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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 NATURAL AND ENVIRONMENTAL SCIENCES Ocean and Earth Science Volume 1 of 1 The role of hydrostatic pressure in constraining the bathymetric distribution of marine ectotherms by Alastair Edward Brown Thesis for the degree of Doctor of Philosophy Submitted August 2014 “Nothing in biology makes sense except in the light of evolution” Dobzhansky, 1973 UNIVERSITY OF SOUTHAMPTON ABSTRACT FACULTY OF NATURAL AND ENVIRONMENTAL SCIENCES Ocean and Earth Science Doctor of Philosophy THE ROLE OF HYDROSTATIC PRESSURE IN CONSTRAINING THE BATHYMETRIC DISTRIBUTION OF MARINE ECTOTHERMS Alastair Edward Brown A hyperbaric and thermal physiological bottleneck at bathyal depths is thought to contribute to bathymetric zonation of marine benthic invertebrates and demersal fishes on deep continental margins. The focus of this thesis was to investigate hyperbaric tolerance in the lithodid crab Lithodes maja as a case study for the effects of hydrostatic pressure on upper bathyal marine ectotherms. Experimental hyperbaric exposures revealed that hyperbaric tolerance is oxygen- and capacity-limited. Hyperbaric tolerance appears proximately oxygen-limited, but ultimately limited by cardiac capacity: adverse hyperbaric impacts on cardiac capacity appear mediated by the effects of pressure on membranes and membrane related functions. However, bathymetric range appears constrained by increased metabolic cost at elevated hydrostatic pressure. Hyperbaric limitation of bathymetric range supports a role for hydrostatic pressure in structuring bathymetric zonation in the deep sea, and lineage- specific physiological tolerances appear to contribute to global phylogenetic bottlenecks. Further, physiological effects of high hydrostatic pressure and low temperature at bathyal depths, acting on shallow-water taxa at the lower limits of their distribution, may invoke a stress–evolution mechanism. The resulting bathymetric variation in speciation rates could drive a unimodal diversity–depth pattern, typically peaking at bathyal depths, over time. Marine ectotherms’ thermal tolerance is also oxygen- and capacity-limited, and functionally associated with hypoxia tolerance. Comparing hypoxia thresholds and hyperbaric thresholds of taxonomic groups of shallow-water fauna revealed significant correlation, supporting the proposition that hydrostatic pressure tolerance is oxygen- limited. Consequently, it appears that the combined effects of temperature, pressure, and oxygen concentration constrain the fundamental ecological niches of marine invertebrates and fishes. Including depth in a conceptual model of oxygen- and capacity-limited fundamental ecological niches’ responses to ocean warming and deoxygenation confirms that polar taxa are most vulnerable to the effects of climate change, but reveals for the first time that temperate fauna as well as tropical fauna may experience substantial fundamental ecological niche expansion with ocean warming and deoxygenation. i Contents ABSTRACT ................................................................................................................. i Contents .................................................................................................................. iii List of tables ........................................................................................................... vii List of figures ........................................................................................................... ix DECLARATION OF AUTHORSHIP ............................................................................... xi Acknowledgements ............................................................................................... xiii 1. Introduction..................................................................................................... 1 1.1 Bathymetric biodiversity patterns ............................................................. 1 1.2 Origin of the deep-sea fauna and the colonisation of the deep sea ......... 4 1.3 Physiological limitation by low temperature and high hydrostatic pressure ..................................................................................................... 9 1.4 Tolerance of high hydrostatic pressure and low temperature ............... 13 1.5 Adaptations to high hydrostatic pressure and low temperature ........... 21 1.6 The Lithodidae: a model family for hyperbaric investigation ................. 23 1.7 Rationale, aim, objectives and hypotheses ............................................. 26 2. Evidence for oxygen- and capacity-limited hyperbaric tolerance and support for bathymetric range limitation by metabolic cost .............................................. 29 2.1 Introduction ............................................................................................. 29 2.2 Materials and Methods ........................................................................... 30 2.2.1 Sample collection, transfer, and maintenance ....................................... 30 2.2.2 The IPOCAMP pressurised incubator ...................................................... 31 2.2.3 Physiological measurements ................................................................... 31 2.2.4 Measuring cardiac activity and oxygen consumption ............................. 33 2.2.5 Experimental protocols ........................................................................... 34 2.2.5.1 Hyperbaric tolerance ............................................................................. 34 2.2.5.2 Sustained hyperbaric tolerance ............................................................ 36 2.2.5.3 Hyperbaric acclimation .......................................................................... 38 2.2.6 Cardiac activity and oxygen consumption data normalisation and statistical analysis .................................................................................... 40 2.2.7 Haemolymph L-lactate concentration measurement and statistical analysis .................................................................................................... 41 iii 2.2.8 Haemolymph ion concentration determination and statistical analysis 41 2.3 Results ..................................................................................................... 42 2.3.1 Survival .................................................................................................... 42 2.3.2 Hyperbaric tolerance ............................................................................... 43 2.3.3 Sustained hyperbaric tolerance .............................................................. 46 2.3.4 Hyperbaric acclimation ............................................................................ 46 2.4 Discussion ................................................................................................ 51 2.4.1 Implications of pressure-sensitive metabolic rate .................................. 51 2.4.2 Oxygen- and capacity-limited hyperbaric tolerance ............................... 55 2.4.3 The mechanism limiting hyperbaric cardiac performance ..................... 57 2.4.4 Bathymetric range limitation by metabolic cost ..................................... 67 2.4.5 Ecological and evolutionary implications of energy-limited bathymetric distribution .............................................................................................. 71 2.4.6 Conclusion ............................................................................................... 73 3. Taxonomic pattern of hyperbaric limitation: support for the hypothesis of oxygen- and capacity-limitation of hyperbaric tolerance ................................ 75 3.1 Introduction ............................................................................................. 75 3.2 Materials and Methods ........................................................................... 77 3.2.1 Data collection ......................................................................................... 77 3.2.2 Statistical analysis .................................................................................... 79 3.3 Results ..................................................................................................... 79 3.4 Discussion ................................................................................................ 79 3.4.1 Conclusion ............................................................................................... 84 4. Synthesis ....................................................................................................... 87 4.1 Do lineage-specific tolerances contribute to global phylogenetic bottlenecks?