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The Transfer and Ecological Effects of Xenobiotic Pollution in Freshwater Ecosystems

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The transfer and ecological effects of xenobiotic pollution in freshwater ecosystems Thesis submitted for the degree of Doctor of Philosophy by Fredric Morgan Windsor, BSc. (Hons) MSc. School of Biosciences Cardiff University April 2019 Declaration This work has not been submitted in substance for any other degree or award at this or any other university or place of learning, nor is being submitted concurrently in candidature for any degree or other award. Signed ………………………… (candidate) Date ………………………… This thesis is being submitted in partial fulfilment of the requirements for the degree of PhD. Signed ………………………… (candidate) Date ………………………… This thesis is the result of my own independent work/investigation, except where otherwise stated. Other sources are acknowledged by explicit references. The views expressed are my own. Signed ………………………… (candidate) Date ………………………… I hereby give consent for my thesis, if accepted, to be available for photocopying and for inter-library loan, and for the title and summary to be made available to outside organisations. Signed ………………………… (candidate) Date ………………………… I hereby give consent for my thesis, if accepted, to be available for photocopying and for inter-library loans after expiry of a bar on access previously approved by the Academic Standards & Quality Committee. Signed ………………………… (candidate) Date ………………………… “As crude a weapon as the cave man's club, the chemical barrage has been hurled against the fabric of life – a fabric on the one hand delicate and destructible, on the other miraculously tough and resilient, and capable of striking back in unexpected ways.” Silent Spring, Rachel Carson (1962) Summary 1. The diversity of synthetic, xenobiotic chemicals reaching the wider environment has increased rapidly over the past century. The nature and severity of their ecological effects in freshwater systems, however, remains poorly understood, even for the so-called ‘legacy’ pollutants. These persistent, bioaccumulative and toxic compounds still risk having negative effects at all levels of biological organisation long after their initial release into the environment. 2. The ability to determine the ecological risks posed by persistent pollutants remains restricted due to: (1) reliance on standardised toxicology testing on individuals in the laboratory; (2) limited understanding of how spatial and biological variation alters potential ecological effects at population, community and food web levels; and (3) poor knowledge of how pollutant bioaccumulation and biomagnification translate to effects in natural ecosystems. 3. Through global, catchment and reach-scale empirical assessments, this thesis investigated spatial and biological variation, trophic transfers and ecological risk in freshwater ecosystems associated with persistent xenobiotic pollutants (polychlorinated biphenyls [PCBs], polybrominated diphenyl ethers [PBDEs] and organochlorines [OCs]). 4. The transfer, accumulation and magnification of persistent pollutants were related to site-specific environmental conditions, biological traits, food web structure and chemical characteristics, and were sufficient for widespread, hazardous levels of contamination. Across river systems, pollutant body burdens could be linked to putative structural and functional effects that appeared to be networked through food webs. 5. Overall, these data indicate the importance of natural processes in influencing the potential effects of persistent pollutants in freshwater ecosystems. Risk assessments that incorporate the variation present in natural systems are required to improve understanding of the role of xenobiotic pollutants in global environmental change across freshwater ecosystems. I Acknowledgements This research was funded by a studentship from the Great Western Four Plus Doctoral Training Partnership (GW4+ DTP) from the Natural Environment Research Council (NERC) [NE/L002434/]. I would also like to thank: My supervisors Prof Steve Ormerod and Prof Charles Tyler for the guidance and support, but also for allowing me to develop my own ideas and entertaining ‘side-projects’. Prof Christy Morrissey for providing data on contaminants in dippers across South Wales. The Environment Agency and Natural Resources Wales for facilitating aspects of the research and providing data from routine monitoring. Specific thanks go to Katie Whitlock and Pete Gough at the EA and NRW, respectively. The members of the Pollution Science Area at the Centre for Ecology and Hydrology in Lancaster. A specific thanks goes to Alex Hunter, Heather Carter and Glόria Pereira for their help and support with chemical analyses. The many helpers I have had the privilege of working with along the way, including: Rosie, Jâms, Owen, Joe, Alienor, Katie, Talek, Dan, Caitlin, Hugh and Claudia. A special thanKs to past and present members of the 6th floor office, including: Willow, Jâms, Rhidian, Jade, Sarah, Mike, Hisham and Emma. II Table of Contents Chapter 1: General Introduction .................................................................. 1 1.1. Background ......................................................................................... 2 1.2. Aims and research questions ............................................................ 4 1.3. Study region (South Wales, United Kingdom) ................................. 4 1.4. Chapter structure ................................................................................ 6 Chapter 2: A review of xenobiotic pollution and endocrine disruption in aquatic ecosystems ...................................................................................... 9 2.1. Abstract ............................................................................................. 10 2.2. Introduction ....................................................................................... 11 2.3. The benefits of up-scaling xenobiotic pollutant research ............ 11 2.4. Advances in broad-scale xenobiotic pollutant research .............. 14 2.4.1. Biotic interactions and trophic transfer of xenobiotic pollutants .... 14 2.4.2. Adaptation to xenobiotic pollutant exposure ................................. 19 2.4.3. Long-term, life-cycle and transgenerational effects ...................... 20 2.4.4. Interactive mixtures of xenobiotic pollutants ................................. 23 2.4.5. Xenobiotic pollutants within the context of multiple stressors ....... 25 2.4.6. Effects of genetics on responses to xenobiotic pollution .............. 26 2.4.7. Trophic cascades and indirect effects of xenobiotic pollutants ..... 27 2.5. Limitations of xenobiotic pollutant impact assessments ............. 28 2.6. Integrated research for studies on xenobiotic pollutants ............ 29 2.7. Future directions .............................................................................. 31 2.7.1. Spatial variation in xenobiotic pollution across aquatic systems .. 31 2.7.2. Xenobiotic pollutant transfers across food webs .......................... 31 2.7.3. Biomarkers for quantifying xenobiotic pollutant effects ................ 32 2.7.4. Applying genetics and modelling to broad-scale analysis ............ 33 2.8. Conclusions ...................................................................................... 34 Chapter 3: A global assessment of the ecological risks from xenobiotic pollutant bioaccumulation in freshwater ecosystems ............................ 35 3.1. Abstract ............................................................................................. 36 3.2. Introduction ....................................................................................... 37 3.3. Material and methods ....................................................................... 39 3.3.1. Selection of high-risk xenobiotic pollutants ................................... 39 3.3.2. Bioaccumulation of selected ‘high-risk’ xenobiotic pollutants ....... 43 3.3.3. Quality scoring criteria .................................................................. 44 3.3.4. Ecological risk evaluation ............................................................. 44 3.3.5. Independent predictor variables ................................................... 45 3.3.6. Data preparation, grouping and analysis ...................................... 45 3.4. Results ............................................................................................... 47 3.4.1. Spatial distribution of available chemical data .............................. 47 3.4.2. Xenobiotic pollutant concentrations in freshwater systems .......... 48 3.4.3. Ecological risk from xenobiotic pollution ....................................... 50 3.5. Discussion ......................................................................................... 53 3.6. Conclusions ...................................................................................... 57 III Chapter 4: Biomonitoring and spatial variation of persistent organic pollutants across river ecosystems in South Wales ............................... 59 4.1. Abstract ............................................................................................. 60 4.2. Introduction ....................................................................................... 61 4.3. Material and Methods ....................................................................... 63 4.3.1. Sample sites and source identification ......................................... 63 4.3.2. Sample collection ........................................................................
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