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Coastal Mycology: Boundary Conditions for Arbuscular Mycorrhizal (AM) Fungi in Incipient Sand Dunes

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Coastal Mycology: Boundary Conditions for Arbuscular Mycorrhizal (AM) Fungi in Incipient Sand Dunes Coastal mycology: Boundary conditions for arbuscular mycorrhizal (AM) fungi in incipient sand dunes Lynda Michelle Lever ORCID 0000‐0003‐3857‐8556 Submitted in total fulfilment of the requirements of the degree of Doctor of Philosophy June 2018 Faculty of Science, School of Geography The University of Melbourne Abstract Little is known about the relationship between the colonization by arbuscular mycorrhizal (AM) fungi in grasses in the ephemeral environment of incipient sand dunes. Yet, consideration of dune vegetation without including the soil biota in the substrate, means that a significant biological component of the dune system is ignored. Ephemeral incipient dunes are an extreme and environmentally stressful ecosystem, encountering strong and salt-laden winds, sea water overwash, and low nutrients and these dunes are subject to a frequency and magnitude of storm action that foredunes are not. Incipient dunes represent a challenging opportunity in which to add to our understanding of coastal AM fungal tolerances, species richness and biogeography, in association with their equally resilient symbionts. Arbuscular mycorrhizal fungi are ubiquitous in soil, and have an association with approximately 90% of terrestrial vascular plants, exchanging mineral nutrients and water for carbon compounds. These fungi are the most common mycorrhizal fungi in the sand dune ecosystem, and play a significant role in the establishment and proliferation of pioneer plants such as Thinopyrum junceiforme (Sea Wheatgrass), an exotic C3 dune grass, and the native C4 dune grass, Spinifex sericeus (Hairy Spinifex). The unifying hypothesis was that AM fungi in incipient dunes have life history strategies that equip them for disturbance and sodium chloride levels not found in other contexts. A series of specific subordinate hypotheses, building one upon the other were posed to fill knowledge gaps on two mutualist plants and the biogeography of coastal arbuscular mycorrhizal (AM) fungi. The edaphic conditions the symbionts inhabit were analysed and compared, and differences were quantified of coastal AM fungal species, which it was hypothesized would differ across successional gradients. It was demonstrated that even in nutrient-poor ecosystems, substrate chemistry plays a significant role in influencing fungal communities. Furthermore, analyses confirmed differences in the presence of these fungal species between the incipient dune and foredune, the former of which was hypothesized would select for coastal fungi that are i better adapted to the disturbance regime. This highlighted that life history strategies have clearly favoured the most robust mutualists. The hypothesis that coastal arbuscular mycorrhizal fungi are resilient to levels of sodium chloride far greater than those traditionally used in saline-tolerant studies was tested and confirmed, as it was for their host Sea Wheatgrass, whose production of roots was unaffected by saline irrigation. It was clearly demonstrated that Sea Wheatgrass exhibits an extraordinary phenomenon of resource allocation to roots rather than tillers when under stressful conditions. Such life history strategies allow this r-strategist to survive the hostile environment of incipient dunes. Investigation of a further hypothesis illustrated that temporal dynamics of mycorrhizal colonization in dune grasses changes seasonally, as soil temperatures influence microbial populations. Furthermore, disturbance specialist arbuscular mycorrhizal fungi rapidly colonized plant remnants following storm scarping, supporting the hypothesis that these disturbance specialists would be found in higher proportions in plant roots post storms, than pre-storms. The knowledge generated in this thesis provides a greater understanding of the robust subterranean ecology of coastal sand dunes, and highlights the biogeography of the coastal arbuscular mycorrhizal fungi found at the research site on the southern Australian coast. Furthermore, findings of this study challenge two points in previous studies concerning the veracity of Sea Wheatgrass in outcompeting Hairy Spinifex and of Sea Wheatgrass building incipient dunes with a greater resilience to storm events than those built by Hairy Spinifex. These findings were not substantiated by my study. ii Dedication To my unborn child, who never saw the light of day. Mummy loves you darling. ‘Would you know my name, if I saw you in Heaven?’ Eric Clapton iii Declaration This is to certify that: 1. The Thesis comprises only my original work towards the PhD except where indicated in the Preface. 2. Due acknowledgement has been made in the text to all other material used. 3. The Thesis is fewer than 100,000 words in length, exclusive of tables, figures, bibliographies and appendices. Lynda Michelle Lever, June 17, 2018 v Preface Chapter 2 is comprised of a substantially unchanged manuscript that has been published in Plant Protection Quarterly, The Biology of Australian Weeds 63, (2014) 29(4), 120 - 126. The authors of this manuscript are L.M. Hanlon (Lever), and M.B. Mesgaran. Lynda Michelle Hanlon (Lever) is the primary author, and contributed greater than 50% of the content. Lynda Michelle Hanlon (Lever) wrote the initial draft of the paper and performed subsequent editing in response to the comments of the editors. Chapter 3 is comprised of a substantially unchanged manuscript that has been published in the Journal of Coastal Research, (2016), 1 (57) (SI 75), 283 - 287. The authors of this manuscript are L.M. Hanlon (Lever), L.K. Abbott, and D.M. Kennedy. Lynda Michelle Hanlon (Lever) is the primary author and contributed greater than 50% of the content. Lynda Michelle Hanlon (Lever) wrote the initial draft of the paper and performed subsequent editing in response to the comments of co-authors. vii Acknowledgements I wish to express my great thanks to my Supervisors, Associate Professor David Kennedy, The University of Melbourne, and Emeritus Professor Lyn Abbott, The University of Western Australia, for their guidance and advice throughout this journey. One does not arrive at the end of PhD research without having travelled many roads to get there. Along those roads, I have had the honour of encountering many splendid people who have walked part way, or all of the way with me, offering encouragement, support and sage advice. Lyn, you feature prominently along that walk, and I am so very grateful for your friendship and guidance, and offer my deep respect in return. I am indebted to you for your financial support of the molecular analyses in my research. I am deeply appreciative of other academics who gave me the courage to believe that what I was undertaking really was worthwhile. In particular, Professor Richard Koske, The University of Rhode Island, who said my ‘hypotheses were feasible and the research needed on so many levels’, and Professor Patrick Hesp, Flinders University, South Australia, whose opening words at my first international conference, ‘there I was alone and unloved on the dunes(!)’ really struck a chord, and gave me the courage to face the disbelievers of coastal mycology. Assistant Professor Mohsen Mesgaran, The University of California, Davis, is a true scholar and gentleman, and I am delighted he co-authored my first publication. I am indebted to Dr. Alex Idnurm at The University of Melbourne for generously allowing me to use the facilities of the Botany Mycology laboratory. I am also very thankful to Dr. Bede Mickan for his statistical wizardry. Thanks also to Chandra Jayasuriya for her cartography of my research site and its environs, and to Gerry Fahey for EndNote help. I was very fortunate to have shared my PhD journey with a fabulous cohort of talented, funny, caring, and often loud (!) RHD peers, many of whom have ‘beaten me to the bonnet’ – Dr. Ben Iaquinto, Dr. Fabio Delai, Dr. Thu Ba Huynh, and particularly Dr. Dora Carias Vega, Dr. Marcella Chaves Agudelo, and Dr. Paula Satizábal (Paulisita), whose constant positivity and warmth I continue to value so much; thanks for the laughs. In particular, Paula’s generosity of spirit has been a great source of ix encouragement during the writing-up stages of my research. The rest of us are coming up behind you and will be there soon, so thanks too, to Arturo Gonzalez-Rodriguez (Speedy), Chengjun Li (CJ), Abdullah Al Baky (Baky-Boy), and Runjie Yuan (Reggie). What an incredible mix of cultures, topics, and disciplines we all encompassed, yet we still supported and encouraged each other when things were a bit bumpy, and celebrated each other’s victories when things were smooth. I am all the richer for having shared my time with you. My research would never have occurred if not for the generosity of scholarships and bursaries I was awarded, and I am indebted to the organizations listed below, for the funds that supported me through my studies, and those that enabled me to purchase laboratory and field equipment, run field trips, and to attend conferences and seminars: – The Australian Postgraduate Award, The University of Melbourne – The Elizabeth Ann Crespin Scholarship, The University of Melbourne – The Victorian Environmental Assessment Council, Bill Borthwick Scholarship – The Dawson Bursary (awarded twice), The University of Melbourne – The Postgraduate Global Environmental Sustainability Award, The Rotary Club of Balwyn I am so very grateful for the assistance I received from Mr. Warren Chapman, Manager, Natural Resource Planning, and the team of people at the Barwon Coast Committee of Management, who allowed my research
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