Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften (Dr. rer. nat.) an der Fakultät für Biologie der Ludwig-Maximilians-Universität München THE BIOGEOGRAPHY, EVOLUTION, AND FUNCTION OF LEAF-OUT PHENOLOGY STUDIED WITH EXPERIMENTAL, MONITORING, AND PHYLOGENETIC APPROACHES Constantin Mario Zohner München, 20. August 2016 ii PREFACE! Statutory declaration Erklärung Diese Dissertation wurde im Sinne von §12 der Promotionsordnung von Prof. Dr. Susanne S. Renner betreut. Ich erkläre hiermit, dass die Dissertation nicht einer anderen Prüfungskommission vorgelegt worden ist und dass ich mich nicht anderweitig einer Doktorprüfung ohne Erfolg unterzogen habe. Eidesstattliche Erklärung Ich versichere hiermit an Eides statt, dass die vorgelegte Dissertation von mir selbstständig und ohne unerlaubte Hilfe angefertigt wurde. Constantin Zohner, 20. August 2016 (Unterschrift) 1. Gutachter: Prof. Dr. Susanne S. Renner 2. Gutachter: Prof. Dr. Hugo Scheer Tag der Abgabe: 25.08.2016 Tag der Disputation: 21.11.2016 iii iv Note In this thesis, I present the results from my doctoral research, carried out in Munich from January 2014 to August 2016 under the guidance of Prof. Dr. Susanne S. Renner. My thesis resulted in four manuscripts, presented in Chapters 2 to 5, of which two have been published (Chapters 2 and 5), one is accepted (Chapter 3), and one is in review (Chapter 4). I also gave the conference talks listed below. I generated all data and conducted all analyses myself except for Chapter 5 for which I contributed the phenological data and conducted some analyses. Writing and discussion involved collaboration with S.S. Renner, with input from J.-C. Svenning (Chapters 3 and 4), and J.D. Fridley (Chapter 4). L. Muffler led the writing in Chapter 5, and I wrote all parts concerned with phenology. Constantin Zohner Prof. Susanne S. Renner (Signature) (Signature) List of publications Peer-reviewed journal articles ZOHNER, C.M., BENITO, B.M., FRIDLEY, J.D., SVENNING, J.-C., RENNER, S.S. In review. Spring predictability explains different leaf-out times in the Northern Hemisphere woody floras. Nature. ZOHNER, C.M., BENITO, B.M., SVENNING, J.-C., RENNER, S.S. In press. Photoperiod unlikely to constrain climate change-driven shifts in leaf-out phenology in northern woody plants. Nature Climate Change. MUFFLER, L., BEIERKUHNLEIN, C., AAS, G., JENTSCH, A., SCHWEIGER, A.H., ZOHNER, C.M., KREYLING, J. 2016. Distribution ranges and spring phenology explain late frost sensitivity of 170 woody plants from the Northern hemisphere. Global Ecology and Biogeography. DOI: 10.1111/geb.12466, first published 29 May 2016 ZOHNER, C.M., AND RENNER, S.S. 2015. Perception of photoperiod in individual buds of mature trees regulates leaf-out. New Phytologist 208: 1023 – 1030. v vi Oral presentations ZOHNER, C.M. Historical climates explain contrasting dormancy-breaking requirements in North American, Asian, and European woody species. EGU General Assembly, Vienna, Austria, 18 April 2016 ZOHNER, C.M. (Why) do temperate woody species use the photoperiod to regulate leaf-out? Phenology Workshop and Prep Meeting for AABG 4, Pont de Nant, Switzerland, 14 November 2015 ZOHNER, C.M. Perception of photoperiod in individual buds of mature trees regulates leaf-out. International Conference on Phenology, Kusadasi, Turkey, 8 October 2015 ZOHNER, C.M. (Why) do plants use the photoperiod to regulate leaf-out? Technical University Munich, Botanikertagung 2015, From molecules to the field, Freising, Germany, 2 September 2015 ZOHNER, C.M. Biogeographic history of Limonium (Plumbaginaceae), inferred with the first model that includes a parameter for speciation with dispersal. 16. Jahrestagung der Gesellschaft für Biologische Systematik (GfBS), Bonn, Germany, 19 March 2015 ZOHNER, C.M. The evolution and function of phenological signals and species-specific changes in leaf-out times. Seminar series at Department of Ecology, Environment and Plant Sciences, Stockholm, Sweden, 19 August 2014 Poster ZOHNER, C.M., AND RENNER, S.S. Does biogeographic origin influence leaf-out phenology? International Biogeography Society: 7th Biennial Meeting, Bayreuth, Germany, Jan 8– 12, 2015. ZOHNER, C.M., AND RENNER, S.S. Climate-change induced shifts in leaf-out times. Radiations 2014, Zurich, Switzerland, June 12–15, 2014. vii viii CONTENTS Preface............................................................................................................................................iii Statutory Declaration...........................................................................................................iii Erklärung.............................................................................................................................iii Eidesstattliche Erklärung.....................................................................................................iii Note.......................................................................................................................................v List of publications...............................................................................................................v Oral presentations...............................................................................................................vi Poster..................................................................................................................................vii Contents.........................................................................................................................................vii Summary.........................................................................................................................................1 Chapter 1: General Introduction.....................................................................................................3 Plant phenology....................................................................................................................5 The ecological implications from phenological transitions in response to climate change..6 Experimental phenology.................................................................................................7 Leaf-out in woody plants and the environmental factors that regulate it........................8 Causes of intra- and interspecific variation in leaf-out phenology...............................10 Research questions..............................................................................................................13 Chapter 2: Perception of photoperiod in individual buds of mature trees regulates leaf-out.......15 Chapter 3: Photoperiod unlikely to constrain climate change-driven shifts in leaf-out phenology in northern woody plants..................................................................................29 Chapter 4: Spring predictability explains different leaf-out strategies in the Northern Hemisphere woody floras...................................................................................................73 Chapter 5: Distribution ranges and spring phenology explain late frost sensitivity of 170 woody plants from the Northern hemisphere........................................................127 Chapter 6: General Discussion...................................................................................................147 6.1. Do temperate woody species use the photoperiod in spring as a cue for leaf-out?...........................................................................................................149 6.2. Geographic variation in leaf-out strategies................................................................151 6.3. Phenology and invasive success................................................................................153 ix x 6.4. Herbarium phenology................................................................................................154 6.5. Future research questions...........................................................................................156 6.5.1. Using latitudinal gradients to study intraspecific variability of leaf-out....156 6.5.2. Leaf senescence and vegetation periods.....................................................159 6.5.3. The molecular basis of dormancy release...................................................160 References....................................................................................................................................162 Acknowledgements.....................................................................................................................171 Curriculum vitae.........................................................................................................................173 xi xii SUMMARY This dissertation deals with the timing of leaf unfolding in temperate woody plants, especially as regards the ongoing climate change. It particularly asks (i) if and how plants use photoperiod duration to regulate leaf-out, (ii) how adaptation to climate parameters relates to inter-specific variability in leaf-out strategies, (iii) if region-specific frost probabilities explain global biogeographic patterns in leaf-out phenology, and (iv) whether a species’ frost sensitivity is linked to its phenological strategy. To address these questions, I studied the phenology of 1600 woody species grown under common conditions in temperate gardens using experimental and monitoring approaches. The experiments particularly served to disentangle the three key drivers of leaf unfolding: photoperiod,
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