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Burrowing and Feeding Ecology of the Ghost Shrimp Biffarius Arenosus (Decapoda: Callianassidae)

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Burrowing and Feeding Ecology of the Ghost Shrimp Biffarius Arenosus (Decapoda: Callianassidae) BURROWING AND FEEDING ECOLOGY OF THE GHOST SHRIMP BIFFARIUS ARENOSUS (DECAPODA: CALLIANASSIDAE). Thesis submitted in fulfilment of the requirements for the degree of Doctor of Philosophy of Victoria University of Technology by Fiona Louise Bird B.Sc. (Hons) Department of Biological and Food Sciences Faculty of Science Victoria University of Technology November, 1997 THESIS 595.3887 BIR 30001005348901 Bird, Fiona L Burrowing and feeding ecology of the ghost shrimp Biffarius arenosus Frontispiece Bijfarius arenosus 11 DECLARATION The research in this thesis has not been previously submitted for a degree or diploma in any University. The thesis contains no material that has been previously published or written by another person, except where due reference is made in the thesis itself. FIONA L. BIRD ni ABSTRACT The thalassinidean ghost shrimp, Biffarius arenosus (Decapoda: Callianassidae), is a dominant component of coastal soft sediment communities in temperate south-eastern Australia. This thesis investigated the burrowing and feeding ecology of a population of shrimps inhabiting an intertidal sandflat in Western Port, Victoria. Biffarius arenosus constructs dynamic, unlined burrows with a complex shape indicating that the shrimps exploit the subsurface food supply. A multiple stable isotope study revealed that the food source was sedimentary organic matter, primarily derived from decomposing seagrass and seagrass epiphytes. Feeding and burrowing activity of the shrimps resulted in comparatively larger particles being ejected from burrows to the sediment surface. An investigation of the impact of burrowing and feeding activity on physiochemical and microbial properties of the sediment revealed that the burrow wall sediments were relatively more oxidised (measured via platinum redox electrodes) and had higher microbial enzyme activity rates (quantified via the hydrolysis of fluorescein diacetate) than surrounding subsurface sediments. Grazing by B. arenosus appeared to affect bacterial abundance (estimated with DAPI epifluorescent counts) in the burrow wall. Other properties of the burrow, such as organic carbon content (measured using a wet digestion technique) and microbial community structure (studied by examining phospholipid fatty acid profiles), did not differ between burrow wall, surrounding subsurface and surface sediments. The combination of active and passive burrow irrigation and an increase in the water-sediment interface surface area (caused by the presence of irrigated burrows in usually anoxic sediments), enhanced the diffusive flux of water from the sediments (quantified using a non-reactive tracer) by 400%. This research indicated that B. arenosus has a significant impact on the biogeochemistry of the marine sediments of Western Port. IV ACKNOWLEDGMENTS A thesis such as this cannot be completed with out assistance from many people, and to all of those who helped and supported me, I express my sincere thanks and gratitude. Many thanks to my principal supervisors, Dr Paul Boon and Dr Gary Poore, for their continual help, encouragement and guidance over the past four years. Their support was invaluable. Thanks also to Dr Nick O'Connor for assisting during the conception stages of the project and for contributing ideas along the way. The Crustacea laboratory (Museum of Victoria) was an excellent place for hght relief during the long, dark thesis writing months. Thanks to all my friends there for their help, moral support and passion for cake. A special thanks to Robin Wilson for his enthusiasm for the wonderful world of burrows. Thanks to all the postgraduate students and staff in the Department of Environmental Management and the Department of Biological and Food Sciences for making Victoria University of Technology (VUT) an enjoyable place to work. A number of VUT technical staff provided assistance with field work, chemical methods, use of equipment and photography. Phillip Holgate and Kylie Ridgeway deserve a special mention. I was privileged to be part of some collaborations which resulted in valuable data for this thesis. Thanks to Dr Phillip Ford for the inspiring weeks we spent investigating aspects of bioturbation, and to Dr Peter Nichols for sharing his phospholipid expertise with me. I have had financial assistance from several sources, without which sections of the project would not be possible: the stable isotope work was funded by a VUT Seeding Grant and Melbourne Water (through the Port Phillip Bay Environmental Study) funded the diffusive flux experiment. I also received considerable financial assistance from my departments and the VUT Secomb Travel Fund for conference travel. Thanks to Nick O'Connor, Alistair Hirst, Simon Heislers and Richard Marchant for statistical advice, and Kate Thompson for help with illustrations. Thanks to Anthony Boxshall and Ely Wallis for advice on how to write a PhD thesis, and to John Wright for his memorable words which got me through some long days "Just keep going!". Thanks to Selby Steele, Vernon Steele, Chris Tudge and Chris Bird for editing sections of the tome, especially Selby who read it from cover to cover. I extend my warmest thanks to my extended family for their love and support and for knowing when not to ask "How is the thesis writing going?" and "Do you know when you will be finished?". Finally, sincere thanks to Vernon Steele for surviving the PhD process with me, sharing the highs and lows, and for his unquestioning faith in my ability. VI TABLE OF CONTENTS Declaration iii Abstract iv Acknowledgments v Table of contents vii Chapter 1 Introduction 1.1 General overview 1 1.2 Thalassinidean fauna 2 1.3 Biffarius arenosus 3 1.4 The thalassinidean burrow 3 1.5 Thalassinidean feeding 5 1.6 Feeding and burrowing activity 6 1.7 The burrow environment 6 1.8 Aims of this study 8 1.9 Format of this thesis 9 Chapter 2 Burrow structure 2.1 Introduction 11 2.2 Methods 12 2.2.1 Study site 12 2.2.2 Burrow casting 14 2.3 Results 14 2.4 Discussion 22 2.4.1 Burrow features 22 2.4.2 Functional morphology of 5. arenosus burrows - can trophic mode be predicted? 28 Chapter 3 Feeding 3.1 What does Biffarius arenosus eat? 3.1.1 Introduction 30 3.1.2 Gut content analysis 31 3.1.2.1 Methods 31 3.1.2.2 Results and discussion 32 3.1.3 Preference experiments 32 3.1.3.1 Methods 32 3.1.3.2 Results and discussion 32 3.2 Stable isotope analysis 3.2.1 Introduction 35 3.2.2 Methods 36 3.2.2.1 Sample collection 36 3.2.2.2 Laboratory methods 37 3.2.2.3 Stable isotope analysis 37 3.2.2.4 Distinguishing potential food sources for Biffarius arenosus 38 3.2.3 Results 39 vu 3.2.3.1 Isotopic signature for Biffarius arenosus and potential food sources 39 3.2.3.2 Delimiting food sources 42 3.2.4 Discussion 44 3.3 Where is food collected from? 3.3.1 Introduction 50 3.3.2 Methods 50 3.3.3 Results and Discussion 51 3.4 Do the burrows indicate active searching for food? 3.4.1 Introduction 53 3.4.2 Methods 54 3.4.3 Results and Discussion 56 3.5 Sediment sorting 3.5.1 Introduction 59 3.5.2 Methods 60 3.5.2.1 Population density 60 3.5.2.2 Sediment ejection rates 61 3.5.2.3 Particle size 63 3.5.3 Results 63 3.5.3.1 Population density 63 3.5.3.2 Sediment ejection rates 64 3.5.3.3 Particle size 65 3.5.4 Discussion 72 3.5.4.1 Population density 72 3.5.4.2 Sediment ejection rates 72 3.5.4.3 Particle size 73 3.6 Chapter summary 76 Chapter 4 Physical characteristics of the burrow environment 4.1 Organic carbon content 4.1.1 Introduction 77 4.1.2 Methods 78 4.1.3 Results 79 4.1.4 Discussion 81 4.2 Burrow lining 4.2.1 Introduction 84 4.2.2 Methods 85 4.2.2.1 Physical description of burrow lining 85 4.2.2.2 Presence of mucopolysaccharides 85 4.2.3 Results 86 4.2.3.1 Physical description of burrow lining 86 4.2.3.2 Presence of mucopolysaccharides 86 4.2.4 Discussion 86 4.3 Redox potential 4.3.1 Introduction 90 4.3.2 Methods 91 4.3.2.1 Equipment 91 4.3.2.2 Redox stability trials 92 4.3.2.3 Laboratory measurements 92 4.3.2.4 In situ measurements 95 Vlll 4.3.2.5 Statistical analysis 96 4.3.3 Results 96 4.3.3.1 Laboratory measurements 96 4.3.3.2 In situ measurements 96 4.3.4 Discussion 101 4.3.4.1 Laboratory measurements 101 4.3.4.2 In situ measurements 101 4.3.4.3 Interpretation of Eh measurements 102 4.4 Diffusive flux of a non-reactive tracer 4.4.1 Introduction 104 4.4.2 Methods 105 4.4.2.1 Burrow surface area 105 4.4.2.2 Measurement of diffusive flux of a non-reactive tracer 105 4.4.2.2.1 Experiment overview 105 4.4.2.2.2 Experimental details 106 4.4.2.2.3 Analysis of data 107 4.4.3 Results 108 4.4.3.1 Burrow surface area 108 4.4.3.2 Diffusive flux of D2O 110 4.4.4 Discussion 112 4.4.4.1 Burrow surface area 112 4.4.4.2 Diffusive flux of D2O 113 4.5 Chapter summary 116 Chapter 5 Microbial characteristics of the burrow environment 5.1 Abundance of bacteria 5.1.1 Introduction 117 5.1.2 Methods 119 5.1.2.1 Methodological trials 119 5.1.2.1.1 Staining bacteria 119 5.1.2.1.2 Validation trials 121 5.1.2.2 Seasonal study 126 5.1.2.3 Statistical analysis 126 5.1.3 Results 127 5.1.4 Discussion 129 5.2 Microbial activity 5.2.1 Introduction 133 5.2.2 Methods 134 5.2.2.1 Methodological trials 134 5.2.2.1.1 Tetrazolium salt (INT) reduction 135 5.2.2.1.2 Fluorescein diacetate 138 5.2.2.2 Seasonal study 141 5.2.2.3 Statistical analysis 144 5.2.3 Results 145 5.2.3.1 Problems with homogeneity of variances 145 5.2.3.2 Microbial activity at in situ temperatures 146 5.2.3.3 The effect of temperature on microbial activity 146 5.2.4 Discussion 149 IX 5.3 Microbial biomass and community structure 5.3.1 Introduction 152 5.3.2 Methods
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