Spatial and Temporal Aspects of Macrofungal Community Structure
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Spatial and Temporal Aspects of Macrofungal Community Structure Aqilah Mohammad School of Biological Sciences Royal Holloway, University of London Egham, Surrey, TW20 0EX United Kingdom A thesis submitted to the University of London in partial fulfilment of the requirements for the degree of Doctor of Philosophy London, May 2013 Declaration of Authorship These doctoral studies were conducted under the supervision of Prof. Alan C. Gange. The work presented in this thesis is the result of original research carried out by myself, whilst enrolled in the School of Biological Sciences as a candidate for the degree of Doctor of Philosophy. This work was conducted independently and has not been submitted for any other degree of award in any other university or educational establishment. Where I have consulted the work of others, this is always clearly stated. Aqilah Mohammad May 2013 2 Acknowledgement First of all, I thank Allah SWT for His blessings and opportunity for me to complete my PhD thesis. I would also like to thank my sponsor, Malaysia Ministry of Higher Education (MOHE) and my employer, Universiti Malaysia Terengganu (UMT) for giving me the opportunity to advance in my career and my research. My special thank goes to my supervisor, Prof. Alan Gange, who has shown me constant support, motivation and patience throughout my study. Thank you for giving me an aspiration and showing me passion. I would also like to thank my advisor, Prof. Julia Koricheva for her constructive comments and suggestions towards my thesis contents. I am grateful to two big names in the British mycology, Prof. Lynne Boddy (Cardiff University) and Ted Green (Crown Estates, Windsor Great Park) for their help in research and permission to work in one of the beautiful historic forests in the UK. I would also like to thank people in my lab especially Neil Sommerville (lab technician) and my lab mates at RHUL for their support throughout my PhD. Many thanks also to Thanos Damialis (University of Ioannina, Greece) for the collaboration project and helping me out with statistics. I would not have contemplated this road if not for my parents, Mohammad and Zahida, and my siblings who never failed to give encouragements and support even though they are thousands of miles away. This thesis would also not be possible without the love and support from Mr. Husband. Dear Aidy Shahril, thank you for being the ideal husband throughout. Thank you for the cuddles every time I got depressed, for company during my field sampling and for every calming word during my difficult times. 3 Abstract The thesis contains an analysis of spatial and temporal aspects of macrofungal fruiting. In total, the thesis contains 8 chapters with 5 experimental chapters. These chapters involved studies of i) fungal phenology (Chapter 3), ii) fungal-host associations (Chapter 4), iii) the relationship between fungi and climatic variables (Chapter 5), iv) seasonal dynamics of fungal interactions (Chapter 6) and v) fungal species co- occurrence patterns (Chapter 7). Most data, analysed in the studies of phenology, host associations and influences of climate on fungi were obtained from a long term fungal dataset with records gathered by local mycologist, Edward G. Gange from more than 1000 localities within a 30 km radius of Salisbury, Wiltshire, UK over 50 years. Chapter 3 describes analyses that I have conducted in order to detect changes in fruiting phenology of ten common fungal functional groups extracted from the dataset. Meanwhile, in Chapter 4, host ranged of 8 common fungal genera were explored and responses of mycorrhizas and saprotrophic fungi were compared. Moreover, the question of whether changes in fungal fruiting patterns in the UK could be affected by climatic factors over recording period are discussed in Chapter 5. For spatial aspects of fungal community structure, field studies have been conducted in Chapter 6 and Chapter 7 of the thesis where samples were obtained from study sites in Windsor Forest (Windsor Great Park), Royal Holloway College (Egham, Surrey) and Wivelsfield (West Sussex). Chapter 6 describes experiments on a model species, Hypholoma fasciculare to examine whether fruit bodies that fruit in the same place have fruit more than once a year. Chapter 7 contains explanations of an attempt to answer the question whether some individuals have gaps/off-year during their fruiting seasons while there are other individuals belonging to the same species that occur elsewhere. This then followed by identifying factors that could triggers the fruit body formation. 4 Table of contents 1 Title page Declaration 2 Acknowledgements 3 4 Abstract 5 Table of contents 9 List of tables 10 List of figures 16 List of abbreviations 17 Chapter 1 General Introduction 24 Chapter 2 Dataset properties Chapter 3 Changes in fungal fruiting phenology in a 58 year old historical data set in England 3.1 Introduction 27 3.1.1 Understanding the fungal fruiting phenology 28 3.1.2 Factors that contribute to the production of fruit bodies 3.1.3 The use of historical data in order to determine fungal fruiting patterns on a 29 long-term basis 3.2 Methods and analysis 3.2.1 Data collection 30 30 3.2.3 Analyses 3.3 Results 3.3.1 Changes of first fruiting date, last fruiting date, length of fruiting and average 31 of fruiting of each ecological groups 31 3.3.2 Frequency of species vs. regression coefficient of first fruiting date 3.3.3 Frequency of species vs. regression coefficient of last fruiting date 33 3.3.4 Frequency of species vs. regression coefficient of RANGE 33 36 3.3.5 Frequency of species vs. regression coefficient of MEAN 5 3.3.6 Relationship between regression coefficient of first fruiting date versus year and overall mean fruiting date 36 3.3.7 Relationship between regression coefficient of last fruiting date and mean fruiting date 36 3.3.8 Relationship between regression coefficients of length of fruiting (RANGE) and mean fruiting date (MFD) 40 3.3.9 Relationship between regression coefficients of average of fruiting (MEAN) and mean fruiting date (MFD) 40 3.3.10 Responses of genera that fruit at similar times 3.3.10.1 Mycorrhizal genera i) Genus Amanita 44 ii) Genus Inocybe 45 iii) Genus Lactarius 46 iv) Genus Russula 47 3.3.10.2 Non-mycorrhizal genera (Saprotrophic genera) i) Genus Clitocybe 50 ii) Genus Collybia 50 iii) Genus Mycena 51 3.4 Discussion 3.4.1 Changes in fungal phenology 55 3.4.2 Responses of genera that fruit at similar times 59 Chapter 4 Do species expand and/or shift their hosts? 4.1 Introduction 4.1.1 Associations between fungi and its host 62 4.1.2 Host specificity and host selectivity 63 4.1.3 Previous study 64 4.2 Methodology 64 4.3 Results 4.3.1 Cumulative number of hosts 4.3.1.1 Mycorrhizal genera 66 4.3.1.2 Saprotrophic genera 73 4.3.2 Host expansion and/or host shift 4.3.2.1 Mycorrhizal genera 78 6 4.3.2.2 Saprotrophic genera 89 4.4 Discussion 98 4.5 Host shift in fungi caused by climate change? 4.5.1 Introduction 106 4.5.2 Methods and analysis 107 4.5.3 Results 108 4.5.4 Discussion 116 Chapter 5 Climate effects on fungal fruiting patterns in the UK 121 5.1 Introduction 5.2 Methodology 5.2.1 Fungal phenology data 123 5.2.2 Weather data 123 5.2.3 Statistical analysis 124 5.3 Results 5.3.1 Temporal patterns of meteorological data 125 5.3.2 Relationship between climatic factors and fungal fruiting patterns 128 5.3.3 Lag-effect discovery 133 5.4 Discussion 135 Chapter 6 Do Hypholoma fasciculare individuals fruit more than once a year? 6.1 Introduction 140 6.2 Methodology 6.2.1 Fungal isolates 142 6.2.2 Fungal interactions in co-culture 143 6.3 Results 144 6.4 Discussion 151 Chapter 7 Co-occurrence patterns of macrofungal species in Windsor Forest / Do mushrooms occur at the same place every year? 7.1 Introduction 155 7.2 Methodology 7.2.1 Study sites 158 7.3 Results 159 7 7.4 Discussion 166 Chapter 8 General discussion 171 Appendices 179 References 189 8 List of tables Table 4.1 The cumulative numbers of hosts where species were found over 58 67 years of study. Table 4.2 Summary of the number of species that grouped into two different 78 functional groups, mycorrhiza and saprotrophs based on their pattern of accumulation curves. Table 4.3 Response of mycorrhizal species regarding host shift. 88 Table 4.4 Summary of responses of mycorrhizal genera in the study. 88 Table 4.5 Response of saprotrophic species showing host shifts. 97 Table 4.6 Summary of responses of saprotrophic genera in the study. 98 Table 4.7 Hosts of A. auricula-judae 112 Table 4.8 Fungi found on Sambucus nigra 113 Table 5.1 (One-way) linear regression results of phonological variables of 353 129 autumnal fungal species against cumulative annual minimum and maximum air temperature for 10 functional groups. Table 5.2 One-way linear regression results of phonological variables against time 130 for genera. Table 5.3 Cross-correlations of fruiting season variables of 10 functional groups of 133 fungi with lagged minimum temperature time-series. Table 6.1 Summary of the H. fasciculare interactions in three study sites. 150 9 Table 7.1 Macrofungal species found in Windsor Forest between 2010 and 2012. 161 Table 7.2 Common species occurring in the study sites during study period. 161 List of figures Figure 2.1 Map of the study area ranging from New Forest National Park to 25 Salisbury.