A Study of Marine Benthic Algae Along a Natural Carbon Dioxide Gradient
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A STUDY OF MARINE BENTHIC ALGAE ALONG A NATURAL CARBON DIOXIDE GRADIENT by VIVIENNE R JOHNSON A thesis submitted to Plymouth University in partial fulfilment for the degree of DOCTOR OF PHILOSOPHY School of Biomedical & Biological Sciences Marine Biology & Ecology Research Centre (MBERC) October 2012 1 This copy of the thesis has been supplied on condition that anyone who consults it is understood to recognise that its copyright rests with its author and that no quotation from the thesis and no information derived from it may be published without the author’s prior consent. 2 A Study of Marine Benthic Algae Along a Natural Carbon Dioxide Gradient Vivienne Johnson Abstract Increasing atmospheric CO2 is causing unprecedented changes in seawater chemistry, yet the uncertainty of the ecological response to these projected changes, termed ‘ocean acidification’, remains considerable at present. To predict the effects of these changes, we need to improve our understanding of the responses of marine primary producers since these drive biogeochemical cycles and determine the structure and function of benthic habitats. The majority of experiments on the effects of ocean acidification on photoautrophs to date have mainly focused on oceanic microalgae, leaving benthic assemblages largely overlooked. Carbon dioxide vents are providing a means for examining and predicting the impacts of ocean acidification on marine ecosystems. In this thesis a temperate CO2 volcanic vent gradient was used to investigate the responses of benthic microalgal assemblages (periphyton, epilithic, epipelic, epipsammic and endolithic) and macroalgae (a calcified phaeophyte, crustose coralline algae and turf algae) to increasing pCO2. The photosynthetic standing crop of microphytobenthic assemblages increased significantly with elevations in CO2 indicating that the productivity of shallow water habitats may be promoted over the course of this century. Some benthic diatoms appear to benefit in naturally CO2 enriched environments whilst benthic cyanobacteria in this study appear to be relatively insensitive to the levels of increase predicted for this century. Dramatic shifts in epilithic macroalgae assemblages were observed along the CO2 gradient and a calcified phaeophyte was revealed as an unexpected ecological winner under ocean acidification scenarios. These observations suggest that benthic algal assemblages have the potential to dramatically alter as CO2 levels continue to rise; this would have profound consequences for the structure and function of benthic ecosystems. 3 List of Contents Acknowledgements 10 Author’s Declaration 12 Chapter 1: General Introduction 14 1.1 Introduction 14 1.2 Ocean acidification 15 1.3 Responses of marine algae to elevated CO2 17 1.3.1 Response of marine benthic microalgae to elevated CO2 20 1.3.1.1 Diatoms 22 1.3.1.2 Cyanobacteria 24 1.3.2 Responses of marine macroalgae to elevated CO2 26 1.3.2.1 Calcareous macroalgae 27 1.3.2.2 Non-calcareous macroalgae 31 1.4 Interactive impacts of multiple environmental stressors 33 1.5 Review of experimental approaches 35 1.5.1 Laboratory experimentation and associated limitations 35 1.5.2 The use of naturally CO2 enriched sites in ocean acidification studies and associated limitations 37 1.6 Summary and thesis aims 39 Chapter 2: Introduction to Vulcano Island volcanic CO2 vent system 41 2.1 Introduction 42 2.1 Methodology 44 2.1.1 Sampling sites 44 2.1.2 Physical and carbonate chemistry measurements 48 2.1.3 Statistical analysis 49 2.3 Results 50 2.4 Discussion 54 Chapter 3: Colonisation of Periphyton Assemblages on artificial substrata along a natural CO2 gradient 60 3.1 Introduction 61 3.2 Methodology 63 3.2.1 Study sites and carbonate chemistry 63 3.2.2 In situ sampling 63 3.2.3 Sample analysis 64 3.2.3.1 Chlorophyll a extraction 64 3.2.3.2 Epi-fluorescence 64 3.2.3.3 SEM 65 3.2.4 Statistical analysis 65 3.3 Results 66 3.4 Discussion 74 4 Chapter 4: Natural marine microphytobenthic assemblages at ambient and elevated levels of CO2 82 4.1 Introduction 82 4.2 Methodology 86 4.2.1 Study sites and carbonate chemistry 86 4.2.2 In situ sampling 87 4.2.2.1 Epilithic biofilms 87 4.2.2.2 Sandy sediment 88 4.2.3 Sample Analysis 88 4.2.3.1 Chlorophyll a extraction 88 4.2.3.2 Diatom densities 89 4.2.3.3 Epi-fluorescence 91 4.2.3.4 SEM 92 4.2.3.5 Sediment properties 93 4.2.4 Statistical analysis 93 4.3 Results 94 4.3.1 Sediment properties 94 4.3.2 Photosynthetic standing crop (Chl a) 95 4.3.3 Benthic diatom densities 96 4.3.4 Epi-fluorescence 98 4.3.5 Benthic diatom assemblage composition 100 4.4 Discussion 108 4.4.1 Epilithic biofilms 108 4.4.2 MPB of sandy sediments 112 4.4.3 Conclusion 117 Chapter 5: Changes in endolithic microalgal and epilithic macroalgal assemblages along a CO2 gradient 119 5.1 Introduction 120 5.1.1 Endolithic microalgae 120 5.1.2 Epilithic algal communities 123 5.2 Methodology 125 5.2.1 Endolithic microalgae 125 5.2.1.1 Preparation of the CaCO3 experimental substrates 125 5.2.1.2 Installation of experimental CaCO3 substrates 126 5.2.1.3 Investigating in situ populations of gastropods for endoliths 127 5.2.1.4 Processing of the CaCO3 substrates 127 5.2.1.4.1 Chlorophyll a extraction 128 5.2.1.4.2 Epi-fluorescence 128 5.2.2 Epilithic algal communities 129 5.2.3 Statistical analysis 129 5.3 Results 130 5.3.1 Endolithic microalgae assemblages in experimentally installed aragonite blocks 130 5.3.2 Endolithic microalgae assemblages in natural populations of gastropods 133 5.3.3 Epilithic algal communities 136 5.4 Discussion 140 5 5.4.1 Endolithic assemblages 140 5.4.2 Epilithic algal communities 143 5.4.3 Conclusion 144 Chapter 6: The ecological and physiological responses of Padina pavonica (Phaeophyta-Dictyotaceae) to elevated CO2 146 6.1 Introduction 147 6.2 Methodology 150 6.2.1 Study sites and carbonate chemistry 150 6.2.2 Padina abundance and sea urchin densities 151 6.2.3 Calcium carbonate content determination and crystal examination 151 6.2.4 Photosynthesis 152 6.2.5 Statistical analysis 154 6.3 Results 155 6.4 Discussion 163 Chapter 7: General Discussion 169 7.1 Discussion of main findings and implications for marine systems 170 7.1.1 Microphytobenthic assemblages 170 7.1.2 Benthic diatoms 176 7.1.3 Benthic cyanobacteria 180 7.1.4 Macroalgae assemblages 181 7.2 Limitations of research 184 7.3 Summary and direction for future research 186 6 Appendices 191 Appendix I. Photographs of benthic changes along the Vulcano CO2 gradient 192 Appendix II. Epilithic biofilm epi-fluorescence images 193 Appendix III. Epipelic epi-fluorescence images 194 Appendix IV. Summary data for the colonisation of experimental CaCO3 substrates 195 Appendix V. Photographs of colonised experimental CaCO3 substrates 196 Appendix VI. Endolithic microalgae epi-fluorescence images 197 References 198 Abbreviations CO2 - Carbon dioxide H2CO3 – Carbonic acid CaCO3 - Calcium carbonate - Carbonate + Ca2 - Calcium - HCO3 - Bicarbonate DIC - Dissolved inorganic carbon TA - Total alkalinity CCM - Carbon concentrating mechanisms Chl a – Chlorophyll a CLSM – Confocal laser scanning microscope SEM – Scanning electron microscope 7 List of Illustrations 2.1 Map of Baia de Levante, Vulcano Island 45 2.2 Photographs of Vulcano Island and the Baia di Levante 46 2.3 Geochemical distribution maps for Baia di Levante 47 2.4 Box plot showing pH range of sampling stations 51 2.5 Bar chart of carbonate parameters along the CO2 gradient 52 3.1 Periphyton Chl a boxplot 67 3.2 Periphyton epi-fluorescence bar chart 70 3.3 Periphyton diversity, evenness and dominance bar chart 71 3.4 Dendrogram for the cluster analysis of the similarity of periphytic diatoms 71 3.5 Bar chart showing composition of periphytic diatom assemblages 72 3.6 SEM images of periphytic assemblages 73 3.7 Bar chart of mean periphytic diatom counts 74 4.1 Chl a boxplot for microphytobenthic assemblages 97 4.2 Bar chart of mean diatom densities in microphytobenthic assemblages 98 4.3 Bar chart of epipelon epi-fluorescence 99 4.4 Bar chart showing composition of diatom assemblages in the microphytobentos 101 4.5 Dendrogram for the cluster analysis of the similarity of diatoms in microphytobenthic assemblages 102 4.6 SEM images of epilithic assemblages 103 4.7 Bar chart of mean diatom counts in microphytobenthic assemblages 106 4.8 Diatom diversity, evenness and dominance in microphytobenthic assemblages 107 5.1 Calcium carbonate reduction and Chl a concentration of aragonite blocks 131 5.2 Photographs of endolithic colonisation of aragonite blocks 132 5.2 Chl a bar chart for endolithic assemblages in gastropod shells 134 5.3 Epi-fluorescence of endolithic assemblages in gastropod shells 135 5.4 Photographs of endolithic colonisation in dead and live limpet shells 136 8 5.5 Epilithic algal community composition along CO2 gradient 137 5.6 Photographs of epilithic algal communities 137 6.1 Abundance of P.pavonica along CO2 gradient 156 6.2 P. pavonica and sea urchin abundance bar/line chart 157 6.3 P.pavonica CaCO3 content 158 6.4 Photographs of P.pavonica thalli and SEM images of aragonite crystals 160 6.5 Bar chart of P.pavonica Chl a content 161 6.6 Rapid light curves of P.pavonica 162 List of Tables Table 2.1 Seawater carbonate chemistry measurements along CO2 gradient 53 Table 2.2 Dissolved nutrient concentrations 54 Table 4.1 Sediment properties of sampling stations 95 Table 6.1 P.pavonica aragonite crystal data 160 Table 6.2 Mean rETR values for P.pavonica 164 Table 7.1 Summary of the recorded responses of various microphytobenthic assemblages to CO2 enrichment 175 9 Acknowledgements It would not have been possible to write this doctoral thesis without the support of many people.