A predictive framework to assess response of invasive invertebrates to climate change: pest mite species of Australian grains Submitted by Matthew Peter Hill, BSc. (Hons) Submitted in total fulfillment of the requirements of the degree of Doctor of Philosophy September 2012 Department of Zoology Faculty of Science University of Melbourne Produced on archival quality paper ABSTRACT Climate change is set to place enormous pressure on both biodiversity and agricultural production. Important vectors of agricultural damage, such as pest invertebrates, are likely to respond to climate change in different ways. Differing pest invertebrate responses in grain crops will translate to shifts in outbreak frequency and persistence of pests, changes to pest species assemblages, and alter biocontrol by natural enemies. Successful management will thus require predictions of how climate change will affect individual species in terms of distributions and abundance. Climate change predictions for species are often based on models that characterize distributions though species-environment relationships. However, there are important factors relating to the ecology and evolutionary biology of species that are not incorporated and will mediate climate change response. This thesis aims to establish a transferrable framework, employing multiple, complimentary lines of enquiry, to build on distribution models and understand how climate change may affect different crop pests. I focus on two important mite species groups, the blue oat mites (Penthaleus spp.) and the redlegged earth mite (Halotydeus destructor). These mite species are invasive, and so understanding how they have adapted since being introduced into Australia will help predict response to climate change in the future. The first part of this thesis applies environmental niche models to distribution data of the three cryptic Penthaleus species, to make preliminary assessments of response to climate change. These models found that the distributions of each species are governed by different climate variables, and that species assemblages are likely to shift under climate change. The remainder of the thesis builds on such models by applying a more integrated approach to assess climate change response of H. destructor. This species provides an ideal candidate to develop this framework as the biology and ecology is well understood, and its introduction and spread in Australia has been well documented. i I first build environmental niche models for H. destructor, and test key climatic variables that limit distributions. The invasive distribution of H. destructor is not predictable from its native distribution alone, and different climate variables limit the present distribution in Australia than did historically. By revealing differences in important variables, hypotheses of traits that may have shifted during invasion can be developed. For H. destructor traits related to temperature appear to have shifted over time. A laboratory study was then used to characterize thermal tolerance traits in both native and invasive ranges of H. destructor. The results suggest a shift in temperature response within Australian populations. To understand if these changes in thermal tolerance traits are correlated with population differences, DNA markers were developed and analysed across populations in both native and invasive ranges. These markers revealed high levels of gene flow between Australian populations, indicating high levels of dispersal across the continent. This may aid in the spread of any adaptive shifts in important traits, like thermal tolerance. These findings point to H. destructor persisting as an important pest species under climate change. Understanding the impacts of climate change on different pest invertebrate species is required for developing targeted management strategies. By combining different tools to investigate the species-environment relationships for H. destructor, it was possible to make a more informed prediction of climate change response. Importantly, the methods presented in this thesis allow for species-specific hypotheses to be generated and tested. The strength of the framework is that it uses simple tools in concert, so is transferrable to a broad range of pest invertebrates. ii DECLARATION This is to certify that: i. the thesis comprises only my original work towards the PhD except where indicated in the Preface, ii. due acknowledgement has been made in the text to all other material used, iii. the thesis is less than 100,000 words in lengths, exclusive of tables, maps, bibliographies and appendices Matthew Peter Hill 19th September 2012 iii PREFACE The following chapters of this thesis have either been published or have been submitted for consideration under the following titles. The nature and contribution of each author for each chapter is also described below. Chapter 2. Hill. M. P., Hoffmann, A. A., McColl, S. & Umina, P. A. (2011) Distribution of cryptic blue oat mite species (Penthaleus spp.) in Australia: current and future climate conditions. Agricultural and Forest Entomology, 14, 127–137. Hill, M.P. (PhD Candidate). Developed methods, conducted analyses and wrote manuscript. Hoffmann, A.A. Supervised development of work and edited manuscript. McColl, S. Conducted Western Australian field collections Umina, P.A. Supervised development of the work and edited manuscript. Chapter 3. Hill, M. P., Hoffmann, A. A., Macfadyen, S., Umina, P. A. & Elith, J. (2012) Understanding niche shifts: using current and historical data to model the invasive redlegged earth mite, Halotydeus destructor. Diversity & Distributions, 18, 191–203. Hill, M.P. (PhD Candidate) Developed methods, conducted analyses and wrote manuscript. Hoffmann, A.A. Supervised development of work and edited manuscript. iv Macfadyen, S. Supervised development of work and edited manuscript. Umina, P.A. Supervised development of work and edited manuscript. Elith, J. Developed methods, contributed to writing and edited manuscript. Chapter 4. Hill M. P. & Hoffmann, A. A. (in review) Increased resistance and plasticity in thermal tolerance traits support niche-shift predictions for an invasive mite, Halotydeus destructor. Global Ecology and Biogeography. Hill, M.P. (PhD Candidate) Developed methods, collected samples, conducted experiments, conducted analyses and wrote manuscript. Hoffmann, A.A. Supervised development of work, assisted with analysis and edited manuscript. v ACKNOWLEDGEMENTS First and foremost I wish to thank Ary Hoffmann for being an exceptional supervisor and guiding me through my PhD. I have learned an incredible amount by being his student, grown immensely as a scientist, and will be forever grateful for the advice and mentoring that he provided. I also sincerely thank Paul Umina and Sarina Macfadyen for being excellent supervisors on this project. I am extremely lucky to have benefited from the time and dedication they have given, the discussions and guidance, and different points of view that have helped me formalize my thoughts. Jane Elith gave a considerable amount of time to help me learn new modelling methods and I am very grateful to now possess these skills. Adam Miller lead me through the laboratory work needed to develop the microsatellite library and guided me on the analysis required. Special thanks to Linda Thomson, who has always been available for advice and supportive discussions and also provided me with opportunities to teach and work as a researcher within the laboratory, both of which I am immensely grateful. Special thanks also to Michael Nash who has always been willing to lend his support and talk about science and beyond over the period of my candidature, as well as assisting on a memorable field trip. Nancy Endersby, Andrew Weeks and Anthony van Rooyen all provided time, advice and assistance for the genetics laboratory work. Elise Furlan was a great help on the field-collecting trip to Tasmania. Emily Thomson was indispensible in helping me manage the funds and paperwork involved with this project. The Loftus-Hills memorial award from the Zoology Department allowed for me to go to South Africa, and I am very grateful to Steven Chown for hosting me in his laboratory there. Thanks to Suzaan Kritzinger-Klopper, Charlene Scheepers and Natalie Theron for assistance with South African fieldwork, and Erika Nortje for providing valuable laboratory assistance. I am forever grateful to my good friends in the laboratory – Pip, Clare, Kat, and Vale, who at different times provided reassurance, friendship and motivation. I also want to thank Re for being so understanding and supportive of me during the write-up time of this thesis. Finally I wish to thank my loving parents, Peter and Carolyn, for being supportive of me through the entirety of my education, providing support and assistance whenever I have required it. I would never have got to this stage without them! vi TABLE OF CONTENTS ABSTRACT ..................................................................................................................i DECLARATION .........................................................................................................iii PREFACE...................................................................................................................iv ACKNOWLEDGEMENTS............................................................................................vi TABLE OF CONTENTS..............................................................................................vii