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A Thesis Submitted in Fulfillment of the Requirement for the Degree Of Natural variations in the zooxanthellae of temperate symbiotic Anthozoa Louise R. Squire B. Sc. (Hons.) A thesis submitted in fulfillment of the requirement for the degreeof Philosophiae Doctor at the University of Wales, Bangor. June 2000 School of Ocean Sciences University of Wales, Bangor Menai Bridge Anglesey LL59 5EY r I'IN OD ýY L'DI0 YN Y Yi\SUNIG TO 6E CONSULTEDIN THE LI IR/\RYONLY a4%BRA CONTENTS Page Acknowledgements v Abstract vi List of tables vii List of figures ix List of plates xii CHAPTER 1 General Introduction 1 CHAPTER 2 Seasonality in tropical and temperate subtidal environments 2.1. Introduction 6 2.2. Methods 10 2.2.1. Study sites 10 2.2.2. Seasonalfluctuations in meteorological conditions 11 2.2.3. Seasonalfluctuations in water column parameters 12 2.2.4. Measurementsof underwater irradiance 12 2.2.4.1.The effect of weatherand seasonon daily cycles of underwaterirradiance 12 2.2.4.2. The effect of seasonon attenuation of downwelling irradiance 13 2.3. Results 14 2.3.1. Seasonalfluctuations in meteorological conditions 14 2.3.2. Seasonalvariations in water column parameters 15 2.3.3. Underwater irradiance 17 2.3.3.1. The effect of weather and seasonon daily cycles of underwater irradiance 17 2.2.3.2.The effect of seasonon attenuationof downwelling irradiance 19 2.4. Discussion 20 Underwater irradiance 23 Conclusions 26 i CHAPTER 3 Natural variations in zooxanthellae characteristics in field populations of Anemonia viridis and Anthopleura ballii 3.1. Introduction 28 3.2. Methods 34 3.2.1. Study sites 35 3.2.2. Survey of anemonedistribution, density and habitat 35 3.2.2.1. Mid-tide level rockpool, Trearddur Bay, Anglesey 35 3.2.2.2. Castle Island Bay, Lough Hyne M. N. R., Ireland (Renoufian sector 13) 35 3.2.2.3. Glannafeencliff, Lough Hyne M. N. R., Ireland 36 3.2.3. The effect of seasonand depth on zooxanthellae characteristics 36 3.2.3.1. Field sampling 36 3.2.3.2. Zooxanthellae characteristics 37 3.3. Results 40 3.3.1.Anemone distribution, density and habitat 40 3.3.1.1. Mid-tide level rockpool, Trearddur Bay, Anglesey 40 3.3.1.2. Castle Island Bay, Lough Hyne M. N. R., Ireland 41 3.3.1.3. Glannafeencliff, Lough Hyne M. N. R., Ireland 42 3.3.2. The effect of seasonand depth on zooxanthellae characteristics 43 3.3.2.1. Seasonalvariation in intertidal Anemonia viridis, Trearddur Bay 43 Zooxanthellae density 43 Mitotic Index 44 Diameter 44 Chlorophyll concentration 45 3.3.2.2. Seasonalvariation in subtidal Anemonia viridis, Castle Island Bay 46 3.3.2.3. Seasonaland bathymetric variation in Anthopleura ballii, Glannafeencliff, 47 3.4. Discussion, 48 Distribution and density of anemones 48 Zooxanthellae characteristics 51 Pigments 55 ü Conclusions 59 CHAPTER 4 Photoadaptive responses of Anemonia viridis and associated zooxanthellae to irradiance of altered spectral quality and intensity 4.1. Inroduction 61 4.2. Methods 64 4.2.1.Collection and maintenance of anemones 64 4.2.2. Measuring intensity and spectral composition of artificial irradiance 65 4.2.3. Buoyant weighing 65 4.2.4. The effect of light of altered spectral composition and intensity 66 4.3. Results 67 4.3.1. Spectral composition of artificial irradiance 67 4.3.2. Buoyant weight 67 4.3.3. The effect of light of altered spectral composition and intensity 69 4.3.3.1. Intensity experiment 68 4.3.3.2. Spectraexperiment 70 4.4. Discussion 72 Conclusions 76 CHAPTER 5 Photoadaptive ultrastructure changes in zooxanthellae symbiotic with temperate Anthozoa 5.1. Introduction 79 5.2. Methods 82 5.2.1. The effect of seasonand habitat on zooxanthellae ultrastructure 81 5.2.2. The effect of light intensity and spectral composition on zooxanthellaeultrastructure 82 5.2.3. Transmission electron microscopy 83 5.2.4. Stereology 84 Background 85 Stereological analysis 86 5.2.5. Statistics 86 111 5.3. Results 86 5.3.1. Field populations 86 5.3.2. Laboratory experiments 88 5.3.24. Intensity experiment 88 5.3.2.2. Spectraexperiment 88 5.4. Discussion 89 Conclusions 95 CHAPTER 6 General Discussion 96 References 108 Appendices Appendix I Experiment to test the suitability of wet weight of tentacles as a standardfor zooxanthellaedensities 124 Experiment to investigate proportion of zooxanthellae in Anemonia viridis tentacles 124 Appendix II Table 1. Abundance and distribution of benthic organisms along a vertical depth profile of Glannafeen cliff, Lough Hyne 125 Appendix III Table 1. Attenuation coefficients for different wavebands in Lough Hyne during summer and winter 127 AppendixIV Figure 1. Attenuation of downwelling irradiance in Lough Hyne during summer and winter 128 AppendixV Table 1. Downwelling irradiance at 6m and 18 m in Lough Hyne on bright days in summer and winter 129 Appendix VI Figure 1. Attenuation of different wavebands of downwelling PAR with water depths in Lough Hyne during winter 130 Appendix VII Table 1. Summaryof field andlaboratory zooxanthellae characteristicdata 133 iv Acknowledgements Firstly I would like to thank my supervisor Dr. John Turner for the opportunity to conduct this research.I am particularly grateful for my introduction to the subtidal delights of Lough Hyne and Mauritius. Thanks to Declan O'Donnell, Warden of the Irish Wildlife Services, for granting permits to work in Lough Hyne and also for providing water column data for Chapter 2. Thanks to Dr. Deollal Daby for water column and meteorological data for Mauritius. Many thanks to Dr. Dave Barnes and Amy Greenwood for their valuable diving services during February and August 1998. Thanks to Dr. Dave Bowers for trusting me with the PRR 600 spectroradiometerin Lough Hyne and for help with processing subsequentdata. I would also like to thank Dr. Graham Walker and Dr. Ian Lucas for help with preparation of samples for electron microscope work, and use of thier laboratory and equipment. I am indebted to them both. Big thanks to Andrew Davies for use of the TEM and developing of films, and Dave Roberts for his impressive stamina in printing the electronmicrographs. Infinite thanks go to Dr. Steve Freeman, my good friend and fellow PhD-sufferer. May we never stop laughing! I thank my parents for being there at all times. And a special thank you goes to Tom for his profound faith and unfaltering support whenever I attempted to crumble. Finally I must thank Dr. Karen Mottart for inviting me to live at Cae Canol Farm during my write-up. V Abstract Few previous studies of zooxanthellae have considered temperate Anthozoan symbioses.The present study investigates how the characteristics of zooxanthellae symbiotic with temperate Anthozoa vary in response to natural variations in environmental parameters. Variations in the number (density), division rate, size and ultrastructure of zooxanthellae from the temperate anemones Anemonia viridis (Forskal) and Anthopleura ballii (Cocks) were examined in responseto season,water depth and artificial irradiance (A.viridis in aquaria). In addition, variations in chlorophyll concentrationswere considered in intertidal and laboratory- maintained A. viridis. Zooxanthellae from both intertidal and shallow subtidal A. viridis showed variations which correlated with seasonal variations in environmental parameters. Zooxanthella density in intertidal A. viridis showed an inverse relationship with temperature, daylength and sunshine. Higher zooxanthella density was observed in A. viridis from a shallow, subtidal habitat during February 1998 (2.06 ± 0.11 x 108 cells g"' wet weight) than during July 1998 (1.01 ± 0.09 x 108 cells g'' wet weight; T= 7.67, p< 0.001). Stereological analysis of transmission electron micrographs showed that zooxanthellae in intertidal A. viridis had significantly higher chloroplast volume fraction during February (32.1 ± 1.5 %) than July (21.8 ± 2.1 %; T= 4.07, p<0.05). The proportion of chlorophyll a per zooxanthella was significantly higher in December than all other months except January (ANOVA, F= 5.62 p<0.05). The zooxanthellae of A. viridis may thus photoadapt to low winter irradiances by increasing zooxanthellae density, chloroplast volume and the proportion of chlorophyll a per cell. By contrast, zooxanthellae from A. viridis maintained in artificial irradiances in the laboratory of 4 µmol m=2 s' and 20 pmol m2 s' showed no variation in density or ultrastructure, due either to the low irradiances used or a lack of variation in other physical parameterscompared to the field. A. ballii zooxanthella density responded to both depth and seasonand was lower at 6m during summer than at 6m during winter and at 18 m during both summer and winter. Chloroplast volume fractions in A. ballii was not affected by depth during winter, nor by seasonat 18 in. Starch and lipid stores in zooxanthellae from both A. viridis and A. ballii responded to seasonalfluctuations. Lipid was present in zooxanthellae during summer (intertidal A. viridis, volume fraction 19.8 ± 3.4 %) and absent during winter, and starch volume was significantly higher from zooxanthellae in A. ballii at 6 in in winter (14.3 ± 4.2 %) than 18 min winter (4.7 ± 1.6 %) or summer (4.7 ± 1.1 %; ANOVA, F= 6.04 0.05). It is p< concluded that the zooxanthellae of the temperate anemonesA. viridis and A. ballfi show variations in zooxanthellae characteristics which correspond to variations in day- to-day weather, seasonand water depth. vi List of Tables CHAPTER 2 2.1. Total daily illumination underwater in Lough Hyne during winter and summer, and in Mauritius during April (1998) in different weather conditions. 2.2. Attenuation coefficients (Kd) and 1% depths (7")for temperatewater, Lough Hyne during summer (8/98) and winter (2/98) and tropical water (1/96), Mauritius. CHAPTER 3 3.1. Dominant speciesat 6m and 18 m on Glannafeen cliff, Lough Hyne.
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