UC Riverside Electronic Theses and Dissertations
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UC Riverside UC Riverside Electronic Theses and Dissertations Title Above- and Below-Ground Consequences of Woody Plant Range Expansion in Alpine Ecosystems Permalink https://escholarship.org/uc/item/1644v6c0 Author Collins, Courtney Grace Publication Date 2019 Peer reviewed|Thesis/dissertation eScholarship.org Powered by the California Digital Library University of California UNIVERSITY OF CALIFORNIA RIVERSIDE Above- and Below-Ground Consequences of Woody Plant Range Expansion in Alpine Ecosystems A Dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Plant Biology by Courtney Grace Collins September 2019 Dissertation Committee: Dr. Jeffrey Diez, Chairperson Dr. Emma Aronson Dr. Jason Stajich Dr. Marko Spasojevic Copyright by Courtney Grace Collins 2019 The Dissertation of Courtney Grace Collins is approved: Committee Chairperson University of California, Riverside Acknowledgements I would like to thank my dissertation advisor and mentor, Dr. Jeffrey Diez for his unwavering support, valuable advice, encouragement and trust in my abilities. Thank you for challenging me to think bigger and shoot higher than I thought I could, for giving me the space and autonomy to follow my research interests, even when they were outside of your own, and for always being available when I needed help. I also thank the members of my dissertation committee, Dr. Emma Aronson, Dr. Jason Stajich, and Dr. Marko Spasojevic, who have all provided invaluable feedback, guidance, and research collaboration over my 5 years at UCR. I thank my graduate academic advisors Dr. Linda Walling, Dr. Norm Ellstrand, and Dr. Amy Litt as well as Laura McGeehan for their time and resources which were critical to my success. I thank past and present graduate student friends and colleagues at UCR including: Dr. Michala Phillips, Teresa Bohner, Sören Weber, Peter Ibsen, Hannah Shulman, Dr. Amanda Swanson, Dr. Justin Valliere, and Dr. Jennifer Eberwein for their help and feedback with research as well as their tremendous friendship and emotional support. I thank Michele Slaton, Dylan Neubauer and members of the CNPS Bristlecone chapter for their helpful botanical knowledge of White Mountain flora and their broad support and enthusiasm for my work. This research would not have been possible without the help of several undergraduate and postdoctoral researchers including Dr. Mia Maltz, Christopher Karunos, Sunny Saroa, Amulya Kunduru, Chloe Hull, Maximilien Osborne-Thacker, Amy Hsu, Andrew Tran and Alexandra Johnson. Finally, I am forever grateful to my family for their unconditional love and support and for always encouraging me to follow my passions in life. iv The text of this dissertation (Chapters 1 and 2), in part or in full, are a reprint of the material as it appears in: “Direct and indirect effects of native range expansion on soil microbial community structure and function” Journal of Ecology 2016 and “Shrub range expansion alters diversity and distribution of soil fungal communities across an alpine elevation gradient” Molecular Ecology 2018. The co-author (Jeffrey M. Diez) listed in these publications directed and supervised the research which forms the basis for this dissertation. Other co-authors including Chelsea J. Carey, Emma L. Aronson, Christopher W. Kopp, Jason E. Stajich, Sören E. Weber, and Nuttapon Pombubpa provided technical expertise, research equipment or lab space, assistance with laboratory analyses and/or bioinformatics, assistance with statistical analyses or graphics creation and helped with manuscript preparation. Funding was provided by the University of California Riverside, Department of Botany and Plant Sciences and Department of Plant Pathology and Microbiology as well as from a White Mountain Research Center Mini grant, Mary DeDecker Botanical grant (CNPS Bristlecone Chapter), and a graduate fellowship from the University of California’s Institute for the Study of Ecological and Evolutionary Climate Impacts (ISEECI), funded by a Presidential Research Catalyst Award. Fungal ITS primers were made available through the Sloan Built Environment Program and sequencing supported by funds through United States Department of Agriculture - National Institute of Food and Agriculture Hatch project CA-R- PPA-5062-H to Jason Stajich. This work was also supported by a National Science Foundation Doctoral Dissertation Improvement Grant (DDIG) Award number 1701979 to Courtney Collins. v ABSTRACT OF THE DISSERTATION Above- and Below-Ground Consequences of Woody Plant Range Expansion in Alpine Ecosystems by Courtney Grace Collins Doctor of Philosophy, Graduate Program in Plant Biology University of California, Riverside, September 2019 Dr. Jeffrey Diez, Chairperson Global change is creating novel communities of organisms around the globe as species shift their geographic ranges to maintain favorable climate conditions. Species range shifts create novel plant species interactions and influence relationships between plants and soil organisms in the new range. One well documented range shift in both arctic and alpine biomes is of woody plants, primarily shrubs, moving upwards in elevation or latitude and establishing in traditionally herbaceous dominated ecosystems. Woody plant range expansion can have significant impacts on belowground ecosystem processes through changes in litter quality and quantity, rooting depth, and interactions with soil microbial communities. In addition, both biotic and abiotic soil conditions can limit the establishment and range expansion of woody plant species. The overarching goal of this dissertation was to understand how plant-soil interactions influence and respond to the range expansion of a sagebrush shrub in the White Mountains of California. I examined multiple belowground processes including soil microbial community structure and function, biogeochemical cycling, and soil feedbacks to other vi native plant species. I used field and greenhouse studies, plant demographic monitoring, laboratory assays, functional trait analyses, next generation sequencing and diverse statistical modeling techniques to link ecological processes from the microbial to ecosystem scale. Overall, sagebrush expansion increased bacterial diversity, soil moisture, soil organic carbon and nitrogen pools and microbial biomass, which were all associated with increased microbial activity (substrate induced respiration). Sagebrush did not strongly influence overall fungal diversity but increased the abundance of fungal groups including the saprotrophic Agaricomycete fungi, which are important wood and litter decomposers. Soil microbial communities influenced both the performance and leaf functional traits of sagebrush seedlings through changes in microbial diversity and extracellular enzyme activity, which suggested strong plant-microbial competition for soil nutrients. Finally, sagebrush influenced the demography of two co-occurring herbaceous plant species through negative plant-soil feedbacks which overwhelmed the effects of abiotic facilitation by sagebrush. Taken together the results of this dissertation provide a more complete picture of how multiple aspects of the soil environment both respond to changes in plant community composition, and feedback to influence plant performance and plant species interactions. vii Table of Contents Introduction………………………………………………………………………………..1 References…………………………………………………………………..……..7 Chapter 1: Direct and indirect effects of native range expansion on soil microbial community structure and function Abstract…………………………………………………………………..………12 Introduction…………………………………………………………………..…..13 Methods…………………………………………………………………..………18 Results…………………………………………………………………..………..30 Discussion…………………………………………………………………..……34 References…………………………………………………………………..……43 Tables and Figures……………………...…………………………………..……53 Chapter 2: Shrub range expansion alters diversity and distribution of soil fungal communities across an alpine elevation gradient Abstract…………………………………………………………………..………61 Introduction…………………………………………………………………..…..62 Methods…………………………………………………………………..………67 Results…………………………………………………………………..………..74 Discussion…………………………………………………………………..……78 References…………………………………………………………………..……92 Tables and Figures……………………...…………………………..……..……103 Chapter 3: Beyond Enemy Release: Multiple microbial mechanisms influence plant-soil feedbacks and range expansion Abstract…………………………………………………………………..……..117 Introduction…………………………………………………………………..…118 Methods…………………………………………………………………..……..123 Results…………………………………………………………………..………134 Discussion…………………………………………………………………..…..136 viii References…………………………………………………………………..…..145 Tables and Figures……………………...…………………………………..…..154 Chapter 4: Plant-soil feedbacks and facilitation influence the demography of herbaceous alpine species in response to woody plant range expansion Abstract…………………………………………………………………..……..171 Introduction……………………………………………………………………..172 Methods…………………………………………………………………..……..176 Results…………………………………………………………………..………181 Discussion…………………………………………………………………..…..183 References…………………………………………………………………..…..193 Tables and Figures……………………...…………………………………..…..200 Conclusion Synthesis and Scope………….………………………………………………….206 Future Directions ………….…………………………………………………...210 References……………………………..………………………………………..212 ix List of Tables Chapter 1 Page Table 1.1 53 Site level soil characteristics for each elevation. Values shown are mean of all samples with standard deviation in parentheses. Table S1.1 58 Parameter estimates for structural