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The Ecological Consequences and Adaptive Function

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The Ecological Consequences and Adaptive Function THE ECOLOGICAL CONSEQUENCES AND ADAPTIVE FUNCTION OF NECTAR SECONDARY METABOLITES By Jessamyn Sara Manson A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Graduate Department of Ecology and Evolutionary Biology University of Toronto © Copyright by Jessamyn Sara Manson, 2009 The Ecological Consequences and Adaptive Function of Nectar Secondary Metabolites Jessamyn Sara Manson Doctor of Philosophy Department of Ecology and Evolutionary Biology University of Toronto 2009 ABSTRACT Plants are under selection to simultaneously attract pollinators while deterring herbivores. This dilemma can lead to tradeoffs in floral traits, which are traditionally thought to be optimized for pollinators. My dissertation addresses the ecological costs and putative functional significance of nectar secondary metabolites, a paradoxical but widespread phenomenon in the angiosperms. I investigate this issue from the pollinator’s perspective using a series of controlled laboratory investigations focused primarily on the bumble bee Bombus impatiens and the nectar alkaloid gelsemine, from Gelsemium sempervirens . I begin by demonstrating that nectar enriched with the alkaloid gelsemine significantly deters visits from bumble bees at a range of natural alkaloid concentrations. However, this aversion can be mitigated by increasing the sucrose concentration such that the alkaloid-rich nectar is more rewarding than its alkaloid-free counterpart. I then demonstrate that the consumption of gelsemine-rich nectar can inhibit oocyte development and protein utilization in bees, but that this effect is limited to bees of suboptimal condition. Continuous consumption of the nectar alkaloid gelsemine also leads to a reduction in the pathogen load of bumble bees infected with Crithidia bombi , ii but direct interactions between the pathogen and the alkaloid have no impact on infection intensity. Gelsemine also fails to inhibit floral yeast growth, suggesting that nectar alkaloids may not be universally antimicrobial. Finally, I demonstrate that gross nectar cardenolides from the genus Asclepias are strongly correlated with gross leaf cardenolides and that the majority of individual cardenolides found in nectar are a subset of those identified in leaves. This pattern suggests that nectar cardenolides are a consequence of defense for Asclepias ; however, they may not be a costly corollary because bumble bees show an overall preference for nectar cardenolides at mean concentrations. Altogether, my dissertation provides a new perspective on the role of chemical defenses against herbivores in plant-pollinator interactions. iii ACKNOWLEDGEMENTS Writing a dissertation is like raising a child – it takes a village! First of all, I’d like to thank my supervisor, James Thomson, who willingly welcomed this stray graduate student back in 2004. James understood that my interests lay in the field of chemical ecology and encouraged me to pursue research questions beyond the expertise of the lab. I am extraordinarily grateful to James for letting me take so many risks and teaching me to be stubbornly independent. I would also like to thank to Spencer Barrett and Peter Kotanen, the intrepid members of my supervisory committee, for their discussion and advice during my doctorate. Because of the integrative nature of my work, I have had a lot of help over the years. A huge thank you to three of my collaborators, Marc-André Lachance, Mario Vallejo-Marìn and Anurag Agrawal, who have allowed my research to grow in exciting new directions. I am very appreciative of all the time and energy that others have invested so that I could complete my chemical analyses; thank you to Sergio Rasmann, Rayko Halitchke, John Arnason and especially to Ammar Saleem, who spent many hours at the HPLC with me. Thanks to Bruce Hall and Andrew Petrie for watering my army of useless plants every time I was out of town. And thanks to Lynn Adler and Rebecca Irwin for suggesting that I work on a plant that shares my name! The members of the Thomson lab have been a wonderful source of guidance, support and collaboration. Thank you to Robert Gegear, without whom I would not know the joys of the flight cage, to Michael Otterstatter, who rekindled my passion for pathogens and to James Burns, Jessica Forrest, Nathan Muchhala, Jane Ogilvie and Alison Parker for being great friends and mentors. I have forged strong bonds with many iv members of the graduate community. I’d especially like to recognize Kate Edwards, Heather Coiner, Danielle Way, Danielle Marcos, Marc Johnson, Patrick Vogan, Sarah Yakimowski, Jannice Friedman, Brechann McGoey, Anna Simonsen and Brandon Campitelli for their friendship, humour and compassion throughout the course of my degree. I have also had an immense about of support from my family, particularly my parents. Thank you mom for teaching me to overcome obstacles with a smile on my face, thank you pa for instilling in me such a strong work ethic, and thank you dad for always telling me to go outside! Finally, this would not have been possible without the love and encouragement of my husband, Chris; your strength and generosity amaze me! I would also like to acknowledge several presses for permitting me to include previously published work in my thesis. Chapter two (R.J. Gegear, J.S. Manson and J.D. Thomson. 2007. Ecological context influences pollinator deterrence by alkaloids in floral nectar. Ecology Letters 10: 375-382) and chapter three (J.S. Manson and J.D. Thomson. 2009. Post-ingestive effects of nectar alkaloids depend on dominance status of bumble bees. Ecological Entomology 34: 421-426) were reproduced with permission from Wiley-Blackwell Publishing. Chapter four (J.S. Manson, M.C. Otterstatter and J.D. Thomson. In Press. Consumption of a nectar alkaloid reduces pathogen load in bumble bees. Oecologia DOI: 10.1007/s00442-009-1431-9) and appendix one (J.S. Manson, M.A. Lachance and J.D. Thomson. 2007. Candida gelsemii sp. nov., a yeast of the Metschnikowiaceae clade isolated from nectar of the poisonous Carolina Jessamine. Antonie von Leeuwenhoeck 92: 37-42) were reproduced with permission from Springer Science and Business Media. v TABLE OF CONTENTS ABSTRACT………………………………………………………………………...ii ACKNOWLEDGEMENTS………………………………………………………... iv TABLE OF CONTENTS…………………………………………………………... vi LIST OF TABLES…………………………………………………………………. x LIST OF FIGURES………………………………………………………………... xi LIST OF APPENDICES…………………………………………………………... xiii CHAPTER ONE – Introduction…………………………………………………… 1 A brief history of nectar secondary metabolites…………………………… 2 A spotlight on alkaloids……………………………………………………. 6 Principal experimental systems……………………………………………. 7 How toxic is “toxic” nectar? Addressing the ecological consequences and adaptive functions of nectar secondary metabolites……………………9 CHAPTER TWO – Ecological context influences pollinator deterrence by alkaloids in floral nectar……………………………………………………………12 Abstract…………………………………………………………………….. 12 Introduction………………………………………………………………… 13 Methods……………………………………………………………………. 16 Bees and flowers …………………………………………………………… 16 Experimental procedure …………………………………………………….17 Data analysis ………………………………………………………………. 18 Results……………………………………………………………………... 20 Flower preference ………………………………………………………….. 20 vi Foraging proficiency ………………………………………………………. 21 Discussion………………………………………………………………….. 21 Acknowledgements………………………………………………………… 26 CHAPTER THREE – Post-ingestive effects of nectar alkaloids depend on dominance status of bumble bees………………………………………………….. 32 Abstract……………………………………………………………………. 32 Introduction………………………………………………………………… 33 Methods……………………………………………………………………. 36 Oocyte development ………………………………………………………... 36 Haemolymph carbohydrates ……………………………………………….. 39 Results……………………………………………………………………... 39 Protein metabolism ………………………………………………………… 39 Carbohydrate concentrations ……………………………………………… 40 Discussion………………………………………………………………….. 40 Acknowledgements………………………………………………………… 45 CHAPTER FOUR – Consumption of a nectar alkaloid reduces pathogen load in bumble bees……………………………………………………………………... 50 Abstract…………………………………………………………………….. 50 Introduction………………………………………………………………… 51 Methods……………………………………………………………………. 54 Statistical analysis …………………………………………………………. 57 Results……………………………………………………………………... 58 Discussion…………………………………………………………………. 60 vii Acknowledgements………………………………………………………… 65 CHAPTER FIVE – Cardenolide concentrations of nectar, leaves and flowers: A comparative study across Asclepias series Incarnatae…………………………... 72 Abstract…………………………………………………………………….. 72 Introduction………………………………………………………………… 73 Methods……………………………………………………………………. 77 Study system ………………………………………………………………... 77 Quantifying cardenolides …………………………………………………... 77 Pollination biology ………………………………………………………….80 Statistical analysis …………………………………………………………. 83 Quantitative cardenolide analysis …………………………………………. 83 Qualitative cardenolide analysis …………………………………………... 84 Behaviour analysis …………………………………………………………. 86 Results……………………………………………………………………....87 Quantitative cardenolide analysis …………………………………………. 87 Qualitative cardenolide analysis …………………………………………... 88 Behaviour analysis …………………………………………………………. 90 Discussion………………………………………………………………….. 92 Acknowledgements………………………………………………………… 101 CHAPTER SIX – CONCLUDING DISCUSSION………………………………... 108 Ecological context is crucial……………………………………………….. 109 A subtle effect is still an effect…………………………………………….. 110 There is no such thing as a general adaptive hypothesis…………………... 111 viii Consequence of defense is often assumed but rarely
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