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Fungal Communities of Beech (Fagus Sylvatica) Trees: Heart Rot and Origins of Decay

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Fungal communities of beech (Fagus sylvatica) trees: Heart rot and origins of decay A thesis submitted to Cardiff University for the degree of Doctor of Philosophy by Emma Christine Gilmartin 2020 DECLARATION This work has not been submitted in substance for any other degree or award at this or any other university or place of learning, nor is being submitted concurrently in candidature for any degree or other award. Signed …………………………………..…… (candidate) Date ……………………… STATEMENT 1 This thesis is being submitted in partial fulfilment of the requirements for the degree of PhD. Signed …………………………………..…… (candidate) Date ……………………… STATEMENT 2 This thesis is the result of my own independent work/investigation, except where otherwise stated, and the thesis has not been edited by a third party beyond what is permitted by Cardiff University’s Policy on the Use of Third Party Editors by Research Degree Students. Other sources are acknowledged by explicit references. The views expressed are my own. Signed …………………………………..…… (candidate) Date ……………………… STATEMENT 3 I hereby give consent for my thesis, if accepted, to be available online in the University’s Open Access repository and for inter-library loan, and for the title and summary to be made available to outside organisations. Signed …………………………………..…… (candidate) Date ……………………… STATEMENT 4: PREVIOUSLY APPROVED BAR ON ACCESS I hereby give consent for my thesis, if accepted, to be available online in the University’s Open Access repository and for inter-library loans after expiry of a bar on access previously approved by the Academic Standards & Quality Committee. Signed …………………………………..…… (candidate) Date ……………………… Dedication To Andrew, who passed away in October 2015. A passionate conservationist, who won the category ‘Most Beautiful’ for his collection of an orange peel fungus (Aleuria aurantia) during our first fungal foray together at Moelyci, Gwynedd in 2012. ii Acknowledgements This project was funded by Cardiff University, Natural England, The Crown Estate and City of London. It has also been significantly supported by Fund4Trees. I owe sincere thanks to many: Firstly, to my supervisors. Lynne Boddy for being a science and life maverick, and for the many road trips. Hefin Jones, for being a force for order with great patience. Ted Green, for being my first friend made under a tree. Jen Hiscox and Mel Savoury, for listening and for the oversharing. For so much help and encouragement through numerous difficult moments. Ian Chedgy and Ed Pyne, for reminding me to that trees have dignity. Ian, for being my champion and mentor. Ed for being generally super, a dependable work partner, poor pot-washer and fire-starter. I am grateful to you both for your enthusiasm and support in coring, climbing and drilling trees for Chapters 2 and 3. The fungal ecology group in all its iterations and all who I've encountered in labs, our coffee room and office. Yu Fukasawa for being inspiringly inquisitive. Mike Reynolds and Willow Smallbone, for lovely lunches and for being examples of efficiency that, unfortunately, I would never match. Thanks to Jordan Cuff for always spicing up my life, Ifan Jâms for the charm and Fredric Windsor for the banter. Jeremy Dagley and City of London staff for all assistance at Epping Forest. To all others who have provided assistance to me in the field and granted permission to work at various locations. Mick Boddy for helping me with an increment borer and Nobby Clarke for teaching me to use a chainsaw. Michelle Jusino, Mark Banik, Dan Lindner and the US Forest Service, for hosting me for a fun and productive stay in Madison. Without your support and collaboration the work in Chapter 4 would not have been possible. Finally, Wyn – my rock – who has kept me going through the very worst, and without whom I could not be writing this now. iii Summary Heart rot and hollowing of tree trunks is an ecologically important phenomenon and is the result of fungal decay of wood. Despite the value of heart rot habitats to thousands of species, globally, little is known about the development of the fungal communities which give rise to them. This thesis explores these aspects in beech (Fagus sylvatica) trees. Destructive and non-destructive methods were used to survey for wood decay fungi in beech trunks. The predominant species identified depended on the survey method employed. In mature trees with no external indicators of heartwood decay, overall incidence of decay was 45%, and a species of Pholiota in the adiposa- aurivella complex was detected most frequently. In recently fallen and felled beech trunks, however, the ascomycete Kretzschmaria deusta appeared most frequently, and was the likely contributor to tree windthrow in most of these cases. Examination of the spatial aspects of fungal communities in trunks permitted observations relating to heartwood patterning and the categorisation of species as principally causing butt or top-rots, and as cavity formers. Metabarcoding of the universal fungal barcode (ITS), and a second barcode (LSU), revealed the distribution and diversity of endophytes, or latent fungi, in functional sapwood of standing trunks. Together, the metabarcoding approach detected a higher diversity of taxa than did isolation of fungi from wood dust samples. Fungal community composition varied between trees at different sampling sites. Overall, several heart rot fungi were detected throughout functional sapwood of trunks, providing evidence that heart rot can, in principle, develop from latent propagules. Interactions between heart rot species other beech decay fungi were compared in wood block pairings and on agar media. Species rankings based on scored outcomes revealed different relative combative ability depending on the medium on which the interactions took place. Of the species examined, Hypholoma fasciculare and Fomitopsis pinicola were the most combative, whilst other heart rot fungi showed no clear trend towards high or low combativeness. Competitive interactions alone were, thus, not sufficient to explain fungal community development in beech trunks. iv Table of Contents Dedication.................................................................................................................ii Acknowledgements .................................................................................................. iii Summary ................................................................................................................. iv Table of Contents .................................................................................................... v List of Tables and Figures ...................................................................................... viii Chapter 1 1.1. Background ............................................................................................. 10 1.2. Heart rot .................................................................................................. 11 1.2.1. Wood structure and heartwood formation ......................................... 11 1.2.2. Constraints on decay development ................................................... 13 1.2.3. Ecology of heart rot fungi .................................................................. 13 1.2.4. Development of heart rot .................................................................. 16 1.3. Heart rot habitats and their importance .................................................... 16 1.3.1. Hollows and cavities ........................................................................ 16 1.3.2. Diversity and specificity in heart rot habitats ..................................... 19 1.4. Fungal communities of beech trees: Heart rot and origins of decay ............ 19 Research rationale ........................................................................... 19 Thesis outline ................................................................................... 20 Chapter 2 2.1. Summary ................................................................................................. 22 2.2. Introduction .............................................................................................. 22 2.3. Methods................................................................................................... 24 2.3.1. Sampling and study design ............................................................... 24 2.3.2. Sample Collection ............................................................................. 25 2.3.3. Core processing ............................................................................... 26 2.3.4. Species identification ........................................................................ 26 2.3.5. Estimation of tree age ....................................................................... 27 2.3.6. Statistical analysis ............................................................................ 28 2.4. Results .................................................................................................... 28 2.4.1. Cores summary and tree age ........................................................... 28 2.4.2. Fungal isolates ................................................................................. 29 2.4.3. Trees with heart rot ........................................................................... 30 2.5. Discussion ............................................................................................... 35 2.5.1. Heart rot fungi were identifiable from tree core samples ..................
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