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The Respiratory and Gut Physiology of Fish: Responses to Environmental Change

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The Respiratory and Gut Physiology of Fish: Responses to Environmental Change The Respiratory and Gut Physiology of Fish: Responses to Environmental Change Submitted by Nicholas John Rogers to the University of Exeter as a thesis for the degree of Doctor of Philosophy in Biological Sciences In August 2015 This thesis is available for Library use on the understanding that it is copyright material and that no quotation from the thesis may be published without proper acknowledgement. I certify that all material in this thesis which is not my own work has been identified and that no material has previously been submitted and approved for the award of a degree by this or any other University. Signature: ………………………………………………………….. i Thesis Abstract Many of the habitats occupied by fish are highly dynamic, naturally demonstrating substantial abiotic fluctuations over diurnal, tidal or seasonal cycles. It is also the case that throughout their 545 million year evolutionary history, fish have existed in aquatic environments very different to those of the present day. However, the past several decades have seen unprecedented rates of environmental change, at local and global scales, arising from human activities. The two major themes of the present thesis are: 1) Respiratory responses of fish to changes in environmental oxygen and temperature in the context of exploring intra- and inter-specific trait variation and its ecological implications 2) The effects of environmental factors (oxygen, carbon dioxide, temperature and seawater chemistry) on the intestinal precipitation and excretion of calcium carbonate by marine teleosts. In the first study (chapter two) a comprehensive database of fish critical PO2 (Pcrit) data compiled from the published literature is presented. The systematic review of this literature provided the opportunity to critically examine methodologies for determining Pcrit as well as its usefulness as an indicator of hypoxia tolerance in fish. The second study (chapter three) examines whether inter- and intra-specific variation in thermal and hypoxia tolerance in two reef snapper species (Lutjanus carponotatus and Lutjanus adetii) reflects their distributions across the contrasting biophysical environments of the reef flat and reef slope surrounding Heron Island on the Great Barrier Reef. L. carponotatus was clearly the most thermally and hypoxia tolerant of the two ° species, demonstrating a ~3.5 C wider thermal tolerance zone (higher CTmax, lower CTmin) and ~26% lower Pcrit than L. adetii. These results suggest that the contrasting distribution of these species between flat and slope reef zones is reflected in their physiological tolerances. However, there was no evidence of intra-species variation in tolerance between flat and slope caught L. carponotatus individuals, indicating that this species does not form physiologically distinct subpopulations between these reef zones. The third study (chapter four) experimentally quantified the effect of hypercarbia (3000 ii µatm) and hypoxia (50% air saturation) on gut carbonate production by the European flounder (Platichthys flesus). Both hypercarbia and hypoxia resulted in a significant increase in carbonate excretion rate (1.5-fold and 2.4-fold, respectively) and acted synergistically when combined. In the final study (chapter five), gut carbonate production was measured in the European flounder undergoing conditions simulating the ‘calcite seas’ of the Cretaceous. The results of this study support the hypothesis that ocean conditions prevalent during the Cretaceous period resulted in piscine carbonate production rates substantially higher (~14-fold) than the present day. Ultimately, this thesis directly links the environmental physiology of fish at the individual level to wider scale implications (past, present and future), ranging from local ecological patterns all the way up to global carbon cycles. iii Acknowledgments Firstly, I wish to express my deep gratitude to supervisor Dr. Rod Wilson for his tireless support and guidance throughout the process of producing this thesis. It has been a great privilege to work alongside and to learn from such a passionate and skilful scientist. Likewise, I am very grateful to members of the Wilson lab group, Dr. Erin Reardon, Dr. Mauricio Urbina, Dr. Cosima Porteus, Dr. Rob Ellis, Sam Newbatt and Christine Stephens for their advice and encouragement along way. This work would not have been possible without the excellent assistance of the technical team within the Environmental Biology theme and Aquatic Resource Centre at the University of Exeter. In particular, my sincere thanks to Dr. Gregory Paull, Jan Shears, Dr. John Dowdle and Steve Cooper. I am also hugely grateful to Dr. Alastair Harborne at the University of Queensland for providing me with the fantastic opportunity to assist with his field work on Heron Island. A special mention must go to my fellow PhD students, housemates and ‘brothers in arms’ - Sam Newbatt and Jon Green; without whom the past four years would not have been so much fun! To Kerina, thank you for your extraordinary patience and loving support during this time. Finally, I dedicate this thesis to my parents, Andrea and Peter, to whom no words could adequately express my gratitude for everything they have provided. This work was funded by a studentship from the Natural Environment Research Council (NERC). Additional funding (chapter two) in the form of a ‘short-term scientific mission’ was provided by the European Union Cooperation in Science and Technology (COST) Action (FA1004) on the ‘Conservation Physiology of Marine Fishes’. iv Table of Contents The Respiratory and Gut Physiology of Fish: Responses to Environmental Change ........................................................................................................... i Thesis Abstract ............................................................................................... ii Acknowledgments .......................................................................................... iv Table of Contents ........................................................................................... v List of Figures ................................................................................................. x Chapter 1....................................................................................................... 1 General Introduction ....................................................................................... 3 The Diversity, Distribution and Value of Fish .......................................... 3 Environmental Change and Ecophysiology ............................................. 4 Respiratory Responses to Environmental Change ................................. 8 Gut Carbonate Production by Marine Teleosts ..................................... 12 Global Significance of Piscine Carbonate Production ........................... 16 Environmental Change and Carbonate Production ............................... 19 Summary .................................................................................................. 21 Chapter 2..................................................................................................... 23 A physiological trait database of hypoxia tolerance (Pcrit) in fish. ................. 25 Abstract .................................................................................................... 25 Introduction ............................................................................................... 26 Methods .................................................................................................... 29 Literature Search .................................................................................. 29 Database Construction.......................................................................... 30 Results...................................................................................................... 32 Database Coverage .............................................................................. 32 Pcrit Methodology ................................................................................... 33 Biotic and Abiotic Interactions ............................................................... 34 Discussion ................................................................................................ 37 v Pcrit Methodology ................................................................................... 37 Pcrit as a Hypoxia Tolerance Trait .......................................................... 42 Biotic and Abiotic Interactions ............................................................... 44 Future Applications ............................................................................... 49 Acknowledgments .................................................................................... 50 Appendix................................................................................................... 51 Chapter 3..................................................................................................... 57 Thermal and hypoxia tolerance as traits of fishes using shallow-water coral- reef habitats. ................................................................................................ 59 Abstract .................................................................................................... 59 Introduction ............................................................................................... 60 Materials and Methods ............................................................................
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