Metapopulation structure of the Western Spotted Frog (Heleioporus albopunctatus) in the fragmented landscape of the Western Australian wheatbelt. Robert A. Davis BSc (Hons) Department of Zoology The University of Western Australia This thesis is presented for the degree of Doctor of Philosophy of The University of Western Australia 2004 Foreword This thesis has been written as a series of self-contained scientific papers, the majority of which are currently being considered for publication in peer-reviewed journals. At the time of writing two co-authored papers (chapters 2 and 3) have been provisionally accepted for publication, pending minor amendment. I contributed 95% to both chapters whilst the second author contributed 5%. To the remaining chapters, I contributed 100%. Publications are as follows: Davis, R.A. and Roberts, J.D. The population genetic structure of the Western Spotted Frog, Heleioporus albopunctatus (Anura: Myobatrachidae) in a fragmented landscape in south-western Australia. Australian Journal of Zoology. (accepted pending minor amendments). Davis, R.A. and Roberts, J.D. Embryonic survival and egg numbers in small and large populations of the frog Heleioporus albopunctatus in Western Australia. Journal of Herpetology. (in press, 2005). Additionally, another published paper arising from (but not a direct part of) this PhD study is appended (Appendix 1). The order of this thesis is such that each paper naturally leads to the other, and all chapters (papers) refer frequently to each other in the text. I have prepared a general introduction outlining the context of this study. Some repetitive introductory material from each chapter has been removed and placed in the general introduction. All references are placed at the end of the thesis. 1 Acknowledgements This project would not have been possible without the support of a great number of individuals and organisations. Above all I would like to thank my supervisor Dale Roberts for his friendship, guidance, constructive criticism, field assistance and insight. Dale reviewed all chapters of this thesis and they have greatly benefited from his input. My partner Jennifer Wilcox has put up with this project for longer than anyone should have to and I thank her for her love, wisdom, inspiration and friendship amongst the chaos. My long-suffering roommate Wes Bancroft has been a continual source of inspiration and I thank him for his friendship and for brightening my day. Primary funding for this research was provided by the Department of Zoology, UWA. I thank the following funding bodies for providing further financial assistance: the Peter Rankin Trust for Herpetology (The Australian Museum), the Australian Geographic Society and The Butler Trust of the Museum of Western Australia. The Department of Conservation and Land Management provided fauna licences NE002947 and SF003756. The UWA Animal Ethics Committee approved all work under licence 99/008/E92. A number of individuals have helped me with statistical advice, laboratory techniques, figures and other questions. I am indebted to Mike Bamford, Wes Bancroft, Christine Cooper and Alex Larcombe for assistance with figure preparation. Bob Black, Jane Prince and Phil Withers assisted with queries on experimental design and statistics. Without the assistance of Mike Johnson, Terrie Finston and Michelle Stuckey I would have been unable to conquer the allozyme lab! I thank them profusely. Bert and Barbara Main from UWA imparted their legendary frog knowledge to me on many occasions. Ken Aplin, Mark Cowan, Ric How and Brad 2 Maryan of Terrestrial Vertebrates at the Museum of Western Australia provided information, advice and access to museum collections. Richard Hobbs of Murdoch University and Michael and Lesley Brooker of CSIRO Sustainable Ecosystems provided information and advice. Rick Roberts, Cameron Duggin and Hai Ngo from UWA Zoology provided cheerful friendship and technical assistance. Colleagues that kindly assisted with reviewing drafts of manuscripts included Paul Doughty, Don Driscoll, Martin Dziminski and Josh Van Buskirk. I thank Henry Disney of Cambridge University, England, for identifying dipteran specimens and co- authoring our paper. I am indebted to a number of friends for providing their advice, friendship and physical assistance with fieldwork. Catherine Arrese, Wes Bancroft, Martin Dziminski, Carole Elliott, Brad Maryan, Brenden Metcalf and Jennifer Wilcox all brightened my fieldwork with their enthusiastic assistance. The transient UWA Herp Lab provided a continual source of coffee, friendship and comradeship. I especially thank Mike Smith and Phil Byrne for showing me how to live life! This project would have been impossible without the co-operation and generosity of the landowners and people of Kellerberrin who offered me accommodation, friendship and assistance when I needed it most. I am particularly indebted to Colin Wilkins and family, Frank and Noelene Morley, Rod and Judy Forsyth and family, Kit and Eileen Leake and family and Gavin and Amanda Morgan and family. Tom Groves also kindly permitted me to work on his land. I thank my family Brian, Ros and Annabelle Davis for always being there for me, and finally to Lexie for always getting in my way when I was trying to type. 3 Abstract Amidst concern over the global phenomenon of declining amphibians, there is an increasing appreciation of the importance of understanding population dynamics at both local and regional scales. Data on the viability and persistence of species in landscapes altered by humans are scarce but an understanding of these dynamics is essential for enabling long-term species conservation in a modified world. Habitat loss, fragmentation and ensuing salinisation are of particular concern for species in Australia’s temperate agricultural regions where the rapid conversion of continuously vegetated landscapes to small fragments has occurred in less than 200 years. This thesis investigated the local and metapopulation structure of Heleioporus albopunctatus to determine the current population structure and likely future of this species in a highly degraded landscape: the wheat and sheep growing areas of south- western Australia. To investigate gene flow and population subdivision, I examined genetic variation at four variable loci in twenty-two populations using cellulose acetate electrophoresis (Chapter 2). I found a moderate, but significant degree of subdivision (Fst = 0.087 ± 0.049, p<0.05) across all populations, and high levels of heterozygosity (H = 0.133, SE = 0.084). Several populations had higher Fst values in pair-wise comparisons. A significant but weak relationship was found between genetic distance and geographic 2 distance (r = 0.019, F1,229 = 4.32, p = 0.039) but this combined with data from multidimensional scaling analyses, revealed that geographic isolation of populations is not a significant determinant of genetic structuring. The regional persistence of this species may be dependent on the maintenance of current or historical metapopulation structures that allow gene flow. 4 In Chapter 3, I examined the hypothesis that small populations in marginal habitats arising from fragmentation and increased salinity, have higher embryonic mortality and lower clutch sizes than larger populations. Although four of 55 clutches examined (~ 7%) were infested by dipteran larvae, embryonic mortality was low, averaging 3% per clutch. I found no significant relationship between clutch size or embryonic mortality and population size. Success at the population level is determined primarily by the number and quality of metamorphosing larvae successfully recruited into the adult population. I investigated the recruitment success of populations of H. albopunctatus breeding in a range of ephemeral pools all derived from human modification of the landscape: e.g salinity interceptor banks (Chapter 4). The three-year recruitment success of 48 ponds monitored was poor with on average only 13.89% of ponds producing metamorphs. Hydroperiod was the most important determinant of recruitment success indicating population regulation at a local scale, with regional implications. Continued recruitment failures will have a profound impact on the survival of local H. albopunctatus populations, potentially resulting in local extinction as populations age or suffer inbreeding effects. I conducted a three year mark-recapture study of five breeding populations to quantify the variance in demographic parameters of a non-declining frog species. Adult survival ranged from 0.34 to 1. Recapture rates were low and ranged from 0.05 to 0.45. Sex ratios and estimated population sizes fluctuated greatly between years and a strong relationship existed between rainfall during the reproductive season and population size (r2 = 0.53 – 1.00). From a management perspective it is critical to be able to predict the long-term survival of this species in a human-altered landscape. In Chapter 6, I used life-history 5 data (Chapters 2-5) to undertake a Population Viability Analysis of H. albopunctatus populations to establish how local populations and metapopulations responded to variations in demographic parameters and climatic events such as drought. Juvenile survival was critical to the long-term persistence of H. albopunctatus at a regional and local scale (see also Chapter 4) but the formation of a metapopulation was sufficient to buffer H. albopunctatus against extinction in the long-term. The life-history attributes of H. albopunctatus, including high fecundity,