Ecological and physiological implications of vascular structure and function in oaks A DISSERTATION SUBMITTED TO THE FACULTY OF THE UNIVERSITY OF MINNESOTA BY Jennifer Teshera-Levye IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY Advisor: Dr. Jeannine Cavender-Bares December 2019 ©2019. Jennifer Teshera-Levye \Drivers of habitat partitioning among three Quercus species along a hydrologic gradi- ent" accepted for publication November 15, 2019 in Tree Physiology. DOI: 10.1093/treep- hys/tpz112 Acknowledgements I am grateful to the support, advice, guidence, and feedback I recieved from countless people over the years. My advisor, Dr. Jeannine Cavender-Bares, has been tremendously supportive of all my ideas and goals. My committee, Dr. Arindam Banarjee, Dr. Rebecca Montgomery, and Dr. Daniel Stanton, as well as former members Dr. Peter Reich and Dr. Emma Goldberg, have helped shape the direction of the work through their questions and insights. My first chapter, \Drivers of habitat partitioning among three Quercus species along a hydrologic gradient" was written with several co-authors: Brianna Miles, Catherine Love- lock, Valery Terwilliger, and Dr. Cavender-Bares. Their feedback and suggestions were invaluable during the submission and revision process for that manuscript. The data used in that chapter was collected by a group lead by Dr. Cavender-Bares at the Smithsonian Environmental Research Center from 2001-2003. I also need to thank the Smithsonian En- vironmental Research Center for logistical support, William Brinley and Nathan Phillips for technical assistance in construction of the sapflow sensors and Geoffrey Parker for providing access to the 50-ha plot and for other support. We thank Marilyn Fogel for allowing us to use her former facilities the Geophysical Lab at the Carnegie Institution in Washington, D.C. for isotopic analyses, Lauren Urgenson, George Raspberry (posthumously), Roxane Bowden, Kati Dawson, Andrea Krystan, and Patrick Neale for technical and other assis- tance. The water table and soil moisture data provided in the appendix were gathered as part of an NSF funded project to Sean McMahon (NSF Grant 1137366) and is curated by Rutuja Chitra-Tarak. The data collected for my second and third chapter was made possible by the greenhouse common garden projects maintained by Dr. Matthew Kaproth and Dr. Beth Fallon, along with a team of undergraduate students. Lab work was assisted by several students, most critically Philip Johnson, Hilary Major, and Alejandra Villasen~or. Cory Teshera-Levye contributed code that was used in the LeafGrapher software. My labmates in the Cavender-Bares lab over the years have provided countless sugges- tions and improvements to my work, and this dissertation would not have been possible without them. Finally, my family and friends offered support in myriad ways. My parents, Marc and Judy Levye, instilled in me from an early age the value of perseverance and dilligence. Cory Teshera-Levye is my partner in life, the universe, and everything. i Dedication \Life needs things to live"1 and graduate students need things to keep them sane. This work dedicated to the people who helped me stay connected, grounded, and who let me escape into fantasy worlds when the real one was overwhelming. Also dedicated to Rosemary, Bernie, and Bean Sprout, for keeping me warm through many cold winters. 1Jaffe, T. (2016) "Critical Role Ep. 63: The Echo Tree." www.youtube.com/watch?v=1cUx2oLUGqI ii Contents List of Figures iv List of Tables vi Introduction 1 1 Drivers of habitat partitioning among three Quercus species along a hy- drologic gradient 3 2 LeafGrapher: A software tool for network analysis of leaf venation 28 3 Network-derived traits help demonstrate resource-allocation trade-offs in oaks 44 Bibliography 59 Appendix 72 iii List of Figures 1.1 Broad and local distributions of Q. alba,Q. falcata, and Q. palustris . 14 1.2 Weather conditions at SERC . 15 1.3 Average daily sap flux patterns . 16 1.4 Water-use traits in mature trees . 20 1.5 Hydraulic conductance in mature trees and seedlings . 21 1.6 Growth rates in mature tree species with elevation . 22 1.7 Physiological traits measured in seedlings . 27 2.1 An illustration of network terminology . 31 2.2 Illustration of graph spectra. 32 2.3 Estimating vessel diameter . 34 2.4 Example leaf venations . 38 2.5 Four core graph metrics . 39 2.6 Efficiency versus hydraulic conductance . 40 2.7 Fault tolerance comparison between ginkgo and oak . 41 2.8 Eigenvalues of the graph Laplacian . 42 3.1 Theoretical \return on investment" . 46 3.2 Correlations between graph traits and leaf functional traits. 50 3.3 Principle component analysis of venation and functional traits . 51 3.4 Hydraulic performance return on investment in vasculature . 52 3.5 Resistance to damage return on investment in vasculature . 52 3.6 Mean trait values in leaves differentiated by venation performance . 53 3.7 Correlations among venation traits and climate variables . 54 3.8 Graph traits vary with mean species aridity index . 55 3.9 Fault tolerence in red versus white deciduous oaks . 56 S1 Appendix: Hypothesis schematic . 74 S2 Appendix: Soil types at SERC . 75 S3 Appendix: Water table depth at SERC . 76 S4 Appendix: Soil water content at SERC . 77 S5 Appendix: Within-tree sap velocity comparison . 78 iv S6 Appendix: Sap flow sensor comparisons . 79 S7 Appendix: Sap flux velocity . 80 S8 Appendix: predawn and midday water potential . 81 v List of Tables 1.1 Soil moisture in mature tree and common garden sites . 6 1.2 Soil charactistics at SERC by elevation . 7 1.3 Mean climatic conditions of species ranges . 13 1.4 Trait means in mature trees . 17 1.5 Trait means in common garden seedlings . 18 3.1 Specimens included in analysis . 47 3.2 Major graph traits, with units and notes. * = unitless . 49 S1 Appendix: Mature tree sampling . 72 S2 Appendix: Weather conditions at SERC . 72 S3 Appendix: Species distributions by elevation . 73 S4 Appendix: Tree wood characteristics . 73 vi Introduction Water plays a critical role in the survival of all life, and access to sufficient water to support physiological needs has been a primary driver in the evolution of plant form and function since they moved onto land. Among other innovations, plants developed a rigid vascular system that offers both mechanical support and transport of water and nutrients (Tyree 2003). Indeed, plant vasculature has been described as the \backbone" supporting the productivity of terrestrial ecosystems (Brodribb 2009). This system is also vulnerable: function can be lost due to air embolism introduced through drought or freezing, as well as through physical damage or blockages introduced by pests or pathogens (Rockwell et al. 2014, Pratt et al. 2008). Despite its importance, there is still much that is unknown about the physiological ecology of the plant vascular system. In this dissertation I investigate connections between plant hydraulics and ecological function at at two scales. First, I consider the implications of differing performance in whole-plant water transport traits for the habitat partitioning of several closely related tree species along a hydrologic gradient. Second, I consider the vascular architecture of leaves by demonstrating a novel methodology for quantifying venation structure and by applying this methodology to consider resource-allocation trade-offs. In this work, I primarily use the oaks (genus Quercus in family Fagaceae) to consider these questions. The oaks are diverse and cosmopolitan; they are a dominant clade in North American forests, and are found across the Americas, Europe, and Asia (Cavender-Bares 2016). The genus includes both evergreen and deciduous species, and can be found in a wide range of habitats. In the United States, the oaks are economically valuable, providing over $22 billion per year in ecosystem services, but are also increasingly vulnerable to climate change and pathogens (Cavender-Bares et al. 2019). The first chapter, \Drivers of habitat partitioning among three Quercus species along a hydrologic gradient", I and my co-authors considered how differences in water-use traits might permit three oak species to co-exist in a small geographic area (the Big Tree Plot at the Smithsonian Environmental Research Center). We compare the performance of both mature trees and and seedlings of these oak species when grown under different hydrologic conditions. In addition to differences in physiological and functional traits, we consider the ability of the climate of broad geographic ranges to predict local habitat partitioning. For my second and third chapters, I shift from a consideration of whole-plant hydraulics 1 to leaf hydraulics. Leaves are a critical bottleneck in the overall water transport system of plants (Sack and Frole 2006), but our understanding of how the structure of leaf vascular systems influences plant function remains incomplete (Roth-Nebelsick et al. 2001). Here, I attempt to apply tools developed from the mathematical field of network theory to better understand vascular architecture. I present \LeafGrapher," a software tool developed to represent a leaf vein system abstractly as a graph, and then calculate a set of metrics drawn from the network theory literature (Barth´elemy 2011). I illustrate the use of this software tool with a sample data set capturing the diversity of plant vascular and show a tentative assoication of one of these metrics with empirically measured leaf hydraulic conductance. I follow this with an analysis of the leaf venation architecture of 16 oak species, testing for associations between known plant functional traits and my new network-informed vascular traits, as well as the potential influence of climate on these venation traits. A central theme running through these chapters is an attempt to understand the trade- offs plants make in allocating resources. Given a limited set of available resources, plants must \choose" between using these resources for growth, productivity, reproduction, pro- tection, or any number of other functions (Obeso 2002, Chapin III 1989, Coley et al.