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University of Southampton Research Repository Eprints Soton 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 Engineering, Science and Mathematics School of Civil Engineering and the Environment Heavy Metal Pollution and Black- headed Gull ( Larus ridibundus L.) Breeding Ecology Kirsty Louise Pickard Thesis for the degree of Doctor of Philosophy May 2010 UNIVERSITY OF SOUTHAMPTON ABSTRACT FACULTY OF ENGINEERING, SCIENCE AND MATHEMATICS SCHOOL OF CIVIL ENGINEERING AND THE ENVIRONMENT Doctor of Philosophy TITLE OF THESIS: HEAVY METAL POLLUTION AND BLACK-HEADED GULL ( LARUS RIDIBUNDUS L.) BREEDING ECOLOGY Author: Kirsty Louise Pickard Heavy metals in air, soil and water are a global problem and present a growing threat to the environment. These metals may have profound consequences for birds and can cause a number of sub-lethal effects, such as decreased reproductive success. The concentrations of selected heavy metals (As, Cd. Co, Cu, Fe, Pb, Mn, Ni, V, Zn) and Se in eggs and feathers from populations of black-headed gulls ( Larus ridibundus L.) located on different colonies in the UK, which have different characteristics and are subject to different sources, types and degrees of pollution, were examined. Concentrations of As, Cu, Pb, Ni, Se and V measured in black-headed gull eggs were consistently high relative to those reported in previous field studies with other gull species. However, no significant effect was observed on the egg characteristics in terms of egg size and dimensions, shell thickness and index as a result of concentrations of metals measured in this study. Concentrations of Co, Fe and Ni were significantly negatively correlated with yolk:albumen ratio in the egg. The usefulness of sampling eggs to provide a reflection of local contamination has been demonstrated, with concentrations related to local sources of metal pollution and site differences reflected in sediment concentrations from previous studies. The importance of taking into account diffuse and historical pollution in addition to point source discharges has also been highlighted. As, Fe, Mn, Pb, Se, V and Zn were found at significantly higher concentrations in egg contents than egg shell, and Cd, Co and Ni concentrations were higher in shell than contents. Cu was distributed approximately equally. Within the egg contents, concentrations of As, Cu, Se and V were higher in the albumen than in the yolk, and Co, Fe, Mn, Ni, Pb and Zn concentrations were higher in the yolk than the albumen. Cd was found mainly in the shell and concentrations in egg contents were largely undetectable. Comparisons were made between a colony subject to high-level commercial egg harvesting and an un-harvested site, and between pre- and post-harvesting eggs on the harvested site. Post- collection eggs were found to be of significantly lower quality than the pre-collection eggs and the eggs from the uncollected site, as indicated by yolk:albumen ratio. Concentration of metals in eggs as a result of relaying forced by commercial harvesting has been demonstrated, with concentrations of Co, Fe and Ni significantly higher in post-collection eggs compared to pre- collection eggs. Average nesting density was significantly lower on the collected colony than the uncollected colony. No effect on egg size was found as a result of changes in nesting density. Concentrations of metals in black-headed gull chick down were measured and compared to egg data in order to assess the usefulness of feathers as a tool for non-destructive monitoring of metal pollution. The results suggest that feathers may be good indicators for As and Zn, and possibly also for Mn and Ni. However, the sample masses were very small and for a number of metals concentrations were largely undetectable using the analytical equipment available in this study. Future work with larger samples of down would be prudent to further examine the use of chick down to provide an indication of the level of pollution to which birds are exposed. The importance of using appropriate washing procedures to remove exogenous contamination of feathers to assess internal concentrations has been demonstrated. ii CONTENTS Page LIST OF TABLES VI LIST OF FIGURES X LIST OF APPENDICES XV DECLARATION OF AUTHORSHIP XVI ACKNOWLEDGEMENTS XVII LIST OF ABBREVIATIONS XVIII CHAPTER 1. GENERAL INTRODUCTION 1 1.1 Seabirds as monitors of pollution 3 1.2 Eggs as indicators of pollution 8 1.2.1 Effects of pollution on eggshell thickness 10 1.2.2 Partitioning of metals in the egg 12 1.3 Feathers as indicators of pollution 13 1.4 Nesting density and breeding success 16 1.5 Black-headed gulls ( Larus ridibundus L.) 17 1.5.1 Egg laying and commercial egg collecting 20 1.6 Study areas 23 1.6.1 Lymington 26 1.6.2 Poole Harbour 27 1.6.3 Raby Estate 29 1.7 Project aims and objectives 31 1.7.1 Aims 31 1.7.2 Objectives 31 1.8 Thesis outline 33 CHAPTER 2. HOW DO THE SIZE, DIMENSIONS AND COMPOSITION OF BLACK-HEADED GULL EGGS VARY BETWEEN SITES? 35 2.1 Introduction 35 2.1.1 Egg size and composition 35 2.1.2 Eggshell thickness and shell index 38 2.1.3 Impacts of egg harvesting on egg quality 40 2.2 Methods 40 2.2.1 Egg collection: 2005 & 2006 40 2.2.2 Egg measurements 41 2.3 Results 43 2.4 Discussion 51 iii 2.5 Summary 55 CHAPTER 3. IMPACTS OF NESTING DENSITY ON EGG SIZE IN BLACK-HEADED GULLS 58 3.1 Introduction 58 3.1.1 Nest density 58 3.1.2 Egg size 62 3.1.3 Effects of commercial egg harvesting 62 3.2 Methods 62 3.3 Results 64 3.3.1 Egg length and breadth 64 3.3.2 Egg volume 69 3.3.3 Comparison of nest density and egg size between sites 72 3.3.4 Comparison of egg size with nest location 75 3.4 Discussion 77 3.4.1 Nest density, nest location and egg size 77 3.4.2 Effect of commercial egg harvesting on egg size and nest density 80 3.5 Summary 81 CHAPTER 4. POTENTIAL SOURCES OF POLLUTION AROUND THE LYMINGTON, POOLE AND RABY SITES 83 4.1 Geology 84 4.2 Land use 84 4.3 Industry and waste 86 4.4 Boats and shipping 88 4.5 Lymington Estuary 90 4.5.1 Geology 90 4.5.2 Land use 90 4.5.3 Industry and waste 92 4.5.4 Boats and shipping 100 4.6 Poole Harbour 102 4.6.1 Geology 102 4.6.2 Land use 102 4.6.3 Industry and waste 104 4.6.4 Boats and shipping 112 4.7 Raby Estate 113 4.7.1 Geology 113 4.7.2 Land use 113 4.7.3 Industry and waste 115 4.8 Summary of sources 121 4.8.1 Point sources 121 4.8.2 Non-point sources 122 CHAPTER 5. HEAVY METALS AND SELENIUM IN BLACK-HEADED GULL EGGS 125 5.1 Introduction 125 5.1.1 Environmental fate and toxicity 126 5.1.2 Heavy metals and selenium in eggs 142 iv 5.1.3 Partitioning of metals in eggs 160 5.2 Methods 161 5.2.1 Results of initial trials 163 5.3 Results 165 5.3.1 Relationship between metal concentrations and egg characteristics 165 5.3.2 Total metal concentrations in the egg 166 5.3.3 Metal partitioning in the egg 178 5.4 Discussion 188 5.4.1 Impacts of metal concentrations on egg parameters 188 5.4.2 Comparison of metal concentrations in eggs between sites 191 5.4.3 Potential impacts of metal concentrations in eggs on the breeding success of black-headed gulls 195 5.4.4 Differences in metal concentrations in black-headed gull eggs pre- and post-harvesting 202 5.4.5 Metal partitioning in the egg 203 5.5 Summary 206 CHAPTER 6. HEAVY METALS AND SELENIUM IN BLACK-HEADED GULL FEATHERS 208 6.1 Introduction 208 6.1.1 Lead and cadmium in feathers 217 6.1.2 Other metals in feathers 219 6.2 Methods 220 6.2.1 Results of initial trials 222 6.3 Results 224 6.4 Discussion 232 6.4.1 Comparison between sites and with egg concentration data 232 6.4.2 Comparison with literature data 237 6.5 Summary 237 CHAPTER 7. GENERAL DISCUSSION 239 7.1 Heavy metals in black-headed gull eggs and feathers 240 7.2 Impacts of commercial egg harvesting 245 7.3 Future work 247 7.4 Concluding remarks 250 v LIST OF TABLES Table 1-1 Common sources of metal pollution 1 Table 1-2 Sub-lethal effects of metals on birds 5 Table 1-3 Characteristics of Lymington, Poole and Raby sites 25 Table 2-1 ANOVA results for comparison of characteristics of black- headed gull eggs between sites, 2005-2006 49 Table 2-2 Tukey test results for comparison of characteristics of black- headed gull eggs between sites, 2005-2006 50 Table 2-3 Comparison of egg length, breadth and volume in black- headed gull eggs from various sites worldwide 55 Table 3-1 Test results for comparison of Lymington and Poole nesting densities and egg size characteristics for black-headed gulls, 2007 73 Table 3-2 Independent t-test results for comparison of egg size with nest location (centre of colony vs edge of colony) for black-headed gulls, Lymington and Poole sites, 2007 77 Table 4-1 Metals released to water (kg/year) from industry around the Lymington site (map references refer to Figure 4-1) 96 Table 4-2 Metals released to air (kg/year) from
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