Tropical rainforests getting their fix: The ecological drivers and consequences of nitrogen-fixing trees in regenerating Costa Rican rainforests Benton Taylor Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Graduate School of Arts and Sciences COLUMBIA UNIVERSITY 2018 © 2018 Benton Taylor All rights reserved ABSTRACT Tropical rainforests getting their fix: The ecological drivers and consequences of nitrogen-fixing trees in regenerating Costa Rican rainforests Benton Taylor Tropical rainforests have an unparalleled capacity to sequester carbon, harbor biodiversity, and cycle water and nutrients due to their high rates of primary production. The large biomass stocks and rapid regeneration rates of these forests are often attributed to ample soil nitrogen and quick recovery of the nitrogen cycle in tropical soils following disturbance. Symbiotic nitrogen-fixing trees, which are relatively abundant at tropical latitudes, have the greatest capacity to provide tropical rainforests with new nitrogen, yet the ecological drivers of tropical symbiotic nitrogen fixers and their effects on the forests they inhabit are not well understood. This dissertation consists of four chapters that examine the patterns, environmental controls, and ecological consequences of symbiotic nitrogen-fixing trees in regenerating and intact rainforests in the Caribbean lowlands of Costa Rica. In chapter 1, I use field sampling in a chronosequence of rainforest plots to show that symbiotic nitrogen fixation declines through succession despite increases in the basal area of nitrogen-fixing trees. Chapters 2 and 3 describe results from a controlled shadehouse experiment assessing the effects of light, soil nitrogen, and plant competition on nitrogen fixation rates and the growth and biomass allocation of nitrogen fixers and non-fixers. In chapter 2, I demonstrate that light regulates nitrogen fixation more strongly than soil nitrogen availability. This is a departure from the historical focus on soil nitrogen as the primary regulator of nitrogen fixation and has the potential to resolve longstanding paradoxes of tropical nitrogen cycling. In chapter 3, I show that nitrogen fixation provides some resistance to competitive effects from neighboring plants in nitrogen-limited conditions, and that nitrogen fixers in these conditions downregulate their fixation rates in the presence of a competitor. This chapter also demonstrates that nitrogen fixation does not represent a significant structural cost to the plant, as reduced root biomass of nitrogen fixers more than compensates for allocation to nodule production. Finally, in Chapter 4, I demonstrate that nitrogen-fixing trees in our chronosequence plots do not promote forest growth, as expected given their capacity to fertilize their neighbors, but rather inhibit forest growth because they are strong competitors. These chapters describe several unexpected findings – i.e. that light primarily drives nitrogen fixation and that nitrogen fixers slow forest growth – which provide new and important insight into the role that nitrogen-fixing trees play in the growth of Costa Rican rainforests. TABLE OF CONTENTS LIST OF FIGURES AND TABLES.............................................................................................. iii ACKNOWLEDGEMENTS ........................................................................................................... iv INTRODUCTION .......................................................................................................................... 1 CHAPTER 1: SUCCESSIONAL DYNAMICS OF NITROGEN FIXATION, NITROGEN AVAILABILITY, AND FOREST GROWTH IN REGENERATING COSTA RICAN RAINFORESTS .............................................................................................................................. 7 Abstract ........................................................................................................................................... 7 Introduction ..................................................................................................................................... 8 Methods......................................................................................................................................... 12 Results ........................................................................................................................................... 17 Discussion ..................................................................................................................................... 21 Figures and Tables ........................................................................................................................ 29 CHAPTER 2: LIGHT REGULATES SYMBIOTIC NITROGEN FIXATION MORE STRONGLY THAN SOIL NITROGEN AVAILABILITY ........................................................ 34 Abstract ......................................................................................................................................... 34 Introduction ................................................................................................................................... 35 Methods......................................................................................................................................... 35 Results ........................................................................................................................................... 36 Discussion ..................................................................................................................................... 38 Acknowledgments......................................................................................................................... 40 Figures and Tables ........................................................................................................................ 42 CHAPTER 3: TROPICAL NITROGEN-FIXING TREES RESPOND TO COMPETITION AND ENVIRONMENTAL CONDITIONS DIFFERENTLY DEPENDING ON THEIR ABILITY TO FIX NITROGEN ........................................................................................................................... 46 Abstract ......................................................................................................................................... 46 Introduction ................................................................................................................................... 48 Methods......................................................................................................................................... 52 Results ........................................................................................................................................... 57 Discussion ..................................................................................................................................... 61 Conclusions ................................................................................................................................... 65 Acknowledgements ....................................................................................................................... 65 Figures and Tables ........................................................................................................................ 67 i CHAPTER 4: NITROGEN-FIXING TREES INHIBIT GROWTH OF REGENERATING COSTA RICAN RAINFORESTS ................................................................................................ 75 Abstract ......................................................................................................................................... 75 Introduction ................................................................................................................................... 76 Methods......................................................................................................................................... 78 Results ........................................................................................................................................... 83 Discussion ..................................................................................................................................... 85 Conclusions ................................................................................................................................... 88 Acknowledgements ....................................................................................................................... 89 Figures and Tables ........................................................................................................................ 90 CONCLUSION ............................................................................................................................. 95 REFERENCES CITED ................................................................................................................. 99 APPENDIX 1: Supplementary Information for Chapter 1 ......................................................... 110 Supplementary Methods ............................................................................................................. 110 Supplementary Tables and Figures ............................................................................................. 115 APPENDIX 2: Supplementary Information for Chapter 2 ......................................................... 129 Supplementary Methods ............................................................................................................