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University of Southampton Research Repository Eprints Soton University of Southampton Research Repository ePrints Soton Copyright © and Moral Rights for this thesis are retained by the author and/or other copyright owners. A copy can be downloaded for personal non-commercial research or study, without prior permission or charge. This thesis cannot be reproduced or quoted extensively from without first obtaining permission in writing from the copyright holder/s. The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the copyright holders. When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given e.g. AUTHOR (year of submission) "Full thesis title", University of Southampton, name of the University School or Department, PhD Thesis, pagination http://eprints.soton.ac.uk UNIVERSITY OF SOUTHAMPTON FACULTY OF ENGINEERING, SCIENCE AND MATHEMATICS SCHOOL OF OCEAN AND EARTH SCIENCE ACCLIMATION AND PHENOTYPIC PLASTICITY OF ECHINODERM LARVAE IN A CHANGING OCEAN by Nadia Elisa Suárez Bosche Thesis for the degree of Doctor of Philosophy January 2011 A mis padres Mario Cesar Suárez-Arriaga & Elke Amanda Bosche Gracias a Ustedes con su apoyo, ejemplo y cariño este sueño fue posible SCHOOL OF OCEAN AND EARTH SCIENCE NATIONAL OCEANOGRAPHY CENTRE This PhD dissertation by Nadia Elisa Suárez Bosche has been produced under the supervision of the following persons Supervisors: Dr. Debora Iglesias-Rodriguez Prof. Paul Tyler UNIVERSITY OF SOUTHAMPTON ABSTRACT FACULTY OF ENGINEERING, SCIENCE AND MATHEMATICS SCHOOL OF OCEAN AND EARTH SCIENCE Doctor of Philosophy ACCLIMATION AND PHENOTYPIC PLASTICITY OF ECHINODERM LARVAE IN A CHANGING OCEAN Nadia Elisa Suárez Bosche Echinoderms are keystone organisms that have representatives in virtually every marine ecosystem. They possess a number of features that makes them an excellent model system, namely 1) their susceptibility to changes in the chemistry of seawater and temperature 2) their ossified skeletons are major contributors to many carbonate formations 3) their variety of life history strategies that enable successful reproduction (e.g. asexual reproduction, fission, cloning and regeneration). In most parts of the ocean, CO2 and temperature co-vary, making it difficult to extrapolate isolated effects of any one variable to natural scenarios. Laboratory and field work was conducted to assess the physiological and biogeochemical response of sea urchin Psammechinus miliaris larvae to changes in water carbonate chemistry. This study used two approaches: 1) the incubation of the larvae with naturally CO2-enriched deep-seawater, and 2) the study of the effect of ocean acidification and ocean warming. It is reported that there was no effect of in situ naturally high CO2 seawater, or laboratory induced CO2 concentrations, on larval physiology or morphology. However, elevated CO2 was found to cause a decrease in fertilization and calcification. An increase in temperature appeared to counteract significantly the negative effect that high CO2 has on fertilization and biocalcification. Therefore, it is argued that the developmental stages of sea urchins may adapt to predicted ocean acidification and increasing temperature scenarios, which is advantageous to maintaining stability and survival of populations under environmental selection pressure. Furthermore, the regeneration capability of the Pacific seastar larvae Pisaster ochraceus and Orthasterias koehleri was investigated. The successful complete re-growth of the larvae can be considered a specific developmental strategy that facilitates the species’ survival. This research suggests that echinoderm larvae are resilient to conditions in a changing ocean, due to their high acclimation capabilities and to their reproduction life history strategies. In this context, echinoderms may be considered an evolutionary success. i ii CONTENTS Abstract i Table of contents iii List of figures ix List of tables xiii Abbreviations xv Declaration xvii Acknowledgments xix CHAPTER ONE: INTRODUCTION, AIMS AND OBJECTIVES 1 1.1 Project summary 3 1.2 General background and theory 3 1.2.1 The carbonate system 5 1.2.2 Dissolved inorganic carbon 5 1.2.3 Alkalinity 6 1.2.4 pH 7 1.2.5 pCO2 7 1.3 The effects of ocean acidification on calcifying organisms 8 1.3.1 The relevance of Psammechinus miliaris 9 1.4 Echinoderms 10 1.4.1 Why study echinoderms? 10 1.4.2 Reproductive system 11 1.4.3 Echinoid larvae 11 1.4.4 Fertilization and larval development 12 1.4.5 Asteroidea larvae 15 1.4.6 Regeneration in Asteroids 17 1.5 Key aims and objectives 19 1.6 Structure of the thesis 20 iii CHAPTER 2: THE PHYSIOLOGICAL TOLERANCE OF THE SEA URCHIN SPECIES PSAMMECHINUS MILIARIS TO HYPERCAPNIC CONDITIONS 23 2.1 Introduction 25 2.2 Materials and methods 27 2.2.1 Study organism and exposure to stressors 27 2.2.2 Scanning electron microscopy of larval skeletons 28 2.2.3 Carbonate chemistry system and experimental design 29 2.2.4 Particulate carbon analyses 31 2.2.5 Statistical analyses 31 2.3 Results 32 2.3.1 Experimental seawater carbonate chemistry 32 2.3.2 Effects on fertilization 32 2.3.3 Effects on larval growth under hypercapnic conditions 33 2.3.4 The effect on feeding structures of the larvae under hypercapnic conditions 36 2.3.5 Larval skeleton 36 2.4 Discussion 38 2.4.1 Fertilization success under ocean acidification conditions 38 2.4.2 Larval growth, development and calcification 39 2.4.3 Calcification of echinoplutei larvae 40 2.4.4 Conclusions 42 CHAPTER 3: THE ACCLIMATION OF ECHINODERM LARVAE TO CO2- ENRICHED DEEP OCEAN WATERS 43 3.1 Introduction 45 3.2 Material and methods 48 3.2.1 Study site 48 iv 3.2.2 Experimental conditions 48 3.2.3 Fertilization and larval culture 48 3.2.4 Larval development and morphology 49 3.2.5 Particulate carbon analyses 50 3.2.6 Natural seawater carbonate chemistry 50 3.2.7 Calculation and representation of Ω-Cal from the WOCE A16 transect line 51 3.2.8 Scanning electron microscopy 53 3.2.9 Natural seawater elemental composition 53 3.2.10 Statistical analyses 53 3.3 Results 54 3.3.1 Natural seawater carbonate chemistry analyses 54 3.3.2 Fertilization and larval development 56 3.3.3 Particulate carbon and calcification 57 3.4 Discussion 59 3.4.1 Physiological response of P. miliaris to CO2-enriched deep seawaters 59 3.4.2 Particulate carbon and calcification 59 3.4.3 The effect of seawater composition on larval development 60 3.4.4 Evolutionary adaptation to the deep-sea 60 CHAPTER 4: TEMPERATURE COUNTERACTS OCEAN ACIDIFICATION EFFECT ON FERTILIZATION AND BIOCALCIFICATION OF SEA URCHIN LARVAE UNDER CLIMATE CHANGE SCENARIOS 63 4.1 Introduction 65 4.2 Materials and methods 68 4.2.1 Experimental conditions and rearing 68 4.2.2 Morphological analysis 69 4.2.3 Carbonate chemistry analysis 70 4.2.4 Particulate carbon 73 4.2.5 Scanning electron microscopy (SEM) of larval skeletons 73 v 4.2.6 Statistical analyses 73 4.3 Results 74 4.3.1 Carbonate chemistry 74 4.3.2 Fertilization and mortality 74 4.3.3 Larval growth and development 75 4.3.4 Particulate carbon 78 4.4 Discussion 80 4.4.1 Fertilization success under ocean acidification and ocean warming 80 4.4.2 Calcification of Psammechinus miliaris under environmental climate change scenarios 83 4.4.3 Conclusions 86 CHAPTER 5: GROWING HALF OF THE BODY: DEVELOPMENT OF THE NERVOUS SYSTEM DURING REGENERATION IN SEASTAR LARVAE 87 5.1 Introduction 89 5.1.1 Regeneration 89 5.1.2 The echinoderm larval nervous system 90 5.2 Materials and methods 91 5.2.1 General description 91 5.2.2 Immunofluorescence protocol 92 5.2.3 Application of Stokes’ theorem to estimate irregular areas 93 5.2.4 Volume estimation 94 5.2.5 Statistical analyses 95 5.3 Results 95 5.3.1 Regeneration of seastar larvae after bisection 95 5.3.2 The larval nervous system in seastars 98 5.3.3 Nervous system during regeneration 100 5.4 Discussion 103 5.4.1 Ontogenesis during regeneration 104 5.4.2 Neurogenesis during regeneration 105 vi 5.4.3 Conclusions 108 CHAPTER 6: GENERAL DISCUSSION 109 6.1 Project summary 111 6.2 Fertilization success in near-future levels of ocean acidification and ocean warming 114 6.2.1 Summary of findings 114 6.2.2 Implications 114 6.3 Mortality rates in near-future levels of ocean acidification and ocean warming 115 6.3.1 Summary of findings 115 6.3.2 Implications 115 6.4 Larval growth and development of Psammechinus miliaris 117 6.4.1 Summary of findings 117 6.4.2 Implications 118 6.5 Changes to calcification rates of Psammechinus miliaris under CO2-induced ocean acidification and ocean warming 120 6.5.1 Summary of findings 120 6.5.2 Implications 120 6.6 Development of the nervous system during regeneration in seastar larvae 121 6.6.1 Summary of findings 121 6.6.2 Implications 122 6.7 Limitations and uncertainties 122 6.7.1 Differences in experimental organisms and seawater conditions 122 6.7.2 Experimental set-up and organism manipulation 123 6.7.3 Limitations of field experimentation 123 6.7.4 New protocol development 124 CHAPTER 7: FINAL CONCLUSIONS AND RECOMMENDATIONS FOR FURTHER RESEARCH 125 vii 7.1 Final conclusions 127 7.1.1 Ocean acidification, changes in carbonate chemistry, the effect of temperature/CO2 interactions and their impact on the development of sea urchin larvae Psammechinus miliaris 127 7.1.2 A study of the nervous system of the seastar larvae Pisaster ochraceus and Orthasterias koehleri during regeneration 129 7.2 Recommendations for further research 129 7.2.1 The effect of changes in carbonate chemistry on the development of sea urchin larvae P.
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