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A Multidisciplinary Study on the Ecological Success of an Estuarine Dweller

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A Multidisciplinary Study on the Ecological Success of an Estuarine Dweller Hide and seek: a multidisciplinary study on the ecological success of an estuarine dweller Andjin Siegenthaler This thesis is presented to the School of Environment & Life Sciences, University of Salford, in fulfilment of the requirements for the degree of Ph.D. Supervised by Dr Chiara Benvenuto & Prof Stefano Mariani December 2017 Image of a black and a white brown shrimp Crangon crangon (L.) after acclimation on black and white sediment, respectively. Pigments are visible within chromatosomes beneath the translucent exoskeleton. The location of the stomach is also visible below the carapace of the white shrimp. Table of contents Table of contents TABLE OF CONTENTS I LIST OF FIGURES IV LIST OF TABLES VI ACKNOWLEDGEMENTS VIII LIST OF ABBREVIATIONS X ABSTRACT XI CHAPTER 1. INTRODUCTION AND BACKGROUND 1 1.1. INTRODUCTION 1 1.2. THE STUDY ORGANISM: CRANGON CRANGON 2 1.2.1. GEOGRAPHICAL DISTRIBUTION AND HABITAT 3 1.2.2. LIFE HISTORY 3 1.2.3. DIET 4 1.2.4. PREDATION 6 1.2.5. IMPORTANCE FOR FISHERIES 6 1.3. ANIMAL CAMOUFLAGE AND COLOUR CHANGES 6 1.4. BENTHIC COMMUNITY AND TROPHIC METABARCODING 9 1.4.1. METABARCODING OF ENVIRONMENTAL AND COMMUNITY SAMPLES 9 1.4.2. TROPHIC METABARCODING 11 1.5. AIMS AND OBJECTIVES 12 CHAPTER 2. QUANTIFYING PIGMENT COVER TO ASSESS VARIATION IN ANIMAL COLOURATION 13 2.1. ABSTRACT 13 2.2. INTRODUCTION 14 2.3. MATERIAL AND METHODS 17 2.3.1. PROTOCOL TO MEASURE PIGMENT COVER 17 2.3.2. CASE STUDY 19 2.4. RESULTS 24 2.4.1. DARK AND LIGHT PIGMENT MEASUREMENTS AND TRANSPARENCY 24 2.4.2. DARK PIGMENT COVER AND CHROMATOPHORE INDEX COMPARISON 24 2.5. DISCUSSION 26 CHAPTER 3. BACKGROUND MATCHING IN THE BROWN SHRIMP CRANGON CRANGON: ADAPTIVE CAMOUFLAGE AND BEHAVIOURAL-PLASTICITY 29 3.1. ABSTRACT 29 3.2. INTRODUCTION 30 3.3. METHODS 33 3.3.1. COLLECTION AND MAINTENANCE OF THE TEST ORGANISMS 33 3.3.2. COLOUR MEASUREMENTS 33 3.3.3. BIORHYTHM 34 3.3.4. BACKGROUND MATCHING 34 3.3.5. DATA ANALYSES 36 i Table of contents 3.4. RESULTS 37 3.4.1. BIORHYTHM 37 3.4.2. REPEATED BACKGROUND CHANGES 37 3.4.3. SEDIMENT VS. BEAKER COLOUR 38 3.4.4. BURYING INHIBITION 39 3.4.5. LONG TERM ADAPTATION 40 3.5. DISCUSSION 42 CHAPTER 4. DNA METABARCODING UNVEILS MULTI-SCALE TROPHIC VARIATION IN A WIDESPREAD COASTAL OPPORTUNIST 47 4.1. ABSTRACT 47 4.2. INTRODUCTION 48 4.3. METHODS 51 4.3.1. SAMPLE COLLECTION AND PROCESSING 51 4.3.2. DNA EXTRACTION 51 4.3.3. DNA AMPLIFICATION AND HIGH-THROUGHPUT SEQUENCING 52 4.3.4. BIOINFORMATIC AND DATA ANALYSES 54 4.4. RESULTS 56 4.4.1. COLLECTION STATISTICS 56 4.4.2. HIGH-THROUGHPUT DNA SEQUENCING 56 4.4.3. DESCRIPTION OF CRANGON CRANGON DIET 57 4.4.4. VARIATION BETWEEN ESTUARIES 61 4.5. DISCUSSION 65 4.5.1. EVALUATION OF C. CRANGON DIET 65 4.5.2. THE APPLICATION OF METABARCODING IN CRUSTACEAN TROPHIC STUDIES 67 4.5.3. GEOGRAPHIC VARIATION IN C. CRANGON TROPHIC ECOLOGY 69 4.5.4. CRANGON CRANGON’S ECOLOGICAL ROLE 70 4.5.5. CONCLUSIONS 71 CHAPTER 5. THE APPLICATION OF TROPHIC MOLECULAR ECOTOXICOLOGY IN THE BROWN SHRIMP, CRANGON CRANGON, FOR ENVIRONMENTAL ASSESSMENTS IN EUROPEAN ESTUARIES 73 5.1. ABSTRACT 73 5.2. INTRODUCTION 74 5.3. METHODS 76 5.3.1. SAMPLE COLLECTION AND PROCESSING 76 5.3.2. HEAVY METAL DETERMINATION 78 5.3.3. DNA EXTRACTION, HIGH-THROUGHPUT AND BIOINFORMATIC ANALYSES 78 5.3.4. DATA ANALYSES 79 5.4. RESULTS 81 5.4.1. HEAVY METAL CONCENTRATIONS IN SEDIMENT AND TISSUE SAMPLES 81 5.4.2. MOTU RICHNESS 84 5.4.3. MULTIVARIATE ANALYSES ON COMMUNITY STRUCTURE 85 5.4.4. RELATIVE ABUNDANCES 87 5.5. DISCUSSION 89 5.5.1. HEAVY METAL ACCUMULATION IN SEDIMENT AND TISSUE SAMPLES 89 5.5.2. BENTHIC COMMUNITY RESPONSES TO HEAVY METAL POLLUTION 91 5.5.3. VARIATION IN CRANGON CRANGON DIET IN RELATION TO HEAVY METAL POLLUTION 91 5.5.4. CONCLUSIONS AND RECOMMENDATIONS 93 ii Table of contents CHAPTER 6. METABARCODING OF SHRIMP STOMACH CONTENT: HARNESSING A NATURAL SAMPLER FOR FISH BIODIVERSITY MONITORING 96 6.1. ABSTRACT 96 6.2. INTRODUCTION 97 6.3. METHODS 100 6.3.1. SAMPLE COLLECTION AND PROCESSING 100 6.3.2. DNA EXTRACTION 101 6.3.3. DNA AMPLIFICATION AND HIGH-THROUGHPUT SEQUENCING 102 6.3.4. BIOINFORMATIC AND DATA ANALYSES 104 6.4. RESULTS 106 6.4.1. MOLECULAR BIODIVERSITY ASSESSMENT 106 6.4.2. COMPARISON OF 12S AND COI MOLECULAR MARKERS AND SAMPLE TYPES 108 6.4.3. GEOGRAPHICAL DIFFERENCES 112 6.5. DISCUSSION 115 6.5.1. GEOGRAPHICAL VARIATION 116 6.5.2. MARKER AND DNA MEDIUM CHOICE 117 6.5.3. APPLICATIONS IN FISHERIES AND ENVIRONMENTAL SCIENCES 118 CHAPTER 7. GENERAL DISCUSSION 121 7.1. MAIN FINDINGS 121 7.2. INDIVIDUAL VARIABILITY AND SURVIVAL IN ESTUARIES 122 7.3. HIDE AND SEEK 123 7.4. IMPLICATIONS FOR ECOSYSTEM MANAGEMENT 126 7.5. FUTURE DIRECTIONS 127 7.6. FINAL CONCLUSIONS 129 REFERENCES 130 APPENDIX 1. GLOSSARY OF TERMS 156 APPENDIX 2. SUPPLEMENTARY MATERIAL FOR CHAPTER 2 158 APPENDIX 3. SUPPLEMENTARY MATERIAL FOR CHAPTER 4 160 APPENDIX 4. SUPPLEMENTARY MATERIAL FOR CHAPTER 4 163 APPENDIX 5. SUPPLEMENTARY MATERIAL FOR CHAPTER 5 167 APPENDIX 6. SUPPLEMENTARY MATERIAL FOR CHAPTER 6 168 iii List of figures List of figures Figure 1.1. Photo of Crangon crangon 2 Figure 1.2. Image showing pigments within chromatosomes on the dorsal side of Crangon 8 crangon Figure 2.1. Stylised representation of the different classes of pigment dispersion in 15 Crangon crangon Figure 2.2. Protocol for pigment cover measurements 18 Figure 2.3. Pigment and transparency values for cover and Chromatophore Index for five 21 shrimp (Crangon crangon) on different backgrounds Figure 2.4. Percentage dark pigment cover and Chromatophore Index of 50 images 23 (1mm2) of Crangon crangon’s exopods Figure 2.5. Relationship between Chromatophore Index and dark pigment cover fraction 25 Figure 3.1. Crangon crangon colour 32 Figure 3.2. Schematic overview of the different protocols to determine the factors 35 involved in Crangon crangon background matching Figure 3.3. Effect of background colour and light on Crangon crangon mean dark pigment 37 cover over a day-night cycle Figure 3.4. Box-and-whisker plots of dark pigment cover during repeated shifts of Crangon 38 crangon between black and white backgrounds Figure 3.5. Box-and-whisker plots of dark pigment cover of Crangon crangon kept for 24h 39 in beakers with different combinations of sediment and beaker colours Figure 3.6. Effect of burying inhibition on Crangon crangon colour change 40 Figure 3.7. Effect of long term background adaptation on Crangon crangon colour changes 41 Figure 3.8. Examples of Crangon crangon’s variation in natural colouration 44 Figure 4.1. Overview of sample locations 52 Figure 4.2. Relative abundances of MOTUs detected in Crangon crangon stomach samples 58 by COI metabarcoding Figure 4.3. Relative abundances of MOTUs detected in sediment samples 60 Figure 4.4. Phyla detected in sediment and Crangon crangon stomach samples by COI 62 metabarcoding Figure 4.5. Multidimensional scaling analysis of MOTUs detected in sediment and Crangon 63 crangon stomach samples Figure 4.6. Multivariate analysis of Crangon crangon diet in six estuaries determined by 63 COI metabarcoding based on MOTUs over all stomach samples Figure 4.7. MOTU accumulation curves showing MOTU richness in Crangon crangon 64 pooled stomach samples in several European estuaries Figure 4.8. Schematic representation of the most important food items of adult Crangon 72 crangon and their probable method of capture/ingestion Figure 5.1. Overview of sample locations 77 Figure 5.2. Mean variation in heavy metal element concentrations (ppm dw) between 81 estuaries measured in sediment samples and C. crangon tissue samples. Figure 5.3. Principle component analysis scores and vectors for environmental variables 83 and heavy metal element concentrations measured in sediment samples (Al- normalised) and Crangon crangon tissue samples Figure 5.4. Canonical correspondence analysis of presence-absence data of MOTUs 86 detected in sediment samples collected in 6 estuaries Figure 5.5. Canonical correspondence analysis (CCA) of presence-absence data of annelid 87 MOTUs detected in pooled Crangon crangon stomach samples in relation to salinity, median grain size and bioaccumulated heavy metal elements Figure 6.1. Overview of sample locations 101 iv List of figures Figure 6.2. Heatmap fish species and genera detected in samples taken from Dutch, UK 107 and Portuguese estuaries Figure 6.3. MOTU accumulation curves representing the number of bony fish MOTUs 108 identified to the species or genus level detected in sediment and Crangon crangon pooled stomach samples analysed with two different primer pairs Figure 6.4. Venn diagrams of fish families, genera and species detected in the DNA of 109 Crangon crangon stomach pooled samples amplified with two different primer pairs; Crangon crangon pooled stomach and sediment samples amplified with MiFish primers; DNA amplified with MiFish primers of Crangon crangon pooled stomach, sediment and water samples collected in the Tees and Tweed estuaries in the UK Figure 6.5. MOTU accumulation curves for the number of bony fish MOTUs and taxa 112 identified to the species or genus level detected in DNA extracted from sediment and Crangon crangon pooled stomach samples collected in different countries Figure 6.6. Boxplots showing differences in bony fish MOTU richness per estuary for 113 Crangon crangon stomach samples and sediment samples amplified with 12S MiFish primer pair, and C. crangon stomach samples amplified with COI Leray-XT primer pair Figure 6.7.
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