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The movement of plastics through marine ecosystems and the influences on bioavailability and uptake into marine biota. Submitted by Adam Porter, to the University of Exeter as a thesis for the degree of Doctor of Philosophy in Biological Science in November 2018. This thesis/dissertation* is available for Library use on the understanding that it is copyright material and that no quotation from the thesis may be published without proper acknowledgement. I certify that all material in this thesis/dissertation* which is not my own work has been identified and that any material that has previously been submitted and approved for the award of a degree by this or any other University has been acknowledged. Signature:________________ ABSTRACT Microplastics are a diverse array of contaminants comprising a suite of sizes, shapes, and polymer types. Here I present a body of work investigating the distribution and movement of microplastics through the marine ecosystems via transportation and transformation pathways. First, I look at litter items of beaches of the Cornish coast, demonstrating that 41% of litter was plastics fragments unattributable to source and that this litter was continually re-stocked such that it was always present despite cleaning efforts. Then I took to the seas to conduct sea surface trawls in the North East Atlantic to investigate the floating proportion of marine plastic debris. Microplastics were found in every sample, yet were highly variable in concentration over geographic space ranging from 0.038 to 0.45 particles m-3. Counter to the prevailing trends, plastic fragments (84 μm – 21.8 mm) were the dominant shape (63%), with fewer fibres present. The likelihood of encounter and therefore risk of plastic to plankton was calculated and it was found that for every 1 plastic particle, there were between 500 and 1000 plankton, suggesting very low risk of biological uptake for this region. Plastics are not just found on the sea surface and are increasingly found in benthic sediments and biota. I tested whether marine snows would act as a transport mechanism of plastics from the surface to the seafloor. I demonstrate that under experimental conditions a range of plastic particle sizes, shapes, and polymer types, all readily incorporated into marine snows. This incorporation into marine snows both overcame the buoyancy of floating particles but also increased the sinking rate of dense particles. Buoyant polyethylene went from floating as a free particle to sinking at 818 m day–1. This repackaging of plastics also increased uptake of polystyrene in the blue mussel by 300 times compared to its uptake as a free sinking particle. I then investigated another route of plastic transformation in the potential for sea urchins to act as bioeroders of plastic. Urchins generated on average 172.9 ± 62.38 plastic pieces per urchin over 10 days; creating microplastics (98.56 μm to 15.8 mm) from a macroplastic tray even when their natural food was present. Despite these generated microplastics being of a buoyant polymer type, 87% of the depurated plastics were retained at the bottom of the tanks. This demonstrates biological fragmentation and the repackaging of plastic within a benthic ecosystem setting. Overall, my work highlights potential co-occurrence zones where plastic and plankton encounters are most likely; provides a mechanism for the transport of microplastics from the surface to the seafloor; and demonstrates two distinct mechanisms by which biological transformations of plastic can affect the behaviour of particles and their bioavailability to marine species. This all adds to our understanding of the risk that microplastics pose to marine environment. Page | ii TABLE OF CONTENTS Title Page………………………………………………………………….i Abstract…………………………………………………………………....ii Table of Contents………………………………………………………..iii List of Figures…………………………………………………….……...vi Acknowledgements………………………………………………..........ix 1CHAPTER I: GENERAL INTRODUCTION……………………….1 1.1 Plastics: An Overview………………………………………..2 1.2 Biological Impacts………………………………...………...11 1.3 Societal Impacts…………………………………………….16 1.4 Historical Field Development………………………………19 1.5 Knowledge Gaps…..………………………………….........20 2.1 CHAPTER II: RESEARCH PAPER 1………………………….28 Andrew J.R. Watts, Adam Porter, Neil Hembrow, Jolyon Sharpe, Tamara S. Galloway, and Ceri Lewis (2017). Through the sands of time: Beach litter trends from nine cleaned north Cornish beaches. Environmental Pollution, 228: 416– 424. DOI: 10.1016/j.envpol.2017.05.016 2.1.1 Introduction 2.1.2 Materials and Methods 2.1.3 Results 2.1.4 Discussion 2.1.5 Acknowledgements 2.1.6 References Page | iii 2.2 CHAPTER II: SUPORTING INFORMATION……………….....38 3.1 CHAPTER III: RESEARCH PAPER 2……………………......41 Adam Porter, Stephanie L. Wright, Brett P. Lyons, Tamara S. Galloway, and Ceri Lewis. Co-occurrence of plastic and zooplankton and the potential for microplastic encounter across ocean seascapes. Manuscript in preparation. 3.1.1 Abstract…………………………………………………….42 3.1.2 Introduction…………………………………………..........43 3.1.3 Methods……………………………………………………52 3.1.4 Results……………………………………………………..57 3.1.5 Discussion…………………………………………………75 4.1 CHAPTER IV: RESEARCH PAPER 3……………………….86 Adam Porter, Brett P. Lyons, Tamara S. Galloway and Ceri Lewis (2018). Role of Marine Snows in Microplastic Fate and Bioavailability. Environmental Science and Technology, 52(12): 7111–7119. DOI: 10.1021/acs.est.8b01000 4.1.1 Abstract 4.1.2 Introduction 4.1.3 Materials and Methods 4.1.4 Results and Discussion 4.1.5 Acknowledgements 4.1.6 References Page | iv 4.2 CHAPTER IV: SUPPORTING INFORMATION……………..95 5.1 CHAPTER V: RESEARCH PAPER 4………………………….105 Adam Porter, Kathryn E. Smith, Brett P. Lyons, Tamara S. Galloway and Ceri Lewis. Sea urchins as bioeroders of plastics. Manuscript in preparation. 5.1.1 Abstract……………………...…………………………...106 5.1.2 Introduction……………………………………………....107 5.1.3 Methods…………………………………………………..112 5.1.4 Results and Discussion…………………………………125 5.2 CHAPTER V: SUPPORTING INFORMATION………………..134 6 CHAPTER IV: GENERAL DISCUSSION……………………......137 7 Bibliography……………………………...………………….…...149 Page | v LIST OF FIGURES CHAPTER I Figure 1: Azorean water sample containing plastic and plankton Figure 2: North Atlantic modelled plankton and plastic abundances. Figure 3: A graphical description of my PhD. CHAPTER II Figure 1: Beached plastic litter on a North Cornish beach Figure 2: Map of North Cornish beach clean sites. Figure 3: Inter-annual trends of beach litter abundance between 2006 and 2011. Figure 4: Inter-annual trends of beach litter type between 2006 and 2011. Figure 5: Seasonal trends of beach litter abundance between 2006 and 2011. Figure 6: Seasonal trends of beach litter type between 2006 and 2011 CHAPTER III Figure 1: Sea Dragon sailing across the North Atlantic Figure 2: Abundances of plastic particles and plankton across the 2014 cruise track. Page | vi Figure 3: Abundances of plastic particles and plankton across the 2015 cruise track. Figure 4: Encounter rates across the 2014 cruise track. Figure 5: Encounter rates (number of plastic particles per zooplankton) across the 2015 cruise track. Figure 6: Particle shapes across the 2014 cruise track. Figure 7: Particle shapes across the 2015 cruise track. Figure 8: The size distribution of all plastic particles collected during the 2014 sampling cruise. Figure 9: Average maximum caliper sizes of fragments and fibres collected during the 2015 sampling cruise. Figure 10: Proportions of the particle polymers found across the 2014 cruise track. Figure 11: Proportions of the particle polymers found across the 2015 cruise track. Figure 12: The relative densities of the polymers identified and abundances across the 2014 cruise track. Figure 13: The relative densities of the polymers identified and abundances across the 2015 cruise track. Figure 14: The species found during the 2015 sampling cruise. CHAPTER IV Figure 1: A mussel ventilating at the bottom of our Vertical Transport Chambers Page | vii Figure 2: Images of marine snows with each of the six polymers incorporated and their sinking rates as free particles and once incorporated into marine snows. Figure 3: Uptake of microplastics into Mytilus edulis as free microplastics, in the simultaneous presence of marine snows, and once incorporated into marine snows. Figure 4: Microplastic polymers identified in subtidal environmental samples from 1−2700 m. CHAPTER V Figure 1: Sea urchin feeding on kelp and plastic Figure 2: Average plastic fragments created per tank by the sea urchin Paracentrotus lividus when exposed to clean polyethylene plastic trays. Figure 3: Amount of plastic fragments produced under the three treatment conditions. Figure 4: A selection of fragments made from the plastic mushroom trays by sea urchins. Figure 5: Sizes of plastic fragmented generated by the sea urchins under the different treatments over 9 days. Figure 6: Partitioning of plastic fragments by the sea urchin Paracentrotus lividus. CHAPTER VI Figure 1: A multidisciplinary team of scientists looking to tackle the problem of microplastic pollution Page | viii ACKNOWLEDGEMENTS Undertaking to do a PhD has been such a rewarding process; both for the work I have done of which I am proud, but also because of the people I have met along the way. As Isaac Newton put it: “If I have seen further it is by standing on the shoulders of Giants”. A PhD is a truly collaborative effort and I want to thank all those involved in my work, but also those that I have met along the way. First and foremost I have to thank my supervisor Ceri Lewis who took a chance on a marine geographer with a penchant for sending hundreds of emails. Thank you for entrusting me with this PhD. It has been a privilege and a pleasure to work alongside and be supervised by you and the way you have run our lab group with openness, friendship and passion greatly appreciated. You have created the environment in which I was allowed to thrive, so thank you. To Tamara, my second supervisor: thank you for always being there with a kind word, a stellar thought to put me back on track, and for all your help in turning my work into something to be proud of.