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Insecticide Contamination of Streams in a Warming Climate

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Insecticide Contamination of Streams in a Warming Climate Insecticide contamination of streams in a warming climate Samuel James Macaulay A thesis submitted for the degree of Doctor of Philosophy at the University of Otago, Dunedin, New Zealand. June 2019 Abstract Feeding a growing global population in the context of a changing climate will bring challenges for food producers and environmental managers seeking to mitigate the impact of intensifying agricultural practices. The control of insect pest populations through insecticide application is an important practice for improving crop yields, yet contamination of the environment with insecticides combined with impacts from climate change are together subjecting ecosystems to novel stressors and stressor combinations. Contamination of surface waters with neonicotinoids, the most widely used insecticides in the world, has become a chronic global problem. Despite a growing body of research investigating the impacts of neonicotinoids in aquatic ecosystems, prior to my research there were no published toxicity data for their effects on aquatic insects in New Zealand. Moreover, international data on chronic, neonicotinoid-mixture, interactive multiple-stressor and community-level effects in stream ecosystems were also lacking. My overall PhD research objective was to investigate the ecological impacts of neonicotinoid insecticides on New Zealand’s freshwater macroinvertebrate communities in a multiple-stressor and climate- change context. I developed and optimized laboratory procedures for testing chronic toxicities of neonicotinoids and observing their lethal and sublethal effects on stream insect larvae in controlled laboratory experiments. Through a series of 4-week experiments, the chronic toxicities of three commonly used neonicotinoids (imidacloprid, clothianidin and thiamethoxam) to nymphs of the ubiquitous New Zealand mayfly Deleatidium spp. were determined (Chapter 2) and possible interactions between the three insecticides were investigated (Chapter 3). In a subsequent 6-week multiple-stressor laboratory experiment, also with Deleatidium nymphs, I focused on possible interactions of low-level imidacloprid exposure with simulated heatwaves and a period of food limitation (Chapter 4). I then conducted a stream-side mesocosm experiment in 128 flow-through stream channels to investigate the individual and combined effects of realistic, pulsed exposures of imidacloprid and raised water temperature on stream macroinvertebrate communities characteristic of fast-flowing and slow-flowing microhabitats (Chapter 5). This experiment is the first empirical evaluation of stream macroinvertebrate community dynamics in response to the world’s most widely used agricultural insecticide, increased water temperature and reduced flow velocity (simulating streams subject to reduced flows due to water abstraction and i climate change). Six hundred and forty invertebrate drift and insect emergence samples each were collected throughout the experiment (on five occasions during and after the insecticide pulses), and 128 benthic invertebrate samples were collected after 24 days of heating and insecticide manipulations. In combination, the long-term laboratory experiments using larvae of a sensitive aquatic insect taxon and the field experiment in stream mesocosms allowed assessing neonicotinoid effects on stream macroinvertebrates at the individual, population and community level in a multiple-stressor and climate-change context. The 28-day concentration-response experiments (Chapter 2) and the neonicotinoid mixture experiment (Chapter 3) revealed imidacloprid as the most toxic of the three neonicotinoids to Deleatidium nymphs and also showed its potential for synergistic interactions with the other, comparably less toxic neonicotinoids clothianidin and thiamethoxam. Imidacloprid was therefore chosen for the subsequent multiple-stressor experiments (Chapters 4 and 5). Both of these demonstrated the strong effects of raised water temperatures on stream invertebrates and especially on Deleatidium larvae. In the 42-day laboratory experiment, sublethal and lethal effects of exposure to 0.4 µg/L imidacloprid took 24−36 days to manifest and were clearest in the absence of heatwaves and starvation because these stressors alone already strongly reduced Deleatidium survival. In the mesocosm experiment, all three manipulated factors strongly affected invertebrate drift community composition, with the first pulse of imidacloprid and increased temperature having a greater impact on communities in fast-flowing channels. Heating and imidacloprid exposure both generally resulted in increased emigration by drift. Increased temperature was the most pervasive stressor for the benthic invertebrate community, negatively affecting 80% of response variables. This was in part due to a natural 10-day heatwave which occurred during the manipulative period, raising temperatures in ambient mesocosms to 29.8°C and in heated channels to 32.9°C. Water temperature in the river reached 31.2°C during a second heatwave seven weeks after the end of the experiment. The snail Potamopyrgus antipodarum showed the only positive response to raised water temperatures, also responded positively to slow flow and was unaffected by imidacloprid highlighting the general tolerance of this invasive species to stressors. Monitoring drift and emergence patterns periodically throughout the experiment also provided insights into how invertebrate community composition changed in response to the natural heatwave. Taken together, the findings of my thesis demonstrate the importance of efforts to mitigate climate change and reduce contamination of surface waters with imidacloprid in order to protect our vulnerable freshwater ecosystems. ii I dedicate this work to my parents: the ones I’ve had from the very beginning, and the ones I’ve gained along the way. iii Acknowledgements I was told before I started this project that finding a good supervisor is more important than finding a good research topic. I was lucky enough to choose both an outstanding primary supervisor and a stimulating area of research. My heartfelt thanks to Christoph Matthaei for his guidance and support over these years of work. Thank you for always having an open door, for providing such helpful feedback and for showing interest in me as a person as much as wanting to see me develop as a researcher. This journey has been made all the more enjoyable and fulfilling under your guidance and direction. Many thanks too to Jay Piggott and Kimberly Hageman for their co-supervision of this project. I could not have solved many issues along the way without your help. Thank you both for bringing your esteemed and valued perspectives to this work. I am extremely grateful to the many hands that assisted me both in the field and in the lab; Peranjali Latchoumy, Ludovic Vincent, Johanna Khan, Teresa Be, Jessica and Nils Styger, Quentin Amalric, Pavel Mikheev, Ewan Bakker, Charlotte Patterson, Noel Juvigny- Khenafou, Nat Lim, Nicola McHugh, Stu Borland, and to Rob Alumbaugh and Sean Lyons in the lab at Utah: this would not have been possible without your important contributions. A special thanks to Jeremy Xu for working through all those samples of bugs that you were able to count. I doubt I’ll meet someone who can id. inverts as efficiently as you can! Thanks to Clyde and Jan Douglas for access to and use of their property at the Kauru. I will always have fond memories of my campsite by the river, especially Jan’s free-range eggs! My research was supported by a University of Otago Doctoral Scholarship and a research budget from the Department of Zoology. And to my family and friends⎯ my closest supporters! I am so grateful for having good friends who’ve been an invaluable source of support, laughter and encouragement during this journey. Mum and Dad, thank you for instilling in me an interest in the outdoors from my earliest days. For carrying me across streams and rivers before I was big enough to wade through them myself or old enough to know what an incredible world existed beneath their surface. Thank you for fostering my passion for ecology, for your continued interest in my work and for your unwavering and unending support and encouragement to see the task through. iv Jonathan and Mary, thank you both for your keen interest in my research and for sparking new passion when my own has waned. I will always think it funny how I came to research streams and climate change and gain you two as parents at the same time. Lastly, to my wonderful Grace, I really am so lucky to have had you by my side every step of the way. I couldn’t have done this without you. You mean the world to me, thank you. v Table of Contents Abstract ................................................................................................................................. i Acknowledgements ............................................................................................................. iv 1 General Introduction ................................................................................................... 2 1.1 Global food security, agriculture and climate change ............................................ 2 1.2 Impacts of agriculture and climate change in freshwater ecosystems .................... 5 1.3 Neonicotinoid Insecticides ...................................................................................... 9 1.4 Thesis aim and outline .......................................................................................... 12 2 Chronic toxicities
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