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The Effects of Silver Nanoparticles on Lower Trophic Levels in Aquatic Ecosystems

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The Effects of Silver Nanoparticles on Lower Trophic Levels in Aquatic Ecosystems THE EFFECTS OF SILVER NANOPARTICLES ON LOWER TROPHIC LEVELS IN AQUATIC ECOSYSTEMS A Thesis Submitted to the Committee on Graduate Studies in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in the Faculty of Arts and Science TRENT UNIVERSITY Peterborough, Ontario, Canada © Copyright by Katarina Ana Cetinic 2019 Environmental and Life Sciences Ph.D. Graduate Program May 2019 ABSTRACT The effects of silver nanoparticles on lower trophic levels in aquatic ecosystems Katarina Ana Cetinic Due to their effective antibacterial and antifungal properties, silver nanoparticles (AgNPs) have quickly become the most commonly used nanomaterial, with applications in industry, medicine and consumer products. This increased use of AgNPs over the past decade will inevitably result in an elevated release of nanoparticles into the environment, highlighting the importance of assessing the environmental impacts of these nanomaterials on aquatic ecosystems. Although numerous laboratory studies have already reported on the negative effects of AgNPs to freshwater organisms, only a handful of studies have investigated the impacts of environmentally relevant levels of AgNPs on whole communities under natural conditions. This thesis examines the effects of chronic AgNP exposure on natural freshwater littoral microcrustacean, benthic macroinvertebrate and pelagic zooplankton communities. To assess the responses of these communities to AgNPs, I focused on a solely field-based approach, combining a six-week mesocosm study with a three-year whole lake experiment at the IISD – Experimental Lakes Area (Ontario, Canada). Our mesocosm study tested the effects of AgNP concentration (low, medium and high dose), surface coating (citrate- and polyvinylpyrrolidone [PVP]-coated AgNPs), and type of exposure (chronic and pulsed addition) on benthic macroinvertebrates in fine and stony sediments. Relative abundances of metal-tolerant Chironomidae in fine sediments were highest in high dose PVP-AgNP treatments; however, no negative effects of AgNP exposure were seen on biodiversity metrics or overall community structure throughout the study. I observed similar results within the ii whole lake study that incorporated a long-term addition of low levels of AgNPs to an experimental lake. Mixed-effects models and multivariate methods revealed a decline in all species of the littoral microcrustacean family Chydoridae in the final year of the study within our experimental lake, suggesting that this taxon may be sensitive to AgNP exposure; however, these effects were fairly subtle and were not reflected in the overall composition of littoral communities. No other negative effects of AgNPs were observed on the pelagic zooplankton or benthic macroinvertebrate communities. My results demonstrate that environmentally relevant levels of AgNPs have little impact on natural freshwater microcrustacean and benthic macroinvertebrate communities. Instead, biodiversity metrics and community structure are primarily influenced by seasonal dynamics and nutrient concentrations across both lakes. This thesis highlights the importance of incorporating environmental conditions and the natural variability of communities when examining the potential risks posed by the release of AgNPs into the environment, as simplistic laboratory bioassays may not provide an adequate assessment of the long-term impacts of AgNPs on freshwater systems. Keywords: Silver nanoparticles, zooplankton, benthic macroinvertebrates, littoral microcrustaceans, whole lake experiment, IISD – Experimental Lakes Area iii Acknowledgements I would like to express my sincere gratitude to my supervisor Dr. Maggie Xenopoulos for allowing me the incredible opportunity to conduct large-scale freshwater research, and providing me with endless patience, support and guidance along the way. I would also like to express special thanks to my committee members, Dr. Dave Beresford and Dr. Gary Burness, for their constant words of encouragement and support, and helpful comments and advice in committee meetings and in the writing stages of my thesis. Thank you also to Dr. Jim Schaefer and Dr. James Rusak for being wonderful members of my defence committee, and for providing me with insightful questions and a broader perspective from which to examine my research. I would like to extend a special thank you to all of the scientists and staff at the International Institute for Sustainable Development – Experimental Lakes Area for their assistance with the Lake Ecosystem Nanosilver (LENS) project. In particular, I would like to thank Dr. Mike Paterson for his continuous support and mentorship throughout the years. I would also like to acknowledge Dr. Beth Norman for her helpful suggestions and contribution towards the experimental design in the first years of this project. Many thanks to everyone who helped with sample collection and analysis throughout the years: Jennifer Vincent, Graham Blakelock, Jonathan Martin, Daniel Rearick, Andrea Conine, Andrew Scott and Paul Finigan. And lastly, to all those at the IISD – ELA that have made every field season so special and memorable. Some of my favourite moments ever were spent up there with you. A warm thank you to Dr. Tom Whillans and Dr. Stephen Hill, for not only being extraordinary professors to TA for, but for providing a constant source of inspiration and iv support. I would also like to thank my Master’s supervisor, Dr. Petar Kružić, for continuing to be a wonderful mentor, even after all these years. Thank you for everything you have taught me, and for helping me grow as a researcher. I extend my sincere gratitude to Linda Cardwell and Mary-Lynn Scriver. The encouragement, patience and support you have shown me over the years have helped me get through many difficult and challenging moments, and I am beyond grateful. Thank you to Holly Kuin and Heathyr Francis at the Centre for Academic Testing for being such amazing supervisors. Your enthusiasm and positive attitude have made working at the Centre a wonderful experience. I am so thankful to all my friends in Canada and Croatia for always being there for me, even when they were thousands of kilometers away. Thank you to Samantha Stephens, Allison Kwok, and Debbie Jenkins for their endless encouragement, especially in the moments leading up to my defence. Your passion, drive and strength are truly inspirational. I would also like to thank Adrian Borlestean for being an exceptional friend. Our road trips and engaging discussions on every topic imaginable are something I will never forget. You have taught me so much about life, have been there for me and supported me in countless ways over the years, and I feel so fortunate to have you in my life. I am especially grateful to my sister Marija and her husband Jeff for all their support and love. You have inspired me immensely, both academically and personally. Thank you for always being there, and for all the adventures and moments spent together. Having you in Canada while I pursued my degree has made all the difference. v Thank you to my beautiful nieces and nephews for their boundless curiosity and wonder. Your interest and presence have taught me so much about what truly matters in life. Lastly, I would like to thank my family in Croatia, especially my mother Biserka and my father Boris, for their endless love and encouragement over the years. You have been there for me, supported me and believed in me in every way imaginable, and I am endlessly grateful. I couldn’t have done it without you. vi TABLE OF CONTENTS PAGE TITLE PAGE ................................................................................... i ABSTRACT ................................................................................... ii KEYWORDS ................................................................................... iii ACKNOWLEDGEMENTS ................................................................................... iv TABLE OF CONTENTS ................................................................................... vii LIST OF TABLES ................................................................................... xi LIST OF FIGURES ................................................................................... xiii LIST OF ABBREVIATIONS ................................................................................... xviii Chapter 1: General Introduction .......................................................................... 1 1.1. Background ............................................................................................ 1 1.2. Objectives ............................................................................................... 4 1.3. Novelty and Importance ......................................................................... 6 1.4. References .............................................................................................. 8 Chapter 2: The effects of silver nanoparticles on natural benthic macroinvertebrate communities in littoral mesocosms 2.1 Preface ..................................................................................................... 15 2.2 Abstract ................................................................................................... 16 2.3 Introduction ............................................................................................. 17 2.4 Materials and Methods ............................................................................ 21 2.4.1 Study Area .................................................................................
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