The Roles of the Cockle Cerastoderma Edule L. on Ecosystem Functioning

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The Roles of the Cockle Cerastoderma Edule L. on Ecosystem Functioning The roles of the cockle Cerastoderma edule L. on ecosystem functioning: cockle comings and goings Thesis submitted in accordance with the requirements of the University of Liverpool for the degree of Doctor in Philosophy by Christopher Peter Cesar September 2009 ABSTRACT ABSTRACT There is increasing interest regarding the impacts of human activities on the functioning of marine systems. A primary driver of change to marine systems is through the impacts of fishing. Biomass-dominant target species have the potential to mediate a number of ecosystem functions, either directly or indirectly, through the influences that taxa have on ecological processes and/or other biotic or abiotic components of the system. This thesis investigates the roles of the cockle, Cerastoderma edule on ecosystem functioning within intertidal sedimentary systems. A series of investigations revealed that cockles have the potential to mediate benthic primary productivity through their roles in the recycling of nutrients and effects of sediment structure and have impacts upon assemblage biomass and functional diversity. However, the roles of cockles on other aspects of ecological functioning were less apparent. An investigation also assessed the suitability of the use of assigning taxa to functional groups when assessing functional diversity. Taxa were shown to have the potential to change their feeding activity following disturbance, with evidence suggesting a change to benthic-pelagic coupling. This change however, would not have been observed with investigations of functional traits alone and thus supports the use of direct measures of functions to support functional trait diversity measures. It is imperative for ecological investigations to consider long-term changes to population dynamics. However, particularly in marine systems, such data are generally lacking. This thesis presents a novel approach, using information from sea fisheries reports to gain a semi-quantitative 30-year data set on cockle landings within Morecambe Bay, north-west England. This technique revealed evidence of temporal changes to the functional processes at a large scale. This thesis provides evidence for cockles acting as key contributors to ecological functioning. The functional role of cockles is tempered by the high degree of redundancy within these assemblages, highlighting a number of issues relating to the use of field studies and encouraging a move towards increased use of traditional ecology in future studies. i ACKNOWLEDGEMENTS ACKNOWLEDGEMENTS First and foremost, I thank Professor Chris Frid for his supervision of this project and for all his assistance, support and advice. I fully appreciate his patience and his staid reluctance to hand back thoroughly-shredded early drafts of written sections. I also thank the University of Liverpool for their funding of this project. I appreciate the efforts and assistance of Les Connor in the laboratory and for his wry sarcasm. Thanks also to Doctors Conrad Chapman and Stan van den Berg at the Department of Earth and Ocean Sciences for their interest in the project and for allowing me to spend time working with them, and for having the patience to answer my questions regarding electrochemistry. I also thank Professor George Wolff at DEOS for providing me with equipment and information for the measuring of nutrient fluxes and for taking the time to discuss stable isotope analyses. Thank you too to Doctor Julie Bremner for her constructive comments. I massively appreciate and owe a huge debt of thanks to all those who came to help me in the field, braving treacherous muddy sand, beating winds and rain and hauling weighty mud up scenic but almost impassable terrain: Keith Hatton, Rebecca Ahmed, Dave Cavanagh, Sarah Cavanagh, Sarah Fowke, Gregor Govan, Karen Hall, Tom Heyes, Diane Jones, Tom Laughland, Hazel Lewis, Elaine Mayers, Jess Mettam, Katherine Nisbet, Laura Nuttall, Ravi Pandalaneni, Odette Paramor, Leonie Robinson, Valerie Samedi, Delores Sellars, Matt Spencer, Heidi Tillin, Tony Tollitt, Alex Winrow-Giffin, Carl Wright and the rangers and dog based at Wirral Country Park. I am greatly indebted to Bill Cook and Bob Houghton from North West & North Wales Sea Fisheries Committee, whose quad bike handling skills made an almost impossible route into Morecambe Bay merely perilous. I also thank Bob and Bill, along with Mark Prime at the University of Hull for their helpfulness, time and effort in the retrieval and electronic-rendering of information from the SFC’s records. On a personal note, I thank my office mates and the Marine Tea fraternity not already mentioned for idle and inane banter, their (often conflicting) advice and, most-importantly, tea, cake and biscuits: Lucy Abram, Mhari Alexander, Ian Goodhead, Jon Green, Cheryl Knowland, Rob Marrs, Katherine Nisbet, Catherine Scott, Angela Sims and Jack Thomson. ii ACKNOWLEDGEMENTS Outside of the office, I really appreciate the friendship, chit-chat and fun quiz-times I’ve had with: Brian O’Hare, Clare Gabbott, Rich & Ange Midgely, Stephen O’Hare, Kat Smith and Dom Stockton. Cheers also to my brother Andrew for a lifetime of nonsensical banter. I owe a massive debt to my parents. Without their love, support and encouragement, I would never have gotten to this stage: I am truly grateful. Last, but certainly not least, I thank Hayley Smith, for too many reasons to list. I thank you for all your love and for your unconditional support and understanding. Thank you. iii TABLE OF CONTENTS CONTENTS Abstract i Acknowledgements ii Contents iv List of Tables and Figures Tables vii Figures viii Chapter 1: Ecosystem functioning 1.1 Introduction 2 1.2 Taxonomic approaches 3 1.3 Functional group approaches 4 1.4 Multiple functional group approaches 6 1.5 Tidal flat systems and the cockle Cerastoderma edule L. 9 1.6 Thesis overview 11 Chapter 2: Baseline investigations of the faunal assemblage and functional structures of three tidal flats in north-west England 2.1 Introduction 16 2.2 Methods Site description 19 Benthic infaunal analyses: univariate and multivariate analyses 20 Biological traits analysis 22 Sediment granulometry 22 2.3 Results Benthic macrofaunal assemblages 24 Univariate analyses 25 Multivariate analyses 27 Biological traits analysis 29 Sediment granulometry 32 2.4 Discussion 32 Chapter 3: Effects of experimental small-scale cockle (Cerastoderma edule l.) fishing on ecosystem function 3.1 Introduction 38 iv TABLE OF CONTENTS 3.2 Methods Site description and experimental design 41 Infaunal assessment 42 Biological traits analysis 43 Sediment properties and chlorophyll a concentration 43 Statistical analyses 44 3.3 Results Infaunal assemblages 44 Biological traits analysis 48 Sediment properties and chlorophyll a concentration 51 3.4 Discussion 52 Chapter 4: Benthic disturbance affects intertidal food web dynamics: implications for investigations of ecosystem functioning 4.1 Introduction 59 Examination of feeding modes of fauna 61 4.2 Methods Site description and faunal sampling 62 Sample preparation and stable isotope analysis 63 Statistical analyses 65 4.3 Results 66 4.4 Discussion 69 Chapter 5: Density-dependent effects of cockles on nutrient availability 5.1 Introduction 76 5.2 Methods Site description 79 Experimental design and set up 79 Nutrient collection and analysis 80 5.3 Results Cockle retention 81 Cockle density-nutrient concentration relationship 82 5.4 Discussion 86 v TABLE OF CONTENTS Chapter 6: Thirty years of cockle stock variation: The ecological controls within Morecambe Bay 6.1 Introduction 95 Abiotic factors 95 Biotic factors 96 Morecambe Bay cockle fishery and current study 97 6.2 Methods Species data 1: Fishery stocks 99 Species data 2: Birds 100 Environmental data 101 Statistical analyses 101 6.3 Results Cyclicity of cockle populations 103 Factors contributing to extreme population changes 107 Model validity: adult cockles 109 Model validity: cockle spat 111 6.4 Discussion 113 Chapter 7: General discussion 121 Appendix: Does the number of mouths matter? Investigation of the suitability of taxon biomass in ecological investigations 131 References 138 vi LIST OF TABLES LIST OF TABLES Table 2.1. Biological traits and modalities used in the fuzzy coding of taxa for biological traits analysis to describe functional diversity 23 Table 2.2. Taxa contributing the most to macrofaunal abundance and biomass at three shores in north-west England 26 Table 2.3. Results of the calculation of similarity percentages (SIMPER) on assemblages from three study shores 28 Table 2.4. Results of the calculation of similarity percentages (SIMPER) comparing macrofaunal assemblages sampled seasonally from three study shores over 27 months 28 Table 2.5. Relative inertia and correlation ratios of biological traits on the first two axes of the fuzzy correspondence analysis 30 Table 3.1. PERMANOVA and pairwise a posteriori comparisons between faunal biomass compositions within two assemblages under different experimental treatments at two different times 45 Table 3.2. Output of the SIMPER analyses displaying the taxa responsible for 90% of the difference between experimental treatments within two assemblages both in terms of overall differences and over two sampling occasions 47 Table 3.3. Relative inertia and correlation ratios of biological traits on the first two axes of the fuzzy correspondence analysis 49 Table 3.4. Summary of the linear mixed model analyses for the sediment parameters quantified to investigate ecological functions 52 Table 4.1. Taxa selected for stable
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