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University of Southampton UNIVERSITY OF SOUTHAMPTON FACULTY OF NATURAL AND ENVIRONMENTAL SCIENCES Ocean and Earth Science Population structure and ecology of wild Crassostrea gigas (Thunberg, 1793) on the south coast of England by Stephanie Rachael Anne Mills Thesis for the degree of Doctor of Philosophy July 2016 UNIVERSITY OF SOUTHAMPTON ABSTRACT FACULTY OF NATURAL AND ENVIRONMENTAL SCIENCES Ocean and Earth Science Thesis for the degree of Doctor of Philosophy Population structure and ecology of wild Crassostrea gigas (Thunberg, 1793) on the south coast of England By Stephanie Rachael Anne Mills Crassostrea gigas (Thunberg, 1793) is native to Japan and Korea, but has achieved global distribution through human mediated dispersal pathways and natural larval dispersal. Considerable variation in recruitment to wild aggregations has been seen regionally across the globe. Wild recruitment of C. gigas in England has increased in frequency since the millennia however a detailed understanding of their occurrence is limited to an area within the Thames estuary. There have been no English studies to date that reveal how C. gigas interacts with recipient ecosystems, or what impacts winter conditions have. Furthermore conclusive evidence has yet to be presented that feral C. gigas in England are self-sustaining. Intertidal surveys found substrate type and shore height to have the greatest impact on the locality and abundance of C. gigas recruitment. Gametogenesis initiated in C. gigas when water temperatures increased above 9.5 °C. Maturity was generally reached in the summer, however spawning differed between locations. Wild, intertidal C. gigas were found to spawn twice in a single reproductive season. Initially, spawning was triggered through tidally induced temperature shocking as water temperatures increased above 18 °C. It is thought that the second spawning was triggered by a combination of warm water (+18 °C) and an increase in phytoplankton abundance. Farmed, subtidal C. gigas spawned once, coinciding with the 2nd spawning of intertidal oysters. Rapid growth rates allow a size refuge from the greatest predation pressure to be achieved before growth rates decline over winter. In particular Carcinus maenas is capable of predating C. gigas with a shell length of up to at least 50 mm. Winter conditions experienced in England are typically colder than those experienced with in the native range of C. gigas, and as such, were detrimental to C. gigas. Juvenile oysters with 4 ± 0.5 mg (dry flesh weight) had significantly higher respiration rates than 6 and 9 ± 0.5 mg juvenile oysters at water temperatures of 7 °C. Temperatures within the pallial cavity of adult C. gigas remained similar to the ambient environment, changing rapidly with tidal immersion/emersion. Furthermore pallial temperatures below 0 °C were recorded and found to reduce gaping activity. Juvenile oysters are the most vulnerable to cold temperatures and are likely affected most years, however only particularly cold years with extensive frosts impacted on adults. This study expands the base-line knowledge of C. gigas distribution in England to include Southampton Water and Poole Harbour, and investigates the impacts that annual water temperatures and predation have on reproduction and recruitment. The accumulated knowledge and information will enable a better understanding of how establishing C. gigas is likely to develop in the future, and has the potential for use in predictive models and other conservation tools. Table of Contents Table of Contents ........................................................................................................ i List of Tables .............................................................................................................. v List of Figures ........................................................................................................... vii List of Accompanying Materials ............................................................................... xv DECLARATION OF AUTHORSHIP .............................................................................. xvi Acknowledgements ............................................................................................... xvii Definitions and Abbreviations .................................................................................. 19 Chapter 1: Introduction .................................................................................... 1 1.1 The study species: Crassostrea gigas.................................................................. 1 1.1.1 Taxonomy and nomenclature ............................................................... 1 1.1.2 Morphology .......................................................................................... 2 1.1.3 Ecology .................................................................................................. 4 1.1.4 Life cycle ................................................................................................ 8 1.2 Crassostrea gigas in aquaculture ........................................................................ 8 1.3 Crassostrea gigas as an invasive species .......................................................... 13 1.3.1 Global distribution .............................................................................. 13 1.3.2 UK distribution .................................................................................... 15 1.4 Aquaculture as a vector for invasive species .................................................... 16 1.5 Impacts of Crassostrea gigas establishment .................................................... 17 1.5.1 Ecological impacts ............................................................................... 17 1.5.2 Economic impacts ............................................................................... 19 1.6 Thesis structure ................................................................................................. 21 1.7 Aims, Hypotheses and Objectives ..................................................................... 24 Chapter 2: Study sites ..................................................................................... 27 2.1 Poole Harbour ................................................................................................... 27 2.2 Southampton Water ......................................................................................... 31 2.3 Collection site monitoring ................................................................................. 34 i Chapter 3: Characteristics of feral aggregations of Crassostrea gigas inhabiting Poole Harbour and Southampton Water ................................................... 35 3.1 Introduction ...................................................................................................... 36 3.2 Materials and methods .................................................................................... 39 3.2.1 Beach surveys and mapping ............................................................... 39 3.2.2 Population structure .......................................................................... 40 3.2.3 Mapping.............................................................................................. 41 3.2.4 Shell morphology ................................................................................ 41 3.2.5 Growth ................................................................................................ 42 3.2.6 Mortality ............................................................................................. 43 3.3 Results .............................................................................................................. 44 3.3.1 Crassostrea gigas population structure ............................................. 44 3.3.2 Physical environmental factors .......................................................... 54 3.4 Discussion ......................................................................................................... 57 Chapter 4: Gametogenic development of wild and farmed Pacific oysters on the south coast of England ............................................................................. 67 Abstract ...................................................................................................................... 67 4.1 Introduction ...................................................................................................... 68 4.2 Materials and Methods .................................................................................... 72 4.2.1 Sample collection ............................................................................... 72 Wild Crassostrea gigas ........................................................................................ 72 Aquaculture Crassostrea gigas ........................................................................... 72 4.2.2 Histology ............................................................................................. 73 4.3 Results .............................................................................................................. 78 4.4 Discussion ......................................................................................................... 96 Chapter 5: Top-down control on recruitment success of Crassostrea gigas ... 107 5.1 Introduction .................................................................................................... 108 5.2 Materials and Methods .................................................................................
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