOTS 167 ABSTRACT 169 INTRODUCTION 171 METHODS 173 STUDY SPECIES 173 STUDY AREA 173 TRAPPING 174 INDIVIDUAL MARKS 176 DATA ANALYSIS 176 RESULTS 177 TRAPPING 177 MODEL CHOICES 180 SURVIVORSHIP 181 CAPTURE PROBABILITY 184 POPULATION ESTIMATES 185 DISCUSSION 187 SURVIVORSHIP 187 CAPTURE PROBABILITY AND POPULATION ESTIMATION 191 CHAPTER 7. GENERAL DISCUSSION 193 INTRODUCTION 195 OVERVIEW OF FINDINGS, THEIR CONTRIBUTION TO KNOWLEDGE AND FUTURE QUESTIONS 195 HOST – PARASITE DYNAMICS 195 - 14 - TRANSLOCATION ECOLOGY 201 CONTRIBUTION OF THIS THESIS TO A GREATER BODY OF KNOWLEDGE 204 PUBLICATIONS ARISING FROM THIS AND ASSOCIATED RESEARCH 207 PEER-REVIEWED PUBLICATIONS 207 SUBMITTED PAPERS 207 MANUSCRIPTS IN PREPARATION 208 CONFERENCE PRESENTATIONS 208 OTHER PUBLICATIONS DURING CANDIDATURE 209 APPENDIX COAUTHORED PEER-REVIEWED MANUSCRIPT 211 REFERENCES 223 - 15 - - 16 - List of Figures Figure 1. Location of two ex-pastoral leases managed by Department of Parks and Wildlife (Western Australia), showing Lorna Glen (Matuwa) and neigHboring EaraHeedy (Kurrara Kurrara) relative to tHe closest town, Wiluna. _________________________________________________________________________________________________________________ 60 Figure 2. Mean montHly rainfall and temperatures for Wiluna weather station, 1899–2013. Data source; BoM (2013). __________________________________________________________________________________________________________________ 60 Figure 3. Annual rainfall for Wiluna weatHer station, 1900–2013. Source: BoM (2013) __________________________ 61 Figure 4. Bullimore land system tHat dominates tHe soutHern Half of Lorna Glen; spinifex (T. basedowii)