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Wall Hawii 0085A 10315.Pdf ENVIRONMENTAL AND BIOLOGICAL EFFECTS ON NUTRITIONAL MODE AND RESOURCE PARTITIONING IN SCLERACTINIAN CORALS A DISSERTATION SUBMITTED TO THE GRADUATE DIVISION OF THE UNIVERSITY OF HAWAI‘I AT MĀNOA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY IN MARINE BIOLOGY May 2019 By Christopher B. Wall Dissertation Committee: Megan Donahue, Chairperson Anthony Amend Amy Moran Brian Popp Christopher Sabine Keywords: Corals, Isotopes, Symbiodiniaceae, Energetics, Nutrition, Climate Change © 2019 Christopher B. Wall ALL RIGHTS RESERVED ii DEDICATION For my family and our times together by the ocean that set me on this path iii ACKNOWLEDGEMENTS I am eternally thankful for my family and their investments in my life and career. To the Walls and Colemans and inlaws Wesleys and Holmes: I am fortunate to have you all in my life and in my heart. To my wife Megan: your support for me has been unyielding. It has survived long tours, longer field seasons, and our shared world travels. You inspire me; you make life beautiful. This accomplishment is ours, together. To my daughter Alana Jane: your love of the ocean rekindles my own fascination with nature. There is nothing in this world I enjoy more than being your father. To my mother Jane: I wish you could have seen the last twenty years come together. I know you were watching, holding your breath in anticipation. To my father James: your extraordinary journey through life has been a constant reminder that adversity and tribulations are speed bumps, not road blocks, and commitment and hard work pay off. Thank you for instilling in me the value of self-reliance, plus a bit of bullheadedness. To my grandmother Geneva: your love of nature made me a botanist prior to being a marine biologist. Thank you for teaching me to appreciate the serenity of a garden and the study of plants. To my brother Matthew and my sister-in-law Jennifer, I am exceptionally proud of you both and love your enduring curiosity and passion for learning. Matthew, thank you for being my confidant, sounding board, and best friend through smooth and rough seas; the quest lives on. To my advisor, Dr. Ruth Gates: Ruth, I wish we could have crossed the finish line together. I am grateful for your optimism, your energy, and the opportunity to have worked with you and learned from you. I am grateful for my committee – Dr. Megan Donahue, Dr. Brian Popp, Dr. Amy Moran, Dr. Anthony Amend, Dr. Chris Sabine – for their contributions to my training and for the fruitful discussions and intellectual challenges provided along the way. I appreciate the iv time you spent guiding and consulting me in my research over the past size years. In particular, Megan Donahue, thank you for taking me under your wing and keeping me on path during a hard time; and Brian Popp, thank you for sharing your expertise and insights on stable isotopes (and introducing me to the extended IsoCamp hui), and always having your door open to an isotope neophyte. Your mentorship has been invaluable. To my mainland and island ohana, I am blessed beyond words to have you all in my life. The best memories of my Ph.D. are thost spent with you – sharing stories and laughs around a grill, by the water, or in the surf. To my extended scientific family – The Ruth Gates Coral Lab, The Megan Donahue Lab, and the Peter Edmunds Polyp Lab – thank you all for the training, experience, and friendships that carried me through this journey. In particular, thank you Peter Edmunds, Hollie Putnam, Ross Cunning, Raphael Ritson-Williams, Crawford Drury, John Burns, Maggie Sogin, Robert Mason, Beth Lenz, Shayle Matsuda, Ariana Huffmyer, Carlo Caruso, Mariana Rocha de Souza for the fruitful discussions, Jen Davidson, Kira Hughes, and invaluable assistance of undergraduate scholars (William Ellis, Mario Kaluhiokalani, Alexandra Wen, Kelly Wyrick, Pansa Cecchini) for logistical support in pursuit of my dissertation research. v ABSTRACT Reef corals are threatened by climate change. Increasing atmospheric CO2 has resulted in ocean acidification (OA) and ocean warming, which contribute to reductions in coral growth and to widespread coral bleaching events. The resilience of coral reef ecosystems to climate change fundamentally relies on the physiological resilience of reef corals to environmental change. Coral resilience may be supported by (i) biomass reserves, (ii) the capacity to switch feeding modes from autotrophy to heterotrophy, and (iii) the flexibility to associate with stress tolerant endosymbionts (Family: Symbiodiniaceae). To better understand the physiological response of corals to natural and human-induced environmental stress, I used a combination of laboratory and field studies to examine the tradeoffs in these three aspects of coral physiological resilience under ocean acidification stress, bleaching and post-bleaching recovery, and light limitation. First, under ecologically relevant irradiances, the coral Pocillopora acuta does not exhibit OA- driven reductions in calcification as reported for other corals. Instead, reductions in biomass reserves suggest that OA induced an energetic deficit and contributed to the catabolism of tissue biomass. Second, coral bleaching had extensive effects on the biomass of Montipora capitata and Porites compressa, and isotope mass balance revealed that changes in coral δ13C values were best explained by changes in tissues (proteins:lipids:carbohydrates) not a greater reliance on heterotrophy during bleaching or recovery. Finally, M. capitata-Symbiodiniaceae holobionts exhibited distinct traits and δ13C isotope values that differed between seasons and were modulated by light-availability. δ13C isotopic values did not reveal changes in nutritional modes, but instead suggest lower rates of carbon fixation/translocation by the symbiont Durusdinium, in agreement with laboratory studies identifying Durusdinium as an opportunist symbiont providing vi less nutritional benefit to the host. Together, my research provides insights into the complex consequences of environmental change on reef-building corals. Moreover, physiological tradeoffs that underlie coral resilience may mask the full effects of climate stressors on coral reefs. My work highlights the need for future research to consider (i) energetic costs and growth tradeoffs, (ii) biomass compound-specific isotope values, (iii) and the role of seasonality and (iv) symbiont community effects. vii TABLE OF CONTENTS ACKNOWLEDGEMENTS…………………………………………………………………. iv ABSTRACT…………………………………………………………………………………. vi LIST OF TABLES AND APPENDICES……………………………………………………. x LIST OF FIGURES………………………………………………………………………….. xi CHAPTER 1…………………………………………………………………………………. 1 Conclusions………………………………………………………………………….. 11 CHAPTER 2………………………………………………………………………………… 13 Abstract……………………………………………………………………………… 14 Introduction……………………………………………………………………….…. 15 Materials and Methods………………………………………………………………. 18 Results……………………………………………………………………….………. 25 Discussion…………………………………………………………………………… 27 Funding………………………………………………………………………………. 35 Acknowledgements………………………………………………………………….. 36 CHAPTER 3………………………………………………………………………………… 45 Abstract……………………………………………………………………………… 46 Introduction……………………………………………………………………….…. 47 Materials and Methods………………………………………………………………. 51 Results……………………………………………………………………….………. 59 Discussion…………………………………………………………………………… 65 Funding………………………………………………………………………………. 74 Acknowledgements………………………………………………………………….. 74 viii CHAPTER 4………………………………………………………………………………… 87 Abstract……………………………………………………………………………… 88 Introduction……………………………………………………………………….…. 89 Materials and Methods………………………………………………………………. 92 Results……………………………………………………………………….………. 100 Discussion…………………………………………………………………………… 105 Funding……………………………………………………………………………… 119 Acknowledgements…………………………………………………………………. 119 CHAPTER 5………………………………………………………………………………… 128 MANUSCRIPT PUBLICATION AND OTHER ACKNOWLEDGEMENTS…………….. 139 APPENDICES……………………………………………………………………………….. 141 REFERENCES………………………………………………………………………………. 165 ix LIST OF TABLES Table 2.1. Summary of selected works testing pCO2 and light treatments on coral calcification using single irradiances and multiple irradiances Table 2.2. Summary of environmental conditions in the experimental treatment tanks between 16 December 2014 and 16 January 2015. Table 2.3. Summary of p-values for pCO2 and light effects on principal component loadings and response variables normalized to skeletal area and tissue biomass. Table 3.1. Statistical analysis of bleached and non-bleached Montipora capitata and Porites compressa at three Kāne‘ohe Bay patch reefs during bleaching and recovery. Table 3.2. Analysis of environmental variables (dissolved inorganic nutrients, sedimentation rates, daily light availability, and temperature) at three Kāne‘ohe Bay patch reefs. Table 3.3. δ15N-nitrate values of seawater collected from three patch reefs in Kāne‘ohe Bay, O‘ahu, Hawai‘i. Table 3.4. Permutational multivariate analysis of variance (PERMANOVA) of bleached and non-bleached Montipora capitata and Porites compressa at three reefs during bleaching and recovery. Table 4.1. Statistical analysis of Montipora capitata host and symbiont physiology and tissue isotope values from four locations in Kāne‘ohe Bay along a depth gradient in summer and winter. x LIST OF FIGURES Figure 2.1. Principal component analyses (PCA) for energy reserves and net calcification normalized to skeletal surface area (cm-2) and tissue biomass (gdw-1). Figure 2.2. Net calcification, total biomass, photopigment concentrations, and symbiont densities
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