Assessing the Effects of Chronic Neonicotinoid Insecticide Exposure
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ASSESSING THE EFFECTS OF CHRONIC NEONICOTINOID INSECTICIDE EXPOSURE ON AQUATIC INSECTS USING MULTIPLE EXPERIMENTAL APPROACHES A Thesis Submitted to the College of Graduate and Postdoctoral Studies In Partial Fulfillment of the Requirements For the Degree of Doctor of Philosophy In the School of Environment and Sustainability University of Saskatchewan, Saskatoon. By Michael Christopher Cavallaro © Copyright Michael C. Cavallaro, April, 2018. All rights reserved. PERMISSION TO USE In presenting this dissertation in partial fulfillment of the requirements for a Postgraduate degree from the University of Saskatchewan, I agree that the Libraries of the University may make it freely available for inspection. I further agree that permission for copying of this dissertation in any manner, in whole or in part, for scholarly purposes may be granted by the professor who supervised my dissertation work or, in their absence, by the Executive Director of the School of Environment and Sustainability, in which my dissertation work was done. It is understood that any copying or publication or use of this dissertation or parts thereof for financial gain shall not be allowed without my written permission. It is also understood that due recognition shall be given to me and to the University of Saskatchewan in any scholarly use which may be made of any material in my dissertation. Requests for permission to copy or make other use of material in this dissertation in whole or in part should be addressed to: Executive Director, School of Environment and Sustainability University of Saskatchewan Room 323, Kirk Hall 117 Science Place Saskatoon, Saskatchewan S7N 5C8 OR College of Graduate and Postdoctoral Studies University of Saskatchewan 107 Administration Place Saskatoon, Saskatchewan S7N 5C9 i ABSTRACT Neonicotinoid insecticides are among the most widely used plant protection products in industrialized agriculture, and are hypothesized to be contributing to losses in non-target insect biodiversity. The lack of toxicological data evaluating the effects of neonicotinoids restricts the ability of regulators to adequately protect sensitive insects particularly those with aquatic larval stages. Many Prairie wetlands are in regions of intensive agriculture and are directly at risk of neonicotinoid contamination and require special considerations to best protect these ecologically important areas. Under laboratory conditions, I compared the effects of imidacloprid, clothianidin, thiamethoxam on the model aquatic insect, Chironomus dilutus. Reduced emergence success, advanced emergence timing, and male-biased sex ratios were observed across all compounds tested. Imidacloprid and clothianidin reduced emergence success at similar concentrations whereas thiamethoxam required a concentration an order of magnitude greater to observe similar toxicity. Normalizing the clothianidin and thiamethoxam toxic responses to imidacloprid, I calculated acute (lethality) 14-day toxic equivalency factors (TEFs) for imidacloprid, clothianidin and thiamethoxam as 1.00, 1.05 and 0.14, respectively, and chronic (emergence inhibition) 40-day TEFs as 1.00, 1.62 and 0.11, respectively. To expand upon these single-species laboratory assessments, in situ limnocorrals were used to determine the chronic effects of the three neonicotinoids to emerging aquatic insect communities in a Prairie wetland. Imidacloprid and clothianidin treatments had similar community responses and non-biting midge (Diptera: Chironomidae) and damselfly (Odonata: Zygoptera) emerged significantly earlier than the controls (18 to 25 days earlier). An additional limnocorral study with clothianidin was inconclusive. While laboratory and limnocorral studies were useful to isolate neonicotinoid effects, multiple anthropogenic stressors were hypothesized to cumulatively influence insect emergence from natural Prairie wetlands surrounded by neonicotinoid-treated canola fields. Multivariate analysis showed neonicotinoid concentration, turbidity, vegetation disturbance and continuity of grasses were significant factors modifying the abundance and composition of emerging insects. Total insect abundance was negatively affected by neonicotinoids (β ± S.E.=- 0.61 ± 0.14, P<0.001) but positively affected by vegetation disturbance (β ± S.E.=0.34 ± 0.11, P<0.001). Collectively, these data suggest more rigorous water quality guidelines and agricultural management strategies are needed to protect aquatic insects and the higher trophic organisms that rely on this important food source. ii ACKNOWLEDGEMENTS First, I want to thank the unwavering support system that gave me the confidence to follow my passion, continue my education, and pursue my PhD. To my big-hearted parents, Caryn and Michael, and my incredible sisters, Cory and Casey, for their unyielding motivation and optimistic attitude through the highs and lows of all my endeavors. You guys are the best! I want to acknowledge the mentorship and direction provided by my co-supervisors, Drs. Christy Morrissey and Karsten Liber. Thank you for taking a chance on a kid from New Jersey. With your guidance this once entomologist, now ecotoxicologist (although I’m still not sold on this metamorphosis) sincerely appreciates the opportunity to work on such exciting and meaningful research. I am truly grateful for your patience, thoughtful insights, and constructive criticisms that have improved my abilities as a researcher. Thank you. I would like to thank the contributing members of my academic committee, Drs. Doug Chivers, Jean-Michel DeVink, Tim Jardine, Garth van der Kamp, and faculty members from the Toxicology Centre and School of Environment and Sustainability, Drs. Helen Baulch, Markus Hecker, David Janz, Vladimir Kricsfalusy, Toddi Steelman, and Graham Strickert, for their time, guidance, and advice throughout my PhD. I would like to send a special thank you to Drs. Bob Clark (Environment Canada), Tim Jardine (SENS), and Iain Phillips (Saskatchewan Water Security Agency) for being outstanding mentors and valued colleagues throughout my program—I truly appreciate it. The grueling marathon of graduate studies is rarely done alone. To all the SENS and Toxicology graduate students, past and present, thank you for your friendship. I feel incredibly lucky that I was surrounded by such kind, encouraging people during my time at the U of S. I was also fortunate to have an outstanding lab mate and role model, Dr. Anson Main, whose perseverance was a constant source of inspiration. Funding for this project was provided by: Natural Sciences and Engineering Research Council of Canada (NSERC), the Department of Fisheries and Oceans Canada (DFO), the University of Saskatchewan, and in-kind support from Environment Climate Change Canada (ECCC). iii DEDICATION I dedicate this dissertation to my first academic mentor and entomology professor, who opened my mind to the world of insects and taught me how to “think like a bug”, Dr. Chris Tipping. iv TABLE OF CONTENTS PERMISSION TO USE ................................................................................................................... i ABSTRACT .................................................................................................................................... ii ACKNOWLEDGEMENTS ........................................................................................................... iii DEDICATION ............................................................................................................................... iv TABLE OF CONTENTS ................................................................................................................ v LIST OF TABLES ......................................................................................................................... ix LIST OF FIGURES ....................................................................................................................... xi LIST OF ABBREVIATIONS ...................................................................................................... xiv CHAPTER 1: INTRODUCTION ................................................................................................... 1 1.1 RESEARCH PURPOSE ..................................................................................................... 1 1.2 RESEARCH OBJECTIVES ............................................................................................... 2 1.3 REVIEW OF LITERATURE ............................................................................................. 3 1.3.1 AGROECOSYSTEMS AND PRAIRIE WETLANDS ............................................. 3 1.3.2 IMPORTANCE OF AQUATIC INSECT EMERGENCE IN FRESHWATER ECOSYSTEMS .................................................................................................................. 4 1.3.3 PREVALENCE AND CONSEQUENCE OF PESTICIDES IN AQUATIC ECOSYSTEMS .................................................................................................................. 6 1.3.4 NEONICOTINOID INSECTICIDE USE, FATE, AND PERSISTENCE ................ 8 1.3.5 TOXICITY OF IMIDACLOPRID, CLOTHIANIDIN, AND THIAMETHOXAM TO NON-TARGET AQUATIC INSECTS ...................................................................... 10 1.3.6 UTILITY OF MESOCOSMS IN ECOTOXICOLOGY.......................................... 12 1.3.7 SYNTHESIS ............................................................................................................ 14 1.4 THESIS STRUCTURE ....................................................................................................