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Environmental and genetic aspects of aboveground-belowground interactions in theAmmophila arenaria system Martijn L. Vandegehuchte Ghent University Faculty of Sciences Academic year 2010‐2011 ENVIRONMENTAL AND GENETIC ASPECTS OF ABOVEGROUND‐BELOWGROUND INTERACTIONS IN THE AMMOPHILA ARENARIA SYSTEM OMGEVINGS‐ EN GENETISCHE ASPECTEN VAN BOVENGRONDS‐ONDERGRONDSE INTERACTIES IN HET AMMOPHILA ARENARIA SYSTEEM MARTIJN L. VANDEGEHUCHTE THESIS SUBMITTED IN FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR (PHD) IN SCIENCES PROEFSCHRIFT VOORGEDRAGEN TOT HET BEKOMEN VAN DE GRAAD VAN DOCTOR IN DE WETENSCHAPPEN Promotor: Prof. Dr. Dries Bonte Co‐promotor: Dr. Eduardo de la Peña Reading committee: Prof. Dr. Wim Bert (Ghent University) Dr. Martijn Bezemer (Netherlands Institute of Ecology) Dr. Gerlinde B. de Deyn (Netherlands Institute of Ecology) Prof. Dr. Hans Van Dyck (Université catholique de Louvain) Other members of the examination committee: Prof. Dr. Dries Bonte (Ghent University) Dr. Eduardo de la Peña (Ghent University) Prof. Dr. Dominique Adriaens (chairman, Ghent University) Date of public defence: 17 December 2010 Vandegehuchte M. L. 2010. Environmental and genetic aspects of aboveground‐belowground interactions in the Ammophila arenaria system. PhD Thesis, Ghent University, Ghent, Belgium. ISBN: 978‐90‐9025921‐5 The research reported in this thesis was conducted at the Terrestrial Ecology Unit (TEREC), Department of Biology, Faculty of Sciences, Ghent University. Address: Karel Lodewijk Ledeganckstraat 35, B‐9000 Ghent, Belgium. This research was funded by a predoctoral grant of the Research Foundation – Flanders (FWO). Acknowledgements This thesis is the product of four years of work, although in retrospect it seems much shorter. Maybe that is because it never really felt like ‘work’ to me. During this period many people helped or supported me in various ways. Without them, writing this book would not have been possible. First of all, I would like to thank two people who were closely involved with my work: my supervisor Dries Bonte and co‐supervisor Eduardo de la Peña. I am fully aware that not many PhD students have the sheer luck to be surrounded by such splendid guides, so a lot of credit for this thesis goes to them. Dries was also the supervisor of my MSc thesis, and when he asked me whether I was interested in applying for a doctoral grant, I needed very little convincing. Dries, your unstoppable enthusiasm about science is downright infectious. In times when scientific excitement tends to dampen, you always reminded me of the bigger picture, the greater goal. Thanks also for your almost instantaneous answers to my numerous questions, many of those via e‐mail at late hours and on Sundays, often about details of which the relevance was questionable. Eduardo, your sense of methodological detail often saved me a lot of practical disaster and lost time. Furthermore, your down‐to‐earth approach of science was often a good counterbalance in these times of publication pressure, where fancy concepts are sometimes valued higher than solid science. Your nice sense of absurd humour often provided a welcome distraction. Thanks also for kindly putting your office at my disposal to use as an aphid culture room, and your laptop to finish this book. However, and more importantly, I would like to thank both of you guys for encouraging me to develop my own ideas, for giving me the opportunity to be part of a constructive team, and last but not least for the fun times at conferences across the globe. Jean‐Pierre Maelfait started as the supervisor of my PhD. Unfortunately, he passed away before I had the chance to get to know him better. He was always prepared to give his well‐thought‐out ideas on any matter, and he i often saw that little detail that others had missed. His advice was much appreciated. He is and will continue to be missed at Terec. Without Viki Vandomme and Hans Matheve, a lot of ideas that looked nice on paper would not have been put into practice. Thanks for driving me around, measuring grasses, digging up sand, carrying sand through the dunes and so on. In this context I would also like to thank the other lab members who, completely voluntarily, helped me out with my much dreaded field work. But I’ll get to you guys in a moment. Viki, thanks for arranging all things administrative for me. This was a luxury that cannot be understated. I would also like to thank Thomas Terrie for the field assistance and the good gardening skills that kept my plants healthy and fresh. I have been fortunate to have had two very good MSc students during my PhD, Bart Vandenbossche and Roeland Cortois. Bart, thanks for the detailed work on the nematodes and good luck with the research in Germany. Roeland, thanks for delivering such good work, despite the fact that I unintentionally sabotaged your plant stock once. I hope all goes well with the PhD in the Netherlands. I am furthermore grateful to Dr. Peter Breyne for performing the AFLP analyses of the grasses. I would like to thank Dr. Oscar Vorst for checking beetle identifications, Dr. Roland Mühlethaler for checking leafhopper identities and Prof. Dr. Juan Nieto Nafría and Dr. Nicolás Pérez Hidalgo for confirmation of aphid identifications. I am also grateful to the members of the reading committee for their valuable comments and suggestions on the previous version of this thesis. To the guys of the lab, Boffie, Bram(bo), Bram (b‐dog), Stevo, Hans, Charlie and the others, thanks for Brabor‐Hanmar, the food‐bot, the whisky tasting, the pub nights, the parties, the coffee table discussions that had to be settled by Wikipedia, the field weeks at the coast in June and the numerous other joyous events that I can’t think of right now. Thanks also for getting me from behind my desk for some sports every now and then. My levels of darts and pool would not have been the same without you guys. ii Thanks also to Kevin for the practical jokes which on regular occasions cheered up everyone but the victim, and thanks to the block of lead for not killing anyone in the process. I would like to thank Carl Vangestel, who was always willing to put aside more urgent matters in order to answer my statistical questions. Carl, the way you manage to explain something abstract in a few lines and words is admirable. The many conferences and workshops that I have attended over the past four years would have been much duller without their social evening aspect. I don’t know how we did it, but we always seemed to quickly find those people who valued this social aspect as much as we did. It was people like Yann Hautier, Klaus Birkhofer, Stefanie Kortman and Sarah Kenyon, to name just a few, who made the difference. If it weren’t for conferences, I would probably never have met Lucía Latorre Piñeiro. Lu, thanks for the hospitality and for guiding us around in Mallorca as well as in Galicia, and for the good times we had both in Spain and back here in Belgium. You’re the living proof that scientists needn’t be boring. Good luck with finishing the PhD and with the band. And by the way, say hi to your mom. I would like to thank my parents, commonly referred to as Matje and Patje, who have always encouraged me to pursue my own interests. I also want to thank my two brothers. Michel, thanks for so often paving the way for me (even though you might have put the standards a bit high). Mau, within a few years it’s your turn, and I’m sure you will do a great job, which you usually do with everything you undertake. Then the world will know three doctors M. Vandegehuchte, which might come in handy when making publication lists. Thank you guys for always being there. Furthermore, I would like to thank my grandfather, Louis Ven, a man with a keen interest in science. He encouraged me throughout my higher education and was always eager to know what I was working on. Thanks to Brecht, Thijs and Karl for keeping the comradeship alive. I think of the ski trekking in Lapland and Jämtland, the Natuurpunt quizzes and the countless gatherings in pubs throughout Ghent. I know many of the crazy plans for journeys to desolate places ended up in the drawer because of the iii PhD, but let’s take them out and see what can be done. Dave, thanks for those entertaining evenings with their sumptuous dinners, potent coffee and South Park episodes. May many of those follow. Bieke, you never made a fuss when, yet again, work got the highest priority. Thanks for your patience, support and optimism. Thanks also for all the good times we had over the past years, including our travels and small trips. Moreover, thanks for proofreading the entire thesis. Life just seems so much easier with you. Bie, thanks for being there and being who you are. Again to all of you people: thanks! Martijn L. Vandegehuchte 6 December 2010 iv Table of contents 1 Introduction ......................................................................................................... 1 1.1 The emerging awareness of the importance of aboveground‐ belowground interactions.................................................................. 2 1.2 The primary producer approach ........................................................ 5 1.3 Herbivore‐herbivore interactions ...................................................... 6 1.4 Herbivore‐mutualist interactions....................................................... 8 1.5 The interplay with abiotic soil factors.............................................. 11 1.6 Evolutionary consequences of aboveground‐belowground interactions ...................................................................................... 14 1.7 Ammophila arenaria: a multifunctional study system..................... 17 1.8 Objectives and outline of the thesis................................................. 26 2 Interactions between root and shoot herbivores of Ammophila arenaria in the laboratory do not translate into correlated abundances in the field ................