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THE EFFECTS OF ATMOSPHERIC COMPOSITION, CLIMATE, AND HERBIVORY ON PLANT SECONDARY METABOLISM AND VOLATILE ORGANIC CARBON EMISSIONS by AMY MARIE TROWBRIDGE B.S., University of Illinois at Urbana-Champaign, 2005 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 & Evolutionary Biology 2012 This thesis entitled: The effects of atmospheric composition, climate, and herbivory on plant secondary metabolism and volatile organic carbon emissions written by Amy Marie Trowbridge has been approved for the Department of Ecology & Evolutionary Biology Russell K. Monson M. Deane Bowers Tim R. Seastedt Alan R. Townsend Dena M. Smith Date 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 above mentioned discipline. iii Trowbridge, Amy Marie (Ph.D., Ecology & Evolutionary Biology) The effects of atmospheric composition, climate, and herbivory on plant secondary metabolism and volatile organic carbon emissions Thesis directed by Professor Russell K. Monson ABSTRACT Quantifying the biosynthesis and emission of terpenes by plants is necessary to understand ecological interactions and improve global atmospheric models. Many studies have addressed the importance of individual factors influencing terpene production and release into the atmosphere, but few have investigated complex interactions between multiple variables and the resulting chemistry’s effects on interactions between organisms across multiple trophic levels. To address this gap in our knowledge, I conducted a series of experiments to examine abiotic and biotic controls over terpene synthesis and emission in Poplar x canescens and Pinus edulis, in which terpenes play prominent roles in plant physiological protection (isoprene) and defense (monoterpenes). Increases in atmospheric CO2 resulted in a smaller contribution of stored extra- chloroplastic carbon towards isoprene biosynthesis and a larger investment from recently assimilated carbon in poplar. In addition to climate change scenarios, it is also critical to understand how abiotic and biotic processes affect terpene concentrations and emissions in situ. Tiger moth herbivory increased pinyon pine monoterpene fluxes three to six fold during spring feeding, but summer drought decreased emissions while maintaining high levels of foliar concentrations. Following a release from drought stress, previously damaged pinyon pines exhibited significantly higher emission rates, potentially due to a drought delayed stimulation of induced monoterpene synthesis. I then performed a series of artificial diet experiments iv investigating how herbivore-induced monoterpenes observed in the field influences insect performance. While the synergistic effect of all monoterpenes present resulted in a trade-off between investment in immunity and growth, diets containing monoterpene levels mimicking herbivore damage encouraged further herbivory with no increase in growth but enhanced immunity to parasitoid infection. To further isolate temperature versus water status controls on monoterpene dynamics, I conducted a pinyon pine transplant experiment. Drought had little influence over the production of foliar monoterpenes, which is largely under genetic control. However, observed stomatal control over emission rates suggests that plant ecophysiology plays a much larger role in controlling monoterpene fluxes than previously thought. Together, my research provides novel insights into the underestimated contribution of ecophysiology in understanding the role of terpenes in higher trophic level interactions and coevolutionary processes. v DEDICATION For the two people who have dedicated their lives to making mine extraordinary. Thank you for always believing in me, Mom and Dad. vi ACKNOWLEDGEMENTS This work would not have been possible without the contribution, support, and insight of many wonderful people. First and foremost I’d like to thank my mentors, Russ Monson and Deane Bowers, for not only providing me with the skills to become a successful and independent scientist, but for fueling my enthusiasm and reminding me that I am smarter than I think I am. I’d like to thank my major advisor, Russ, for giving an ambitious, garrulous, goofy, mildly entertaining girl with a strong Chicago accent a chance and accepting me into his lab. Russ has taught me the importance of living in the moment, being patient, and seeing the big picture in both life and research. He has also given me opportunities to see the world and pursue my research passions, all the while pushing me to be better than I ever thought I could be. His contribution to my career and my personal growth has been invaluable, and words cannot express the amount of gratitude I have for his advice, support, and friendship. I was also extremely lucky be advised by Deane, whose chemical ecology seminar changed my research interests and professional goals, but whose endless support and encouragement has changed my life. Deane has always made me believe that my work is exciting and worth sharing with the world. She is inspiring, and her endless energy and enthusiasm for science and life has made her someone I will continue to try and emulate. I feel so lucky to have had the opportunity to be a part of her lab and to learn from her. I am so grateful for her time, invaluable advice, encouraging words, and friendship. I’d also like to thank all of my friends and colleagues at CU, without whom this would not have been possible. I would particularly like to thank Yan Linhart and Ken Keefover- Ring for providing me with invaluable advice, hours of intellectually stimulating conversation, and plenty of French wine. I’d also like to thank my wonderful committee, Tim vii Seastedt, Alan Townsend, and Dena Smith, for offering me their insights and feedback and for nurturing my curiosity and interest in plant-insect interactions. I’d also like to thank Cesar Nufio and Kasey Barton, who taught me just about everything I know about insects and I am grateful that they were the ones to introduce me to the amazing world of entomology. I could not have made it through graduate school without the many hugs, stories, and laughs I shared with my peers, especially Susan Whitehead, Mary Jamieson, Carolina Quintero, Nicole Trahan, Se Jin Song, Katie Driscoll, Joey Hubbard, Maggie Richards, Allyson Eller, Mick Wilkinson, and Marcus Cohen. Of course, this research could not have happened without the many lab assistants I have worked with over the years including Jonathan Kleinman, Ryan Weaver, Nate Monson, Lindsay Young, Jeff Beauregard, Meredith Casciato, Jen Morse, Patricia Kazimier, Gift Poopat, and Melissa Bernatis. I would also like to offer many thanks to the funding agencies that supported this work, including The Department of Ecology and Evolutionary Biology, The University of Colorado Graduate School, The John Marr Fund, CIRES, as well as the UROP and BURST programs. I would like to express my everlasting gratitude to my family. I am so lucky to be surrounded by such loving, caring, selfless, and supportive people. I am the person I am today only because of you. I cannot thank you enough for all of the sacrifices you made, for answering my 3am phone calls, and reminding me every day that you are proud of me no matter what I choose to do with my life. Finally, but most of all, I would like to say thank you from the bottom of my heart to my fiancé, Paul Stoy, who was instrumental in almost every single aspect of completing this dissertation. His constant encouragement and use of the collective noun “we” when referring viii to finishing this thesis has served as a reminder that I not only have a partner in science but also in life. Words cannot express how grateful I am for his patience, unconditional love and support, and for always believing in me. His faith in my thoughts, ideas, research, and teaching mean more to me than he will ever know. I know I could not have done this without his gentle encouragements, his creative insights and edits, coffee runs, and hugs. Thank you for loving me through it all. ix CONTENTS CHAPTER I. INTRODUCTION……………………………………………………….1 1.1 Plant Secondary Chemistry………………………………..1 1.2 Environmental functions of isoprene and monoterpenes….1 1.3 The role of climate on isoprene and monoterpene synthesis and emissions…………………………………...4 1.4 Effects of monoterpenes on herbivore performance………6 1.5 Experimental questions…………………………………..10 II. CONTRIBUTION OF VARIOUS CARBON SOURCES TOWARD ISOPRENE BIOSYNTHESIS IN POPLAR LEAVES MEDIATED BY ALTERED ATMOSPHERIC CO2 CONCENTRATIONS………....…..12 Abstract………………………………………………………………....12 Introduction…………………………………………………..…………13 Materials & Methods……………………………………………………17 Results…………………………………………………………………..24 Discussion……………………………………………………….……...38 Conclusion…………………………………………………………...….44 III. HERBIVORY AND CLIMATE INTERACT SERIALLY DURING THE GROWING SEASON TO CONTROL MONOTERPENE EMISSIONS FROM PINYON PINE FORESTS……………………………………….……...46 Abstract..............................................................................................…...46 Introduction………..………………………………………………….…47 Materials & Methods………………………………………………….…49 Results…………………………………………………………………...58 Discussion………………………………………………….…………....70 IV. HERBIVORY-INDUCED CHANGES IN MONOTERPENE CONCENTRATIONS OF PINYON PINE NEEDLES ENCOURAGE FURTHER HERBIVORY
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