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A SPECIES-ASSEMBLAGE INVESTIGATION by Andrew David William Tongue Msc, PG Cert, PG Dip, Bsc

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A SPECIES-ASSEMBLAGE INVESTIGATION by Andrew David William Tongue Msc, PG Cert, PG Dip, Bsc GULLS (LARIDAE) AS BIOINDICATORS OF FLAME RETARDANT EMISSIONS FROM LANDFILL: A SPECIES-ASSEMBLAGE INVESTIGATION by Andrew David William Tongue MSc, PG Cert, PG Dip, BSc A thesis submitted to the University of Birmingham for the degree of DOCTOR OF PHILOSOPHY (PhD) Division of Environmental Health and Risk Management College of Life and Environmental Sciences The University of Birmingham Edgbaston Birmingham B15 2TT UK September 2019 University of Birmingham Research Archive e-theses repository This unpublished thesis/dissertation is copyright of the author and/or third parties. The intellectual property rights of the author or third parties in respect of this work are as defined by The Copyright Designs and Patents Act 1988 or as modified by any successor legislation. Any use made of information contained in this thesis/dissertation must be in accordance with that legislation and must be properly acknowledged. Further distribution or reproduction in any format is prohibited without the permission of the copyright holder. ABSTRACT The contamination of free-living avifauna via chemical pollution resulting from anthropogenic activity is globally ubiquitous and poses a threat for avian conservation. Waste streams are important reservoirs of several persistent organic pollutants (POPs), including legacy brominated flame retardants (BFRs). However, landfill is often an important foraging substrate for birds such as gulls (Laridae). Some BFRs are known to exert deleterious effects on birds. Given that lipophilic pollutants sequester in the yolk compartment of avian eggs, this tissue can be an important non-invasive biomonitoring matrix. The primary aim of this thesis was to assess whether gulls breeding in proximity to a UK landfill constitute effective bioindicators of BFR emissions, with an additional aim being the identification of a suitable bioindicator species for future biomonitoring purposes. Polybrominated diphenyl ethers (PBDEs) were detected in substantial concentrations (up to 7,000 ng/g lipid weight) in the eggs of five larid taxa of UK / European conservation concern (black-headed gulls Chroicocephalus ridibundus, common gulls Larus canus, great black-backed gulls L. marinus, European herring gulls L. argentatus and lesser black-backed gulls L. fuscus) breeding in proximity to a municipal solid waste landfill compared to reference conspecifics breeding away from landfill. Mean ∑8 PBDE concentrations in the eggs of landfill-breeding gulls followed lesser black-backed gulls > great black-backed gulls > herring gulls > common gulls > black-headed gulls. The novel brominated flame retardant, DBDPE, was detected in the highest concentrations reported in biota to date globally in the eggs of landfill-breeding great black-backed gulls and herring gulls (up to 8,000 ng/g lw) but was not detected in reference eggs. Given their numerical superiority at the landfill and colonies, the most statistically robust data was obtained for herring gulls. The eggs of landfill- breeding herring gulls exhibited significantly higher burdens of ∑8 PBDEs compared to reference conspecifics (P = 0.02). A significant negative relationship between BDE-209 and δ13C enrichment in eggs indicated that the more terrestrial diets of landfill-breeding herring gulls resulted in them being more exposed to this PBDE congener, formerly widely used in the UK. However, behavioural observations indicated that ingestion of food was unlikely to be the primary pathway of BFR contamination in gulls using landfill, and that dermal contact, respiration and preening may be more important routes of exposure. Notwithstanding the potential conservation implications of herring gull BFR exposure at such sites, this species can be considered an important bioindicator of BFR emissions from municipal solid waste landfill in north-west Europe. DEDICATION This thesis is dedicated to my wonderful daughter Grace, who is well on her way to becoming an outstanding scientist. ACKNOWLEDGEMENTS I owe a tremendous debt of gratitude to my ever-present supervisors Stuart Harrad, Jim Reynolds and Kim Fernie. Working under their combined tutelage was a privilege, allowing me to exploit Stuart’s far-from-common common sense, Jim’s forensic attention to ornithological detail and Kim’s authority as a leading avian toxicologist. Thank you all. I am also indebted to Daniel Drage (University of Birmingham) who undertook the analysis of egg samples for brominated flame retardants and Rona McGill (Scottish Universities Environmental Research Centre) who provided egg stable isotope data. I would like to thank the UK’s Natural Environment Research Council for the funding of my PhD studentship. I would also like to thank the Centre for Ecology and Hydrology for hosting my stay with the Predatory Bird Monitoring Scheme based at the University of Lancaster in autumn 2016. I am grateful to Environment and Climate Change Canada for hosting me at the Canada Centre for Inland Waters for scholarly visits in 2017 and 2018. These visits were funded by the European Union’s Horizon 2020 research and innovation network under the Marie Skłodowska-Curie Actions programme. In addition, I would like to thank the Royal Society of Chemistry, the Seabird Group and the Waterbird Society for the provision of additional funds. I am also grateful to Mohamed Abdallah, John Bowler, Clive Craik, David Jardine, Henk Krajenbrink, Ruedi Nager, Ian Newton, Nina O’Hanlon, Peter Rock, Jon Sadler, Richard Shore and Shane de Solla for their advice and insight. I would like to thank all those County Bird Recorders who kindly provided data on the landfills used by gulls and their breeding colonies across the UK. I am grateful to Scottish Natural Heritage for granting me licences to collect gull eggs. I want to say a very big thank you to my daughter Grace for putting up with Dad being away in Birmingham, Canada and Scotland for long periods. Finally, but by no means least, thank you to my parents Linda and David, for their love and support. TABLE OF CONTENTS CHAPTER I ......................................................................................................................... 1 1.1 Birds as bioindicators............................................................................................................. 4 1.2 Landfill as a source of environmental BFR contamination ..................................................... 6 1.3 Bird utilisation of landfill ....................................................................................................... 7 1.4 BFR contamination in bird populations associated with landfill ............................................. 8 1.5 Routes of BFR exposure, toxicokinetics and toxicity ........................................................... 16 1.5.1. Polybrominated diphenyl ethers (PBDEs) ................................................................ 17 1.5.2 Hexabromocyclododecane (HBCDD) ...................................................................... 20 1.5.3 NBFRs .......................................................................................................................... 20 1.6 Summary of research to date ................................................................................................ 21 1.7 Aims, objectives, working hypotheses and structure of this thesis ........................................ 22 CHAPTER II ...................................................................................................................... 24 2.1 Field sampling ..................................................................................................................... 24 2.1.1 Study area ..................................................................................................................... 24 2.1.2 Vantage point surveys of gull flightlines ........................................................................ 29 2.1.3 Egg sampling ................................................................................................................ 30 2.2 Egg processing .................................................................................................................... 35 2.3 Laboratory analysis of BFR concentrations in eggs .............................................................. 36 2.3.1 Validation and QA/QC criteria ...................................................................................... 37 2.3.2Analyte identifcation and quantification criteria ............................................................. 37 2.3.3 Determination of internal standard recovery .................................................................. 38 2.3.4 Validation of method and ongoing accuracy and precision ............................................ 40 2.3.5 Analysis of blanks, LODs and LOQs ............................................................................. 43 2.4 Stable isotope analysis (SIA) of egg contents ....................................................................... 44 2.5 Foraging and loafing behaviours of gulls at the study landfill ............................................... 46 2.5.1 Data extraction of foraging behaviour from video recordings ........................................ 50 2.6 Statistical analyses ............................................................................................................... 51 CHAPTER III .................................................................................................................... 53 3.1 Synopsis .............................................................................................................................
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