Temporal Determinants of Fungal Community Assembly
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TEMPORAL DETERMINANTS OF FUNGAL COMMUNITY ASSEMBLY A DISSERTATION SUBMITTED TO THE DEPARTMENT OF BIOLOGICAL SCIENCES AND THE COMMITTEE ON GRADUATE STUDIES OF STANFORD UNIVERSITY IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY Devin R. Leopold May 2017 © 2017 by Devin Robert Leopold. All Rights Reserved. Re-distributed by Stanford University under license with the author. This work is licensed under a Creative Commons Attribution- Noncommercial 3.0 United States License. http://creativecommons.org/licenses/by-nc/3.0/us/ This dissertation is online at: http://purl.stanford.edu/kj190rg6492 ii I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Tadashi Fukami, Primary Adviser I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Erin Mordecai I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Kabir Peay I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Peter Vitousek Approved for the Stanford University Committee on Graduate Studies. Patricia J. Gumport, Vice Provost for Graduate Education This signature page was generated electronically upon submission of this dissertation in electronic format. An original signed hard copy of the signature page is on file in University Archives. iii Abstract Fungi play key roles in terrestrial ecosystems, driving many biogeochemical processes and influencing the structure of plant and animal communities as mutualists and pathogens. The fungal kingdom is also taxonomically and functionally diverse, and efforts to understand what determines fungal species composition in ecological communities are motivated by the functional consequences of fungal community assembly. Recent advances in DNA sequencing-based microbial community profiling have facilitated rapid advances in the study of fungal community ecology. However, the factors that determine the outcome of community assembly are not static through time, and factors related to the temporal scale of fungal community assembly remain poorly defined. In this dissertation I explore two temporal determinants of fungal community assembly, ecosystem age and species arrival order. First, I explore the effect of ecosystem age using an observational study of the fungi associated with the roots of an ericaceous plant, Vaccinium calycinum, across a 4.1 myr soil chronosequence in Hawaii. I show that soil development promotes greater diversity in ericaceous root-associated fungal communities and that soil-age related nutrient limitation facilitates colonization of ericaceous roots by a greater diversity of non- mycorrhizal fungi in both young and old soils. Second, I use a laboratory microcosm study of V. calycinum root-associated fungi to show that fungal species pools from older ecosystems include species that are more likely to coexist within the roots of a single seedling. Finally, I use a community of wood-decomposing fungi in a microcosm experiment to show that the interactive effects of top-down (grazing) and bottom-up (nutrient availability) forces determine the importance of immigration history (i.e., priority effects) for community composition and function. Taken together these results demonstrate that temporal processes occurring at both short and long time scales can be important determinants of fungal community assembly. iv Acknowledgments I would like to thank Tadashi Fukami for encouraging me to pursue a PhD at Stanford and for being an outstanding advisor and friend throughout the process. My committee members, Erin Mordecai, Kabir Peay, and Peter Vitousek, have each provided important feedback and assistance at various points along the way. Kabir, in particular, has contributed a significant amount of his time and resources, for which I am grateful. The entire Fukami Lab and Stanford community has always made me feel welcomed, despite my infrequent trips to campus. Specifically, Holly Moeller, Matt Knope, Marie-Pierre Gauthier, and Rachel Vannette all helped me grow as a scientist and became good friends along the way. This work was supported by research grants from the National Science Foundation, The American Society of Naturalists, and the Mycological Society of America. Laboratory space and other resources were generously provided Michael Shintaku and Anne Veillet, at the University of Hawaii, Hilo, Scott Gibb, at the USDA-ARS, Pacific Basin Agricultural Research Center, and Christian Giardina, at the USFS, Institute of Pacific Islands Forestry. Finally, and most importantly, I have to thank my family for their support and encouragement. Christina Leopold has supported me in countless ways and her confidence in my success has often been greater than my own. Her contribution to this dissertation is immeasurable. My son, Nico Leopold, who was born during the second year of my PhD, has provided much needed distraction from my work, as well as renewed motivation for success. Lastly, I am fortunate to have parents, Karen and Robert Leopold, who have always encouraged me to pursue my interests freely and worked hard to set me up for success in life. v Table of contents Chapter 1: General introduction and author contributions............................................1 General Introduction...........................................................................................2 Author contributions...........................................................................................6 References...........................................................................................................7 Chapter 2: Ericoid fungal diversity: challenges and opportunities for mycorrhizal research...........................................................................................................................9 Abstract.............................................................................................................10 Introduction.......................................................................................................11 Diversity of ericoid mycorrhizal fungi..............................................................14 Biogeography of ericoid mycorrhizal fungi......................................................19 Research opportunities for ericoid mycorrhizal systems..................................24 Conclusions.......................................................................................................28 Acknowledgments.............................................................................................29 References cited................................................................................................30 Figures...............................................................................................................42 Chapter 3: Diversity of Vaccinium calycinum (Ericaceae) root-associated fungi increases throughout long-term ecosystem development.............................................44 Abstract.............................................................................................................45 Introduction.......................................................................................................46 Materials and methods......................................................................................49 Results...............................................................................................................55 Discussion.........................................................................................................57 Acknowledgments.............................................................................................61 References cited................................................................................................62 Tables................................................................................................................69 Figures...............................................................................................................70 Supplemental materials.....................................................................................76 Chapter 4: Local richness increases more with regional richness under older species pools: evidence from root-associated fungi..................................................................77 Abstract.............................................................................................................78 Introduction.......................................................................................................79 Material and methods........................................................................................81 Results...............................................................................................................91 Discussion.........................................................................................................92 References cited................................................................................................95 Tables..............................................................................................................102 Figures.............................................................................................................103