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THE EFFECT of CLIMATE CHANGE on DEVELOPMENT, GROWTH and METABOLISM of EMBRYONIC ELASMOBRANCHS, Scyliorhinus Sp

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THE EFFECT of CLIMATE CHANGE on DEVELOPMENT, GROWTH and METABOLISM of EMBRYONIC ELASMOBRANCHS, Scyliorhinus Sp THE EFFECT OF CLIMATE CHANGE ON DEVELOPMENT, GROWTH AND METABOLISM OF EMBRYONIC ELASMOBRANCHS, Scyliorhinus sp. A thesis submitted to the University of Manchester for the degree of Doctor of Philosophy in the Faculty of Biology, Medicine and Health 2019 MUHAMMAD SYAFIQ BIN MUSA School of Medical Sciences Division of Cardiovascular Sciences LIST OF CONTENTS LIST OF TABLES 7 LIST OF FIGURES 8 LIST OF ABBREVIATIONS 10 ABSTRACT 11 DECLARATION 12 COPYRIGHT STATEMENT 13 THE AUTHOR 14 ACKNOWLEDGEMENTS 16 CHAPTER I GENERAL INTRODUCTION 17 1.1 Climate Change 17 1.1.1 Temperature 17 1.1.2 Hypoxia 19 1.1.3 Predicted future climate 20 1.2 Elasmobranchs 20 1.2.1 Importance of elasmobranchs 21 1.2.2 Reproduction of elasmobranchs 22 1.2.3 Egg cases of oviparous elasmobranchs 23 1.2.4 The plight of sharks 24 1.2.5 Vulnerability of early life stages oviparous elasmobranchs 25 1.2.6 Greater spotted catshark and small-spotted catshark 26 1.2.7 Embryological study of oviparous elasmobranchs 29 1.3 Climate Change on Elasmobranchs and Other Ectothermic Fish 29 1.3.1 Temperature 29 1.3.2 Hypoxia 31 1.3.3 Climate change on intertidal organisms 32 1.4 Aim and Objectives 33 2 CHAPTER II GENERAL METHODOLOGY 36 2.1 Introduction 36 2.2 Animal Species 36 2.2.1 Small-spotted catshark (Scyliorhinus canicula) 36 2.2.2 Greater spotted catshark (Scyliorhinus 37 stellaris) 38 2.2.3 Egg case shaving 2.3 Experimental Treatments 39 2.3.1 Temperature 39 2.3.2 Hypoxia 39 2.3.3 Experimental rearing conditions 40 2.4 Water Quality 42 2.5 Energy Budget 42 2.6 Growth and Survival 43 2.7 Metabolism 43 2.8 Respirometry 44 2.8.1 Experimental respirometer setup 44 2.8.2 Oxygen consumption calculations 46 CHAPTER III OVIPAROUS ELASMOBRANCH DEVELOPMENT INSIDE THE EGG CASE IN 7 KEY STAGES 48 Abstract 49 3.1 Introduction 49 3.2 Materials and Methods 53 3.2.1 Egg cases source and maintenance 53 3.2.2 Developmental staging 54 3.2.3 Growth pattern and average daily body length gain (ADL) 55 3.2.4 Yolk consumption rate 56 3.2.5 Development time (embryo age and the duration of each developmental stage) 56 3.2.6 Hatching process 57 3.2.7 Effect of air exposure on egg cases 57 3.2.8 Statistical analysis 57 3.3 Results 58 3 3.3.1 The egg case 58 3.3.2 Stage 1 60 3.3.3 Stage 2 60 3.3.4 Stage 3 62 3.3.5 Stage 4 64 3.3.6 Stage 5 66 3.3.7 Stage 6 68 3.3.8 Stage 7 70 3.3.9 Growth pattern and average daily body length gain (ADL) 75 3.3.10 Yolk consumption rate 77 3.3.11 Development time (embryo age and the duration of each developmental stage) 79 3.3.12 Hatching process 82 3.3.13 Effect of air exposure on S. stellaris egg cases with jelly and without jelly 83 3.4 Discussion 84 3.4.1 Early embryogenesis 85 3.4.2 Egg case structure and function 86 3.4.3 Jelly as protection 87 3.4.4 Opening of seawater slits 87 3.4.5 Gills and respiration 88 3.4.6 Fin and body morphology 89 3.4.7 Yolk consumption during development 90 3.4.8 Conclusions 91 Acknowledgements 91 Funding 91 References 92 Supporting Information 96 CHAPTER IV THE EFFECTS OF TEMPERATURE AND HYPOXIA ON GROWTH AND SURVIVAL OF EMBRYONIC SMALL-SPOTTED CATSHARK (Scyliorhinus canicula) 97 Abstract 98 4.1 Introduction 98 4.2 Materials and Methods 100 4.2.1 Supply of egg cases and care of animals 100 4.2.2 Experiment (biospheres) tanks and mimic of different climatic conditions 101 4 4.2.3 Developmental staging 101 4.2.4 Growth pattern and growth rate 104 4.2.5 Yolk consumption 105 4.2.6 Survival rate 105 4.2.7 Development time and hatchling size 106 4.2.8 Statistical analysis 106 4.3 Results 106 4.3.1 Growth of S. canicula embryos 106 4.3.2 Yolk consumption of S. canicula embryos 108 4.3.3 Survival rate 110 4.3.4 Development time and hatchling size 111 4.4 Discussion 112 4.4.1 Growth rate 113 4.4.2 Yolk consumption 114 4.4.3 Survival of S. canicula under future ocean warming and hypoxia 115 4.4.4 Development time and hatchling size 116 4.4.5 Conclusions and conservation implications 118 Acknowledgements 119 Funding 119 References 120 CHAPTER V THE EFFECTS OF OCEAN WARMING AND HYPOXIA ON METABOLISM OF SMALL- SPOTTED CATSHARK, Scyliorhinus canicula DURING EMBRYONIC DEVELOPMENT 127 Abstract 128 5.1 Introduction 128 5.2 Materials and Methods 131 5.2.1 Animal husbandry and experimental rearing conditions 131 5.2.2 Developmental stages investigated 132 5.2.3 Assessment of metabolic rate during development in different climatic rearing environments 134 5.2.4 Excess post-exercise oxygen consumption (EPOC) 135 5.2.5 Statistical analysis 136 5.3 Results 137 5 5.3.1 Effects of different climatic conditions on metabolism at each developmental stage 137 5.3.2 Effects of development on metabolism under different climatic conditions 139 5.3.3 Effects of rearing environment and developmental stage on EPOC 139 5.3.4 Temperature sensitivity (Q10) of metabolism 141 5.3.5 Developmental plasticity and metabolism 142 5.4 Discussion 144 5.4.1 Effect of temperature on embryonic and early post-hatch metabolism 145 5.4.2 Effect of dissolved oxygen levels on embryonic and early post-hatch metabolism 146 5.4.3 Ontogenetic changes in metabolism 148 5.4.4 Developmental environment does not have a lasting impact on metabolism 148 5.4.5 Implications for future oceans 149 5.4.6 Conclusion 151 Acknowledgements 151 Funding 152 References 152 CHAPTER VI GENERAL DISCUSSION AND CONCLUSION 162 6.1 Introduction 162 6.2 Contributions of Current PhD Work 162 6.3 Summary of PhD Findings 165 6.4 Conclusion 171 REFERENCES 172 APPENDIX 187 Final word count: 41,227 6 LIST OF TABLES Table 3.1 Comparison of 7 developmental stages inside the egg case from S. stellaris and S. canicula. 73 Table 5.1 Temperature sensitivity (Q10) of S. canicula oxygen consumption rates (MO2) at different developmental stages developed under normoxic and hypoxic conditions. 141 Table 5.2 Temperature sensitivity (Q10) of S. canicula EPOC recovery (τ values) at different developmental stages under normoxic and hypoxic conditions. 142 7 LIST OF FIGURES Figure 1.1 Scyliorhinus sp. adult. 27 Figure 1.2 Egg cases and hatchlings of S. stellaris and S. canicula. 28 Figure 2.1 The experimental rearing tanks of S. canicula egg cases. 41 Figure 2.2 The respirometer of S. canicula egg cases. 45 Figure 2.3 A summary of the metabolism study on S. canicula embryos. 47 Figure 3.1 External features of the S. stellaris egg case at stage 1. 59 Figure 3.2 The inside of the S. stellaris egg case at stage 2. 61 Figure 3.3 The inside of the S. stellaris egg case at stage 3. 63 Figure 3.4 The inside of the S. stellaris egg case at stage 4. 65 Figure 3.5 The inside of the S. stellaris egg case at stage 5. 67 Figure 3.6 The inside of the S. stellaris egg case at stage 6. 69 Figure 3.7 The inside of the S. stellaris egg case at stage 7. 70 Figure 3.8 7 key developmental stages of S. stellaris inside the egg case. 72 Figure 3.9 S. stellaris body length and external yolk sac volume across the 7 developmental stages. 75 Figure 3.10 Average daily body length gain (ADL) during each of the 7 developmental stages. 76 Figure 3.11 Yolk consumption rate during the 7 developmental stages. 78 Figure 3.12 Development time (age) to reach 7 developmental stages and hatch. 80 Figure 3.13 Duration of development time of the 7 developmental stages. 81 Figure 3.14 The hatching process. 82 Figure 3.15 Shrinking rate of S. stellaris egg cases (% in area h-1) with and without jelly. 84 Figure 4.1 Oviparous elasmobranch development inside the egg case in 7 key stages. 103 Figure 4.2 Summary of specific developmental stages that were investigated in this study based on the 7 key stages of development laid out in Musa et al. (2018). 104 8 Figure 4.3 Growth of S. canicula embryos developed under different climatic conditions. 107 Figure 4.4 Yolk consumption of S. canicula embryos developed under different climatic conditions. 109 Figure 4.5 Survival rate (SR) of S. canicula embryos developed under different climatic conditions. 110 Figure 4.6 Development time (age) of S. canicula embryos under different climatic conditions. 111 Figure 4.7 Hatchling size of S. canicula embryos under different climatic conditions. 112 Figure 5.1 Oviparous elasmobranch development in 7 key stages. 133 Figure 5.2 Oxygen consumption rates (MO2) of S. canicula embryos at stage 4 and 6 of development and at 1-day post-hatch under different treatments. 138 Figure 5.3 Time constant of recovery of excess post-exercise oxygen consumption (EPOC) of S. canicula embryos at stage 4 and 6 of development and at 1-day post-hatch under different treatments. 140 Figure 5.4 Oxygen consumption rates (MO2) of S. canicula hatchlings under different treatments and hatchlings acclimated (a week) to control treatment (normoxia at 15 °C).
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