An ecological and evolutionary perspective on functional diversity in the genus Salix A DISSERTATION SUBMITTED TO THE FACULTY OF THE GRADUATE SCHOOL OF THE UNIVERSITY OF MINNESOTA BY Jessica Anne Savage IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY Dr. Jeannine Cavender-Bares May 2010 © Jessica Savage 2010 Acknowledgements I would like to acknowledge all of the people and organizations that helped me complete this research and supported me during my time as a student. I would like to thank all of the faculty, including my advisor, Jeannine Cavender-Bares, and my committee, Rebecca Montgomery, Peter Reich, George Weiblen, and Ruth Shaw for their guidance and input over the years. I would also like to thank my collaborators including Amy Verhoeven and Lawren Sack. I am especially grateful for Amy’s help developing protocols for my photoprotection study and her help with the HPLC analyses. I would also like to thank Jonathan Friedman with the U.S. Geological Survey and Steve McNamara with the University of Minnesota Landscape Arboretum for their input in regards to my freezing experiments. Both Jonathan and Steve shared information about their research and helped me develop several protocols for my larger-scale study. I also received valuable input on my molecular research and phylogenetic analyses from Irena Belyvaea and the late Steven Brunsfeld. Irena Belyvaea shared with me the ADH primers designed in her lab, along with her PCR protocols. Steven Brunsfeld was one of my first contacts when I began considering adding a phylogenetic component to my research. He shared his research with me and engaged me in several interesting conversations about willow phylogenetics. Additionally, I would also like to acknowledge all of my peers who have given me feedback on my research, especially my lab group: Nicholas Deacon, Paul Gugger, Gina Quiram, Heather Whittington, Alyson Center and Xiaojing Wei. A critical part of working with willows was learning how to properly identify species in the field. I am greatly indebted to all of the people who assisted me with species identification and helped me locate willows both within Minnesota and in my travels. At Cedar Creek Ecosystem Science Reserve, I had the opportunity to spend time in the field with John Haarstad and Barabara Delaney. They both helped me learn my first willow species and showed me where multiple populations were within the reserve. John Haarstad always let me know when he came across new populations of different species and was a wealth of information about the site’s natural history. His presence at Cedar Creek is greatly missed. I also appreciate all the support I received from the staff and researchers that work at Cedar Creek. I am grateful i that I had the opportunity to work in such a wonderful location. In Minnesota, I also worked in several preserves managed by the Minnesota Department of Natural Resources, the Nature Conservancy and the Science Museum of Minnesota, including Helene Allison Savannah SNA, Boot Lake SNA, Savage Fen SNA, Black Dog Preserve SNA, Carlos Avery WMA and St. Croix Watershed Research Station. I appreciate all the support I received from these organizations over the last five years. I received substantial support from a variety of organizations, researchers and willow enthusiasts during my travels. In Arizona, I received assistance from the U.S. National Forest Service and worked with members of the Apache National Forest. I also had the amazing opportunity to work with Mr. Carl-Eric Granfelt, who has worked extensively with the willows in the region. I greatly appreciate the time he invested in helping me and will always appreciate his enthusiasm for the natural world. In Alaska, I collected willow samples at Bonanza Creek LTER. Everyone at the site was extremely helpful and it was incredibly helpful to have access to their equipment and facilities. I would especially like to thank Teresa and Jamie Hollingsworth for their support during my time in Fairbanks. In Oregon, I was able to collect willows with permission of the U.S. Bureau of Land Management. I also had the great opportunity to meet with Bruce Newhouse from Salix Associates (a great name for a company!). He helped me with my collections and also offered me a dry place to spend the night so that I could get away from all the rain. In Florida, I was able to collect samples in several state parks with permission from the Bureau of Parks District 2 Administration. While I was unable to use any of the plant collected in Mexico because of poor survival, I would like to thank Antonio Gonzalez-Rodriguez for collecting for me. I also appreciate George Argus for taking the time to meet with me and share his extensive knowledge about willow ecology and identification. My research would not have been possible without assistance from our lab managers and lab technicians. I would especially like to thank Kari Koehler, Annette Pahlich and Brianna Miles for all of their hard work and help in the lab and field. I would also like to thank Frank Hoerner for maintaining my large greenhouse experiment. I would not have been able to set up this experiment as smoothly without his help and input (and the support of his wife Penny). The greenhouse staff at the University of Minnesota has also helped me throughout my time here, especially keeping the pests at bay. Both in the lab and in the ii field, I received assistance from multiple students and interns. I would like to extend a special thanks to Cassandra Olson, Ethan Warner, Nicole Adams, Margaret Wright, Kali Rauk-Nelson and Victoria Rolfshus. I received financial support from the University of Minnesota (the Crosby Fellowship, the Brand Fellowship, the Doctoral Dissertation Fellowship and the Thesis Research Grant), the Plant Biology Department (Summer stipends and travel grants), the Bell Museum (Dayton-Wilkie Funds) and the National Science Foundation (LTER grant to the Cedar Creek Ecosystem Science Reserve (DEB: 0620652, JCB). Without this support, this research would not have been possible. Lastly, I would like to thank all my friends and family who supported me during the last five years, especially Dustin Haines, whose support and input has been instrumental in my completion of this research. I would also like to acknowledge Gail Kali and all of the staff in both the EEB and Plant Biology offices for helping me jump through all the hoops of applying for funding and completing my degree. iii Dedication I dedicate this dissertation to my grandparents because they laid the building blocks that made this possible, especially to my grandfather Arthur Brackett Hess (1923-2009) who really wanted to be here to see me graduate. iv Table of Contents List of Tables ……………………………………………………………………………………………..v List of Figures ……………………………………………………………………………………………vi Introduction Investigating the processes that influence willow species (genus: Salix ) distributions at two spatial scales……………..……………………………………………………………1 Chapter 1 Willow species with contrasting habitat affinities differ in their photoprotective responses to water stress……………………………………………………………………………...4 Chapter 2 Divergence in drought survival strategies of sympatric willow species……………..…..24 Chapter 3 Niche differentiation and the role of trait lability in the structuring of willow and poplar communities in Minnesota…………………………………………………………..…...51 Chapter 4 Photoperiod and timing of cold acclimation modify a trade-off between freezing tolerance and growth rate in the willow family (Salicaceae)………………………..…...92 Bibliography …………………………………………………………………………………………..129 Appendix 1 Supplemental material for Chapter 3……………………………………………….......143 Appendix 2 Supplemental material for Chapter 4 …………………………………………………..151 v List of Tables Table 1.1 Average chlorophyll fluorescence and gas exchange parameters of six willow species during a dry-down…………………………………………………………………………………….…17 Table 1.2 Average leaf pigment concentrations of six willow species during a dry-down……………....18 Table 2.1 Pre-drought traits of willow habitat generalists and wetland specialists……………………... 42 Table 2.2 Species-level drought responses of willow habitat generalists and wetland specialists……….43 Table 2.3 Traits that are the same and that differ between species with the same habitat affinities……..44 Table 3.1 Willow and poplar species, their typical habitats and their distributions across a water availability gradient in the study area…………………………………………………….……79 Table 3.2 Correlations between species composition and environmental variables based on NMS ordination analysis………………………………………………………………………….… 80 Table 3.3 Average plot and null model co-occurrence values for three indices……………………….... 81 Table 3.4 Species and guild niche overlap across a water availability gradient and a soil organic matter gradient…………………………………………………………………………………….…. 82 Table 3.5 Phenotypic clustering within field plots………………………………………………….……83 Table 3.6 Phylogenetic signal of phenotypic traits and niches……………………………………….…..84 Table 4.1 The 24 willow and poplar species in the freezing study and information on their collection sites………………………………………………………………………………………...... 118 Table 4.2 Description of freezing experiments ………………………………………………………....119 Table 4.3 Variation in species’ mortality in the tropical and temperate treatments………………...…..120 Table 4.4 Differences in the relationship between species’ native ranges and their growth rates in the tropical and temperate growth treatments………………………………………………….…121 Table 4.5 Evidence