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Thesis Template Impacts of aboveground and belowground interactions on the performance of an invasive thistle, Cirsium arvense by Krystal Anne Maria Nunes A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Department of Ecology and Evolutionary Biology University of Toronto © Copyright by Krystal A Nunes 2018 Impacts of aboveground and belowground interactions on the performance of an invasive thistle, Cirsium arvense Krystal Anne Maria Nunes Doctor of Philosophy Department of Ecology and Evolutionary Biology University of Toronto 2018 Abstract Interactions with natural enemies are important to the success of invasive plants in their invaded range. However, little is known of the relative impacts of above- and belowground interactions, or how these interactions may change across the invaded range or between growing seasons. My research investigated these questions using Asteraceae occurring in Ontario, Canada. First, I quantified aboveground herbivory for exotic and native Asteraceae across a latitudinal gradient with the expectation that marginal or more northern populations would experience reduced enemy pressure. Herbivory did not always decline with increasing latitude, but often depended upon the causal herbivorous organism(s) or whether the species was native or exotic. I then further investigated a single non-native species exhibiting strong latitudinal trends in herbivory, Canada thistle (Cirsium arvense). I manipulated distance between plots of C. arvense to see if local spatial and/or temporal isolation also allowed escape from aboveground enemy pressure. Herbivory patterns changed significantly over 4 years, with initial patterns of reduced damage with isolation disappearing by the final year. However, variation in aboveground damage did not explain performance. I then investigated the effects of belowground interactions using a soil feedback experiment with soil collected from across the invaded range, and found C. arvense performed best in range edge soils with shorter invasion histories. This was reflected in ii compositional shifts in soil mesofauna, and most strikingly, the soil microbiota. Finally, to determine the relative importance of these interactions, I created replicate common gardens in which C. arvense was treated with above- and/or belowground exclosures. Regardless of garden location within the invaded range, protection from both aboveground and belowground enemies improved performance, but belowground interactions tended to have a greater negative impact. Together these results emphasize the importance of spatial and temporal scale in studies of invasions, as well as the need to consider both aboveground and belowground interactions when describing invader performance. iii Acknowledgments After 5 years in the PhD program at the University of Toronto Mississauga, one of the most important things I have learned is that this cannot be done alone. I was fortunate enough to have an incredibly supportive and encouraging network of friends, family, and peers to get me to the finish line. First and foremost, I would like to thank my supervisor Dr. Peter Kotanen. Thank you for having faith in my abilities to complete this degree, and for dedicating your time and effort to help me grow as a researcher, learner, and naturalist. Thank you for your patience and positivity throughout this process, and for being my own personal Sibley guide at all times – I could not have asked for anything more. Thank you to my committee members, Dr. Marc Johnson and Dr. Benjamin Gilbert. Your guidance and advice was immeasurably helpful, and your mark has been left on this thesis as well. I would like to thank my co-author, former roommate, and friend Connor Fitzpatrick. We began our graduate school adventure together, and I could not have finished my own journey without your help. Thank you for always being there to talk about the good and the bad (namely R code). I would like to thank Colin Cassin and Jason Verbeek for being the greatest lab mates I could have hoped for. Colin – thank you for the countless hours we spent on the road together, for the immeasurably helpful conversations about our research, and for introducing me to The Vinyl Café. Jason – thank you for being an endless source of entertainment both inside and outside the lab, and (especially) during TA hours. Thank you to Felipe Torres and Julian Bermudez for adventuring with me every weekend. Thank you to Aaron LeBlanc and Nash Turley for helping me photograph my invertebrates, but more importantly for maintaining our friendship across thousands of kilometres. I also thank the graduate students in my department whose friendship and encouragement were incredibly appreciated: Amy Wong, Chris Wong, Mark MacDougall, Audrey Reid, Dachin Frances, and Sarah French, to name a few. iv Thank you to the army of undergrads who have helped me with my experiments over the years. If it wasn’t for your dedication, I would still be washing roots to this day. A special thank you goes to Ariana Longley for refusing to leave our lab for years (I promise this is a compliment), and to Jack Hu, Anna Mikhailitchenko, Leigh-Anne Goodine, and Neil Oliveira. I would like to thank my parents, Al and Lorna Nunes, for raising a bookworm who refused to leave school until the tender age of 27. Thank you Dad for helping me dig holes, and for keeping me hydrated during those hot days of field work with lemon water that was more lemon than water. Thank you Mom for never remembering the name of my degree, but bragging about me nonetheless. I have endless gratitude towards my best friend, confidant, and husband Joshua O’Connell. You have played an invaluable role in my completion of this thesis. Thank you for listening to my struggles and rants, and for celebrating the successes along the way. Thank you for helping me complete my field work every summer, and for driving me to and from Timmins on multiple occasions (especially during that snowstorm in May). I could not have done this without you, and this degree is as much yours as it is mine. Finally, I would like to thank Cirsium arvense for being the star of the show. I can now walk through a patch of Canada thistle without even noticing the spines piercing my skin; if this special skill doesn’t land me the dream job, I have at least gained a great party trick. v Table of Contents Acknowledgments.......................................................................................................................... iv Table of Contents ........................................................................................................................... vi List of Tables ................................................................................................................................ xii List of Figures .............................................................................................................................. xiv List of Appendices ....................................................................................................................... xxi Chapter 1 General Introduction .......................................................................................................1 Biological Invasions ....................................................................................................................1 1.1 Hypotheses of plant invasions .............................................................................................2 1.1.1 Darwin’s Conundrum...............................................................................................2 1.1.2 Evolution of Increased Competitive Ability ............................................................2 1.1.3 Enhanced Mutualist Hypothesis ..............................................................................3 1.1.4 Novel Weapons Hypothesis .....................................................................................3 1.1.5 Enemy Release Hypothesis ......................................................................................3 1.2 Latitudinal gradients in plant-herbivore interactions ...........................................................4 1.3 The role of aboveground and belowground interactions in plant performance ...................5 1.3.1 The effect of aboveground enemy interactions on invader establishment ...............7 1.3.2 The effect of belowground enemy interactions on invader establishment ..............8 1.4 Thesis overview .................................................................................................................10 1.4.1 Study site: Province of Ontario ..............................................................................10 1.4.2 Study site: Koffler Scientific Reserve ....................................................................10 1.4.3 Study system: Asteraceae ......................................................................................11 1.4.4 Focal species: Cirsium arvense (Canada thistle) ...................................................11 1.4.5 Chapter 2 Overview ...............................................................................................14 1.4.6 Chapter 3 Overview ...............................................................................................15 1.4.7 Chapter 4 Overview ...............................................................................................15 vi 1.4.8 Chapter 5 Overview ...............................................................................................16
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