Persistence of Corals in Marginal Habitats: the Role of the Environment, and Symbiont Diversity and Ecophysiology

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Persistence of Corals in Marginal Habitats: the Role of the Environment, and Symbiont Diversity and Ecophysiology Persistence of corals in marginal habitats: the role of the environment, and symbiont diversity and ecophysiology Laura Caroline Wicks A thesis submitted to Victoria University of Wellington in fulfillment of the requirements for the degree of Doctor of Philosophy in Science 2009 Abstract Abstract Many corals live in marginal habitats, close to their survival thresholds of water temperature, light penetration and aragonite saturation. Living under these highly variable and extreme conditions is likely facilitated by specific physiological adaptations and/or the presence of unique species of coral and their symbionts but data on these factors are limited. The specific objectives of the study were to: (1) examine the diversity and distribution patterns of corals in marginal environments, (2) investigate the diversity, distribution patterns and host specificity of symbionts in corals in marginal environments, (3) assess the influence of environmental variables on host and symbiont distribution in marginal environments, in comparison to ‘optimal’ environments, and (4) examine the physiological responses to changing environmental conditions and stress of corals and their symbionts in marginal environments. Surveys of coral community patterns were conducted at the Kermadec Islands (KI), New Zealand, and Palmyra Atoll, USA, with local scale environmental parameters (i.e. wave exposure and sedimentation) found to control the diversity and distribution of the coral communities. Symbiodinium types were identified to sub- cladal level in a range of coral species at each of the survey sites, using ITS2-DGGE. A high diversity of C type symbionts (19 types in 13 host genera), and reduced host specificity was observed at the high latitude site of Lord Howe Island (LHI), Australia, with similarly high diversity at the KI (10 types in 9 genera). Thirteen novel clade C types were identified in corals at LHI, with two of these types also present in hosts at the KI. The reduced host specificity of symbionts at LHI, II Abstract compared to tropical sites, implies that the evolution of novel holobionts may be an important mechanism whereby corals can cope with variable and stressful conditions. Further, physiological assessment of the novel LHI symbionts led to the suggestion that Symbiodinium at LHI may be specialised for cooler and more variable temperatures, so contributing to the success of corals at this marginal location. In contrast, a low diversity of generalist symbionts (C and D types) were uncovered at the equatorial site of Palmyra Atoll (10 types in 13 genera), attributed to the stressful environmental regime resulting in a reduced population of stress- tolerant symbionts. The variation in environmental parameters, particularly sedimentation, around Palmyra Atoll has led to diversification of coral communities, however this environmental variation has not affected the symbiont communities. While it has been suggested that marginal coral communities might be better adapted for survival in an environment modified by global climate change, the local scale environmental factors are also important drivers of both coral and symbiont distributions, and should be considered when making predictions for the future. Further, assessment of the physiological tolerance ranges of both the multiple, novel symbionts at high latitudes, and the few, potentially stress-tolerant symbionts at Palmyra should be conducted, to help determine whether they have the ability to adjust to new environmental conditions. III Contributions Contributions and publications This thesis is written as a series of manuscripts, which are in the review process or to be submitted in the near future. All field-work, lab-work and writing were conducted by the Author, with expections as below. Chapter 2 This chapter has been submitted for publication to the Marine Ecology Progress Series, and is in review. Sample collection was undertaken by JPA Gardner and J Long, of Victoria University of Wellington. Chapter 3 The molecular work in this chapter was assisted by Dr Eugenia Sampayo, of The University of Queensland. Figure 3.3 was designed by Dr Sampayo, and made editorial comments on the text. Chapter 5 The design and implementation of this study was aided by Dr Ross Hill of The University of Technology, Sydney. Dr Hill also made editorial comments on the text II Acknowledgements Acknowledgements There are many people that I would like to thank for their invaluable support, both academically and personally, that made the completion of this thesis possible. I would like to thank everyone that has aided me in this journey; if I have forgotten anyone I apologise. Foremost, I would like to thank my supervisor Dr Simon Davy for his continual support and insightful suggestions in the last three and a half years. Simon was always there to listen and give feedback, despite his busy schedule, and this thesis would not have existed without him. I would also like to thank my second supervisor Dr Jonathan Gardner, who not only was there with help and support when required, but also gave me the amazing opportunity to conduct research at Palmyra Atoll, an indescribable experience. I am also grateful to the collaborators on two of my projects, Dr Eugenia Sampayo and Dr Ross Hill, and their supervisors, Prof Ove Hoegh-Guldberg and Dr Peter Ralph for allowing me to work in their labs and monopolise their post-docs’ time. Additionally, I am indebted to all the people who lent me support and expertise in the lab, namely Dr Tyrone Ridgway, Dr Jo Zuccarello. Dr Ann Wood, Kristen Westfall, and Pelayo Salinas de Leon. I wish to thank my lab group, for both their support and the constant reminder that, although my lab-work was testing at the best of times, I could have been cleaning anemones! In particular, for their kind assistance with fieldwork, I wish to thank Dr Jo Davy, Dan Logan and Gareth Williams. Additional thanks goes to Gareth for his stats advice and expertise, and his true gentlemanly behaviour in the face of a tiger shark. III Acknowledgements Many people outside VUW assisted with the fieldwork component of my studies. For their contribution to my Lord Howe Island work, thanks go to Ian Kerr and Sallyann Gudge of Lord Howe Island Marine Parks Authority, Tas Douglass, Lauren Gatherer, Brian ‘Busty’ Busteed, Dr Peter Harrison and Dr Carden Wallace. For field assistance at Palmyra Atoll, I thank the staff of The Nature Conservancy, particularly Roseanne for her quick thinking in the tiger shark episode. For permits I wish to thank NSW Marine Parks Authority, US Fish and Wildlife Services, and the Department of Conservation, New Zealand. For funding, I acknowledge the Commonwealth Scholarship scheme, New Zealand Postgraduate Study Abroad, Project Aware, Australian Geographic, the British Ecological Society, and finally Victoria University of Wellington for their research funding, faculty grant and submission scholarship. During my PhD, I have appreciated the presence of many good friends, in particular Anna Smith who shared with me the ups and downs, and many bottles of wine. I also wish to thank Jade Berman, Emily Dicks and the rest of my office buddies, for their support through the hard times, and fun times beside. Jessie and Peter Bakker receive special thanks for providing me with a happy home on multiple occasions, with many memorable nights out and in. The writing up period was always going to be a challenge, but Chrissie and Brian Stuart-Nairne made the experience an enjoyable one, giving me a home in beautiful surroundings, and thus enabling me to keep my sanity at the same time as writing my thesis. I have to mention the mischievous antics of their Goldies, Bobby and Madge; Bobby especially made me laugh on more occasions than I thought possible during my PhD. IV Acknowledgements Lastly, and most importantly I need to thank the people to whom I dedicate this thesis, my parents and sisters, and Brett. Thank you mum and dad, not only for your financial support in times of crisis (and non-crisis!), but mainly for your emotional support and your faith in me over these long years. Despite the time difference, those weekly phone calls from home, and sporadic texts from Soph made me feel part of a wonderful family, even at such a distance. And finally to my partner Brett, I owe the greatest thanks. It cannot have been easy to have a girlfriend in a different country, let alone one doing a PhD, but you stuck with me through the hard times, made me smile when times were bad, and I am looking forward to all the good times yet to come. V List of Figures Table of contents Abstract II Contributions and publications II Acknowledgements III Table of contents VI List of Figures XI List of Tables XIV List of abbreviations XVI Glossary of terms XVIII Chapter 1 - 1 - General Introduction - 1 - 1.1 Corals and symbiosis - 1 - 1.2 Genetic diversity of Symbiodinium - 4 - 1.3 Host-symbiont specificity and flexibility - 9 - 1.4 Biogeographic and ecological variability of Cnidarian-Symbiodinium partnerships - 12 - 1.5 Physiological variability and susceptibility to environmental stress - 14 - 1.6 Photophysiology of Symbiodinium - 17 - 1.7 Corals in marginal environments - 20 - 1.8 Symbiodinium in marginal environments - 25 - 1.9 Objectives - 26 - VI List of Figures Chapter 2 - 30 - Spatial patterns and regional affinities of coral communities at the Kermadec Islands Marine Reserve (New Zealand), a marginal high-latitude site - 30 - ABSTRACT - 30 - 2.1 INTRODUCTION - 31 - 2.2 Materials and Methods - 35 - 2.2.1 Study area - 35 - 2.2.2 Sampling - 35 - 2.2.3 Regional affinities - 37 - 2.2.4 Data analysis - 38 - Kermadec Islands - 38 - Regional affinities - 39 - 2.3 RESULTS - 40 - 2.3.1 Kermadec Islands - 40 - 2.3.2 Regional affinities - 45 - 2.4. DISCUSSION - 49 - 2.4.1 Kermadec Islands - 49 - 2.4.2.
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