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Slinn Heather 202104 Phd.Pdf Community-level consequences of Piper chemistry on tropical herbivores, parasitoids and fungi by Heather Lea Slinn A Thesis presented to The University of Guelph In partial fulfilment of requirements for the degree of Doctor of Philosophy in Integrative Biology Guelph, Ontario, Canada © Heather Lea Slinn, April, 2021 ABSTRACT COMMUNITY-LEVEL CONSEQUENCES OF PIPER CHEMISTRY ON TROPICAL HERBIVORES, PARASITOIDS, AND FUNGI Heather Lea Slinn Advisors: University of Guelph, 2020 Dr. Jonathan Newman Dr. Lee Dyer Plant chemistry is a defining feature of plants as taxa exhibit extensive chemical variation, which influences interactions with other organisms, especially insect and mammalian herbivores and fungi. Plant chemistry can act as an important ecological filter that shapes which fungi can colonize host plant tissue and which insects and mammals form associations with it. The majority of research that has been done on the consequences of plant-insect, and more generally plant-herbivore, interactions has focused on isolating the effects of one or two plant compounds. However, looking at phytochemical profiles as a whole is a better reflection of nature as plants often contain compounds that are rich in structural and functional diversity. In addition, tropical ecosystems are home to extremely diverse fungal communities, which are formed by complex ecological filters. Fungi can largely influence plant chemistry and therefore plant-insect interactions; however, only a small percentage of fungi have been characterized, and scientists understand even less about their functional roles. Here, I contribute to the research addressing these knowledge gaps using Piper, which is a pantropical plant genus with a broad spectrum of phytochemistry, and which hosts highly specialized insect and mammalian herbivores and diverse fungal communities. I start Chapter One with an introduction to the overarching concepts and theoretical framework of my three research chapters (Chapters Two-Four). In Chapter Two, I investigate how phytochemical diversity across several plant species in two tropical ecosystems vary in their effects on herbivore immune response and herbivore parasitism by parasitoids. Chapter Three begins my research into the microbial world of Piper, where I examine how heritability of plant chemistry in Piper sancti-felicis and land-use history at the site affect herbivory, herbivore immunity, and fungal endophyte communities. Chapter Four establishes the consequences of bat digestion on the seed fungal communities of P. sancti-felicis and identifies anti-fungal properties in the fruit. I conclude with a summary and overall integration of the themes and findings of my research chapters in Chapter Five. In conclusion, I show how plant chemistry in neotropical Piper is an important determinant of species interactions and community assembly across two different kingdoms of organisms. iv ACKNOWLEDGEMENTS There are many people over the course of my degree that have assisted with my research and development as a scientist. First, I’d like to acknowledge my colleague and good friend, Bernal Matarrita-Carranza, who is a phenomenal scientist and taught me many microbial techniques while I was at La Selva Biological Station. I hope we can continue to work together in the future. Thanks to Greg Crutsinger, Kerri Crawford, Mariano Rodriguez-Cabal and Matt Barbour who got me started in science. I wouldn’t be here if it weren’t for the time and energy that you put into my development. To the UNR folks: Thanks to my former advisors Angela Smilanich and Matt Forister, and my committee member Paul Hurtado for your support and investment in me while I was at UNR. I hope I was a beneficial addition to the plant-insect group. Special thanks to my friends and colleagues that in some ways acted as unofficial advisors: Josh Harrison, Josh Jahner and Zach Marion. Sorry I never achieved becoming an asshole. I’d like to thank my La Selva friends for making my Costa Rica research trips extra memorable: Jan Bechler, Leith Miller, Paul Fellmann, Elodie Moureau, Orlando Vargas Ramirez, Laura Bizzarri, Nada Nikolic, Ping and Diego (and family). I miss our time together and I hope to see you on the other side of the pandemic. Many thanks go to the numerous funders of my research over the last five years, including: NSERC, Sonoma County Mycological Association, Mycological Association of America and to UoG and UNR. I would not be writing this document if it weren’t for your financial investment. To my advisors: Lee, thanks for staying with me as I transitioned back to Canada and for putting up with my incessant Canadian jokes and (hockey) trash talk; Jonathan, v thanks for taking me in mid-degree without knowing me. I hope I was a valuable addition to the lab. Thanks also to my committee member Posy Busby who stayed with me across this transition. And to Sally Adamowicz for joining my advisory committee in Guelph and for providing valuable advice in your fields of barcoding and bioinformatics. Lastly, I’d like to thank my partner Chris for his love and support, especially as I trekked around Latin America looking at plants, insects and fungi for months at a time. vi 1 Table of Contents Abstract ................................................................................................................................ ii Acknowledgements .............................................................................................................. iv List of Tables ........................................................................................................................ xi List of Figures ..................................................................................................................... xiv List of Appendices ............................................................................................................. xviii Chapter Publications .......................................................................................................... xxii 1 General Introduction ...................................................................................................... 1 1.0 Overview ...........................................................................................................................1 1.1 Tropical Ecosystem Significance ..........................................................................................2 1.2 Species’ Functional Roles and Interaction Diversity are Central to Communities ..................3 1.3 Community Assembly and Ecological Filtering of Microbial Communities ............................6 1.4 Objectives..........................................................................................................................8 1.5 Study Sites .........................................................................................................................9 2 Across Multiple Species, Phytochemical Diversity and Herbivore Diet Breadth Have Cascading Effects on Herbivore Immunity and Parasitism in a Tropical Model System ........... 10 2.1 Abstract ........................................................................................................................... 10 2.2 Introduction .................................................................................................................... 11 vii 2.3 Methods .......................................................................................................................... 15 2.3.1 Piper–Eois, Piper–Quadrus System ...................................................................................................... 15 2.3.2 Long-term Rearing Databases .............................................................................................................. 16 2.3.3 Immune Assay ...................................................................................................................................... 17 2.3.4 Statistical Analyses ............................................................................................................................... 18 2.4 Results............................................................................................................................. 19 2.5 Discussion ........................................................................................................................ 22 2.6 Tables .............................................................................................................................. 27 2.7 Figures ............................................................................................................................. 32 3 Intraspecific variation in plant chemistry and land-use history in a common garden experiment act as an ecological filter to insect herbivory and fungal endophyte communities 35 3.1 Abstract ........................................................................................................................... 35 3.2 Introduction .................................................................................................................... 36 3.2.1 Causes of Phytochemical Variation ...................................................................................................... 36 3.2.2 Consequences of Phytochemical Variation.......................................................................................... 37 3.2.3 Objectives ............................................................................................................................................
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