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This Thesis Has Been Submitted in Fulfilment of the Requirements for a Postgraduate Degree (E.G. Phd, Mphil, Dclinpsychol) at the University of Edinburgh

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This Thesis Has Been Submitted in Fulfilment of the Requirements for a Postgraduate Degree (E.G. Phd, Mphil, Dclinpsychol) at the University of Edinburgh This thesis has been submitted in fulfilment of the requirements for a postgraduate degree (e.g. PhD, MPhil, DClinPsychol) at the University of Edinburgh. Please note the following terms and conditions of use: This work is protected by copyright and other intellectual property rights, which are retained by the thesis author, unless otherwise stated. A copy can be downloaded for personal non-commercial research or study, without prior permission or charge. This thesis cannot be reproduced or quoted extensively from without first obtaining permission in writing from the author. The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the author. When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given. Ant-pollinator interactions in Turnera velutina: ecological costs and evolutionary consequences for the ant-plant pollination Nora Villamil Buenrostro January 2019 A thesis submitted for the degree of Doctor of Philosophy University of Edinburgh 2019 LAY SUMMARY Ant-plants recruit aggressive ants to defend themselves against herbivores. Herbivores, eat plants voraciously. Plants have evolved different mechanisms to defend themselves against herbivores. Some are poisonous: like coffee or tobacco; some are prickly: like cacti or nettles. But others, persuade mercenaries - mostly ant guards - offering them sugary rewards and housing, and hence are called ant-plants. So, in exchange for protection services, these plants provide ants with food and nesting sites. However, most ant-plants are pollinated by animals, different from ants, and they also reward them with food, such as nectar. But guarding ants are usually not great at discriminating between friends and foes that visit the plant. So, pollinators may be weary when visiting the flowers of ant-plants. This plant problem is called ant-pollinator conflict. My PhD research tries to answer: Do ants and pollinators fight directly or over nectar? Does having efficient bodyguards scare pollinators away and how does this affect the plants? Can plants bribe ants away with extrafloral sugary rewards? I found that ants and bees do not fight over nectar, but they may fight directly. Pollinators spend less time visiting the flowers where the most aggressive ants are. Bodyguards scare away pollinators affecting flowers’ sex life. By reducing the time pollinators spend inside flowers, ants help the plants avoid mating with themselves (self-pollinating). Self-pollination can make plant seeds grow poorly, like haemophilia, an illness that made the royals die from bleeding and was caused by them marrying with their relatives. However, to reduce ant-pollinator conflicts, plant bribe ants away from the flowers providing them extrafloral sugary rewards on the outskirts of the flowers. Understanding how guarding ants affect the pollination biology and fruit production of ant-plants is crucial for all of us, since we deeply care about our morning toast, sweet or savoury, and our passionfruit juice to down the toast. ABSTRACT Ant-plants recruit ants to defend them against herbivores, but most of them also require pollinator for successful seed set. Interactions between patrolling ants and pollinators on ant-plants have received relatively little attention. Negative ant- pollinator interactions are expected for several reasons. First, ants and pollinators benefit from plant investment in different functions (defence and reproduction, respectively) which can lead to plant trade-offs. Second, although more aggressive ants are likely to be better defenders, they may also deter pollinators, affecting plant fitness. However, ant-plants may have mechanisms to manage ant-pollinator interactions, maximising the benefits from their services whilst minimising the costs. I used field experiments to investigate the ecological costs and evolutionary consequences of ant patrolling for the pollination biology of a facultative ant-plant, the Mexican endemic Turnera velutina (Passifloraceae), addressing the following questions: a) Which are the most aggressive and best ant defenders of T. velutina? b) Is there direct (pollinator deterrence) or indirect (nectar trade-offs) ant- pollinator conflict? c) What are the ecological costs and evolutionary consequences of myrmecophily for the host plant pollination and mating system? d) Do ant-plants have adaptations to cope with both mutualists, avoiding conflict? Answers: a) Cephalotes sp. ants was detected as parasitic non-defenders, and the remaining ant species were ranked as: Capmponotus planatus < Crematogaster sp. < Paratrechina longicornis < Brachymyrmex sp. < Dorymyrmex bicolor. b) I found evidence for direct but not for indirect conflict. c) Ant patrolling affected pollinator visit duration, pollen loads, outcrossing rates, and male fitness, leading to negative effects on pollinator foraging efficiency, but such changes had positive effects for plant fitness increasing outcrossing and male fitness. d) Extrafloral nectar also serves to bribe ants away from reproductive structures during the crucial pollination period, reducing the probability of ant-occupation of flowers, reducing ant-pollinator conflict, and increasing plant reproductive success. DECLARATION I declare that this thesis has been composed solely by myself and that it has not been submitted, in whole or in part, in any previous application for a degree. Except where stated otherwise by reference or acknowledgment, the work presented is entirely my own. 14 January 2019 Nora Villamil Buenrostro ACKNOWLEDGEMENTS First and foremost, thanks to the Mexican people. Their tax contributions, despite the Mexican government’s well-known skimming of public resources, funded my postgraduate studies through a Conacyt Graduate Scholarship. A real privilege for which I will be always grateful. Thanks to my supervisors, both past and surviving ones. My PhD was not a smooth glide, but rather a jumpy rollercoaster with constant changes. With almost as many supervisory teams as years in the PhD. Two locations and three different projects down the line, this was not a smooth journey, but a very enrichening one. Although I cursed them at the time, now I appreciate every single one of those transitions. Thanks to Graham, my longest standing official supervisor. Thanks for the opportunity provided, despite the abnormal starting circumstances. I am very grateful for your openness and risk-prone behaviour. Being willing to take a random person with a half-started project which did not align with your current projects and for which there was no budget, is quite a bet I shall always be grateful for. Without that opportunity this PhD would not have been possible, and I have thoroughly enjoyed it. I am very glad to have been ‘associated to’ your lab. Thank you as well for your knowledge and patience, and meticulous teachings on how to use whiskey to proofread a paper for the 500th time. For the nourishing discussions on hypothesis and biological implications. Thank you for all the space and freedom you gave me to shift my project in any direction I wanted to. But above all, thanks for being always open to receiving critical views, even those that were not coated with Britishness. Thanks for resisting all the meetings, half of which I know felt like boxing matches. I have learned so much and it has been all good fun. Thanks, and many of them, to Jarrod. Your contribution towards the successful completion of this thesis was enormous and scattered in all dimensions. Thanks for your kind disposition to take me on board, the statistical advice and for being the wizard that turned weeks of problems into solutions in an R spell. Thanks for the patience, empathy, but above all, the modesty with which you share your knowledge and time. Thanks also for employing me as a field assistant despite my spatial awareness and visa handicaps. The salary was essential for the writing up months, but the outdoorsy break was too! To Karina all my gratitude for being the longest standing unofficial supervisor, bearing with me for over a decade. Thanks for the advice, for always being there for me ‘en las buenas y en las malas’. Welcoming, year after year, project after project, helping me get out of every ditch I got myself into. For giving me the courageous spell to exit Harry-Potterland. Your never-ending enthusiasm, your encouragement for the good ideas, and your honest discouragement of the crazy ones have been invaluable. Thanks for believing in me even when not even I did so. Your support has been so big that it spread across the ocean! Roosa, long time no see but still many thanks for the starting push, the coffee room meetings where you patiently listened to and unravelled messy ideas and enhanced them with accurate suggestions. Thanks for showing me the best sandwich shop in town, the yoga lessons and the opportunity of a fresh, new start. William and Cicely, thanks for the multiple rescue missions expanding from the advisory realm to the emergency couch, or the great plans Ebola destroyed. Your passions for tropical botany are contagious and were inspiring and sparkling bubbles in the flattest and darkest of times. Many thanks to Alex Twyford and his lab for kindly being my foster lab, even though I struggle to comprehend any genomics! Thanks to Susie Johnston and Patrick Walsh for their support. I am grateful to my examiners, Ally Phillimore and Scott Armbruster, who brought upon themselves this heavy document. To the Stone lab, past and present members, a great crowd! To the LIPA lab, a place of endless comradery. To Sofía and Xochitl for a decade of side-by-side growth, fun and friendship. To all the other Turneritos and non- Turneritos. Thanks to the volunteers who helped out during fieldwork: Sofía Ochoa, Xochitl Damián and Paulina Zedillo, Alberto Bernal, Arturo Martínez, Rosa Ríos, Iñigo Silva, Adriana Fournier, Jorge Comensal, Ana Urrutia, Aura Orloff, and to Helene Köck who helped processing pollen samples. Thanks as well to the staff at CICOLMA Field Station for the palapa chats, the best beans in the world, the natural remedies for any ailment and much more.
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