NORTHWESTERN UNIVERSITY Using Trees to Seed Prairies: Incorporating Phylogenetic Information to Guide Tallgrass Prairie Restoration A DISSERTATION SUBMITTED TO THE GRADUATE SCHOOL IN PARTIAL FULFILLMENT OF THE REQUIREMENTS for the degree DOCTOR OF PHILOSOPHY Field of Plant Biology and Conservation By Rebecca Samantha Barak EVANSTON, ILLINOIS June 2017 2 ABSTRACT Ecological restoration is vital to the conservation of biodiversity and provision of ecosystem services in a changing world. Biodiversity is often a goal of restoration, and species to be planted for restoration are often selected based on diversity objectives. But species are not independent; they are related to one another through the evolutionary tree of life. Species’ positions on the phylogenetic tree can reflect their traits. How broadly species in a community are drawn from across the tree can predict ecosystem function. I studied the role of evolutionary history and diversity in restoration of the tallgrass prairie. Prairies are one of the most endangered ecosystems on earth, and they have been an intensive focus of ecological restoration throughout the history of the field. In chapter 1, I describe how restoration can be informed by historical ecological information like recorded, archeological, paleoecological, and evolutionary data. These “long view” persectives can provide context for better understanding contemporary ecosystems, and can contribute to goal setting, management, and monitoring for restoration. Phylogenetic diversity specifically can inform restoration because it is a strong predictor of ecosystem functions that are also key restoration objectives, like stability, productivity, support of higher trophic levels, and invasion resistance. Phylogenetic information can also be useful for understanding how restored sites compare to remnant habitats that serve as reference sites for restoration. In chapter 2, I found that restored prairies have lower phylogenetic diversity than remnant prairies, in addition to differing in species richness and community composition. These differences may occur because restored 3 prairies are subject to higher levels of disturbance than remnants, and because species seeded to establish restored prairies are more closely related than expected by chance. I identified “missing branches” – clades found in remnant prairies, but absent from restoration seed mixes – that could be planted in restorations to increase their compositional and functional equivalency to reference systems. Increasing biodiversity of restored prairies depends on an understanding of how seeds germinate and establish to build restored plant communities. Seed traits, which are understudied relative to vegetative plant traits, are critical for understanding assembly of restored communities. In chapter 3 I tested the effects of seed traits, phylogenetic position, and germination pre-treatment on germination response in species commonly used in prairie restoration. I found that seed traits, particularly shape variables, predicted germination response. Phylogenetic position was also an important predictor of germination, indicating that the phylogeny may supply information that is integrative over many traits, both measured and unmeasured. Seeds come together to form seed mixes, the raw materials of prairie restoration. Seed mix design is motivated by objectives related to biodiversity and ecosystem function, but also by economic constraints. In chapter 4 I studied biodiversity of commercially available seed mixes, in terms of species richness, conservatism, and phylogenetic diversity, and compared commercial mixes to restored and remnant prairies. I also tested whether price was predictive of biodiversity in commercial mixes. I found that commercial mixes were generally less diverse than remnant prairies, but similar in diversity to extant restored prairie communities. Lastly, I found that seed mix price was predictive of multiple measures of biodiversity. 4 ACKNOWLEDGEMENTS Most sincere thanks to my dissertation advisor, Dan Larkin. Your mentorship in all things is helping me become the scientist I aspire to be. Thank you to my doctoral committee, Kay Havens, Andrew Hipp, Andrea Kramer, and Jack Pizzo, for your insight. I am not saying goodbye, because I look forward to working with all of you in the future. Thank you to the fantastic research assistants I have had the pleasure of working with during my doctoral studies: Gabriella Carr, Meghan Kramer, Taran Lichtenberger, Jessica Riebkes, Robert Sherman, and Alyssa Wellman-Houde. Extra special thanks to Taran for measuring literally thousands of seeds. Thanks to Evelyn Williams for being my co-head-counselor for Camp Prairie Phun. Thanks also to the Larkin lab, the Kramer-Havens lab, and the ladies of community ecology for their constant support and insight. Thank you to the following people for access to and information about restored prairies and species used in this dissertation: Kyle Banas, Dawn Banks, Trish Burns, Jenny Clauson, Pat Hayes, Erick Huck, Keith Guimon, Jack Pizzo, Nagulapalli Rao, Cassi Saari, Sue Swithin, Byron Tsang and Lauren Umek. Thank you to the Program in Plant Biology and Conservation, the Illinois Association for Environmental Professionals, the Society for Ecological Restoration, Midwest-Great Lakes Chapter, and The Dr. John N. Nicholson fellowship from Northwestern University, and National Science Foundation awards DEB-1354426, DEB-1354551 and DBI-1461007 for financially supporting this research. 5 Thank you to my family for their support throughout graduate school. Yuval, you are the best partner I could ever ask for. Boaz and Oren, you are the absolute joys of my life. To my parents, Karen and Hanoch Barak, you have always believed that I could do anything. Your massive, constant support (and hours and hours of babysitting) made this work possible. Thank you to my network of family and friends for all the love, and for indulging me when I just want to talk to you about plants. 6 DEDICATION This dissertation is dedicated to my grandmother, Shirley Oppenheim, and my grandmother-in- law, Janice Cohn. They sow seeds of wisdom and generosity that will bear fruit for generations to come. And To the land stewards and managers that restore and conserve the tallgrass prairie ecosystem. 7 TABLE OF CONTENTS 1 Title page 2 – 3 Abstract 4 – 5 Acknowledgements 6 Dedication 7 Table of contents 8-9 List of tables and figures 10 – 36 Chapter 1- Taking the long view: Integrating recorded, archeological, paleoecological, and evolutionary data into ecological restoration 37 – 56 Chapter 2 - Restored tallgrass prairies have reduced phylogenetic diversity compared with remnants 57 – 72 Chapter 3 - Cracking the case: seed traits, phylogeny, and seed pre-treatments drive germination in tallgrass prairie species used for ecological restoration 73 – 85 Chapter 4 - Shopping for a prairie: species richness, conservatism, and phylogenetic diversity of commercially available seed mixes for restoration 86 – 91 Dissertation summary and implications for management 92 – 114 Tables and figures 115 – 142 Literature cited 143 – 166 Appendix 1 - Supplementary material from chapter 2 167 – 170 Appendix 2 – Supplementary material from chapter 3 8 LIST OF TABLES AND FIGURES Chapter 1 92 – 93 Table 1.1 - Restoration questions that could be addressed by data from different temporal scales 94 Figure 1.1 - Historical timescales and their potential contributions to ecological restoration 95 Figure 1.2 - Vegetation changes at 100-yr intervals over the past 1200 years in Wisconsin sand plain 96 Figure 1.3 - Conceptual framework for the placement of traits according to their ecological and evolutionary structure Chapter 2 97 Figure 2.1 - Site and plot diversity metrics for species richness, species richness with non-native species excluded, and standard effect sizes for mean pairwise distance (MPD), and mean nearest taxon distance (MNTD) 98 Figure 2.2 - Non-metric dimensional scaling ordinations of remnant and restored prairies and seed mixes, based on community taxonomic and phylogenetic ordinations: mean pairwise distance (MPD), and mean nearest taxon distance (MNTD) 99 Figure 2.3 - Taxonomic and phylogenetic diversity of seed mixes and resultant prairie communities for only species planted at each site, for species richness, standard effect sizes of mean pairwise distance, and mean nearest taxon distance 100 Figure 2.4 - Planted (green) and unplanted (grey) species are indicated on the phylogeny containing all species found at remnant and restored sites and seed mixes (n = 589) Chapter 3 101 – 102 Table 3.1 - Species included in the experiment, and final percent germination under three pre-treatments: cold stratification, gibberellic acid and an untreated control 9 103 Table 3.2 - Best models of time-to-germination ranked by Akaike information criterion (AIC) for 32 prairie species 104 Table 3.3 - Model-averaged estimate, standard error, and 95% confidence interval (CRI) for all parameters in best fitting models (∆AIC ≤ 4) for 32 prairie species. 105 Table 3.4 - Phylogenetic signal of measured traits 106 Figure 3.1 - Ordination of phylogenetic distance matrix for 32 species in the study 107 Figure 3.2 - Time-to-event curves for all species by germination treatment 108 – 109 Figure 3.3 - Phylogenetic tree of species used in the experiment and phylogenetic distribution of trait values representing seed size (mass), shape (width) and embryo traits (ESlength) 110 Figure 3.4 - Estimates from averaged models (table