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The Chemical Mediation of Multi-Trophic Interactions: Testing

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The Chemical Mediation of Multi-Trophic Interactions: Testing THE CHEMICAL MEDIATION OF MULTI-TROPHIC INTERACTIONS: TESTING COMPONENTS OF THE TRI-TROPHIC INTERACTIONS HYPOTHESIS by CAITLIN ANNE KELLY B.S. Lafayette College, 2007 M.S. Villanova University, 2009 A thesis submitted to the Faculty of the Graduate School of the University of Colorado in partial fulfillment of the requirement for the degree of Doctor of Philosophy Department of Ecology and Evolutionary Biology 2016 This thesis for the Doctor of Philosophy degree by Caitlin Anne Kelly has been approved for the department of Ecology and Evolutionary Biology by ___________________________________ M. Deane Bowers ___________________________________ Michael Breed ___________________________________ Rebecca Safran ___________________________________ Timothy Seastedt ___________________________________ Shannon Murphy The final copy of this thesis has been examined by the signatories, and we find that both the content and the form meet acceptable presentation standards of scholarly work in the abovementioned discipline. iii Kelly, Caitlin (Ph.D., Ecology and Evolutionary Biology) The chemical mediation of multi-trophic interactions: Testing components of the tri-trophic interactions hypothesis Thesis directed by Professor M. Deane Bowers ABSTRACT Although there are multiple hypotheses regarding the top-down and bottom-up controls of herbivore populations, the Tri-Trophic Interactions (TTI) Hypothesis is the first to make predictions regarding the simultaneous effects of plant quality, herbivore diet breadth, and natural enemies on herbivore performance. My dissertation research tests several predictions of the TTI hypothesis to determine how plant secondary metabolites, herbivore diet breadth (specialist or generalist) and natural enemies interactively determine the performance of insect herbivores. I study plants in the genus Penstemon (Plantaginaceae), which are chemically defended by bitter iridoid glycosides (IGs), and their associated lepidopteran herbivores. First, I examined the bi-trophic interactions between two different Penstemon species and generalist and specialist lepidopterans. The fitness of the generalist species varied greatly between the two plants, whereas the specialist performed consistently well on both host plant species. Second, I determined the level of variation in Penstemon IGs to which herbivores are naturally exposed. I focused on three potential sources of variation: inter-annual (across years), location (among geographically distinct populations) and plant tissue type. Finally, I examined the role of IGs in tri-trophic interactions by examining the ability of IGs to protect a specialist caterpillar from predators and parasitoids. Ant bioassays indicated that even low amounts of IGs are effect deterrents against invertebrate predators. However, measurements of phenoloxidase activity, an iv important component of the insect immune response cascade, suggested that caterpillars reared on certain diets were more vulnerable to parasitoid attack. This research provides important contributions to the recently proposed TTI hypothesis and increases our understanding of the chemical mediation of multi-trophic interactions. v ACKNOWLEDGEMENTS First and foremost, I would like to thank my committee members who have supported me these last several years. I would especially like to recognize my advisor, Deane Bowers, who never gave up on me, even when I wanted to give up on myself. Michael Breed was my mentor first and my cheerleader second. I am grateful to have been a part of the Animal Behavior team, but more importantly, I am grateful for his unwavering faith in me, which saw me through the toughest of times. I would also like to acknowledge my other committee members, Becca Safran, Tim Seastedt and Shannon Murphy, for all of their time, insight and assistance. I owe many thanks to several other CU faculty members, EBIO staff, students, and colleagues who have supported me in many different, and often unexpected, ways. My research would not have been possible without my many, fantastic undergraduate assistants: Lauren Bradley, Hadley Hanson, Jason Hong, Quinn Langsfeld and many others. I am also grateful for the Colorado Parks and Wildlife for allowing me to use Crescent Meadows as my main field site for six consecutive summers. I greatly appreciate the support provided by the Department of Ecology and Evolutionary Biology in the form of fellowships and teaching assistant ships. Funding for research presented in this thesis was provided by the Boulder County Nature Association, John W. Marr Fund in Plant Ecology, the Department of Ecology and Evolutionary Biology at CU, the Hazel Schmoll Research Fellowship in Colorado Botany, the William H. Burt award provided through the University of Colorado Museum of Natural History, and the National Science Foundation. Finally, I would like to acknowledge my family and friends, for never doubting me and providing endless emotional support. I especially thank Zach, for his statistical wisdom and our loving relationship, and my besties, for being the highlight this journey. vi TABLE OF CONTENTS CHAPTER 1. INTRODUCTION 1.1 Research Rationale and Goals .......................................................................................1 1.2 Plant Secondary Metabolites and Herbivore Preference and Performance ...................2 1.3 Plant Secondary Metabolites and Herbivore-Natural Enemy Interactions ....................4 1.4 The Tri-Trophic Interactions Hypothesis .......................................................................6 1.5 Study System Penstemon glaber .....................................................................................................8 Penstemon virgatus ..................................................................................................9 Euphydryas anicia .................................................................................................10 1.6 Research Overview ......................................................................................................10 CHAPTER 2. PREFERENCE AND PERFORMANCE OF GENERALIST AND SPECIALIST HERBIVORES ON CHEMICALLY DEFENDED HOST ABSTRACT .......................................................................................................................13 INTRODUCTION .............................................................................................................14 METHODS ........................................................................................................................18 RESULTS ..........................................................................................................................24 DISCUSSION ....................................................................................................................30 CHAPTER 3. THE UNPREDICTABLE PENSTEMON: VARIATION IN DEFENSIVE CHEMISTRY ACROSS YEARS, POPULATIONS, AND TISSUES ABSTRACT .......................................................................................................................34 INTRODUCTION .............................................................................................................34 METHODS ........................................................................................................................38 RESULTS ..........................................................................................................................41 DISCUSSION ....................................................................................................................48 CHAPTER 4. HOST PLANT IRIDOID GLYCOSIDES MEDIATE HERBIVORE INTERACTIONS WITH NATURAL ENEMIES ABSTRACT .......................................................................................................................52 INTRODUCTION .............................................................................................................53 METHODS ........................................................................................................................56 RESULTS ..........................................................................................................................62 DISCUSSION ....................................................................................................................68 vii CHAPTER 5. CONCLUSIONS 5.1 Principle Findings ........................................................................................................73 5.2 Hypotheses in Multi-Trophic Interactions ..................................................................76 5.3 Tests of the TTI Hypothesis .........................................................................................79 5.4 Synthesis ......................................................................................................................82 5.5 Future Directions and Closing Remarks ......................................................................83 LITERATURE CITED ...............................................................................................................86 viii LIST OF TABLES Table 3.1 The six Penstemon virgatus sampling populations in Colorado, USA. ........................43 Table 3.2 Summary of three-way, repeated measures ANOVAs that tested the effects of tissue type, population and year and their interactions on the iridoid glycoside content of Penstemon virgatus. The iridoid glycosides catalpol and scutellarioside were measured as a concentration (% dry weight). ..............................................................................................................................44
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