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The Bioaccumulation of Cyanotoxins in Aquatic Food Webs

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The Bioaccumulation of Cyanotoxins in Aquatic Food Webs University of New Hampshire University of New Hampshire Scholars' Repository Doctoral Dissertations Student Scholarship Summer 2019 THE BIOACCUMULATION OF CYANOTOXINS IN AQUATIC FOOD WEBS Amanda Lee Murby McQuaid University of New Hampshire, Durham Follow this and additional works at: https://scholars.unh.edu/dissertation Recommended Citation Murby McQuaid, Amanda Lee, "THE BIOACCUMULATION OF CYANOTOXINS IN AQUATIC FOOD WEBS" (2019). Doctoral Dissertations. 2481. https://scholars.unh.edu/dissertation/2481 This Dissertation is brought to you for free and open access by the Student Scholarship at University of New Hampshire Scholars' Repository. It has been accepted for inclusion in Doctoral Dissertations by an authorized administrator of University of New Hampshire Scholars' Repository. For more information, please contact [email protected]. THE BIOACCUMULATION OF CYANOTOXINS IN AQUATIC FOOD WEBS BY AMANDA MURBY MCQUAID BS Marine and Freshwater Biology, UNH, 2006 MS Zoology, UNH, 2009 DISSERTATION Submitted to the University of New Hampshire in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in Zoology in the Department of Biological Sciences September, 2019 This dissertation has been examined and approved in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Zoology in the Department of Biological Sciences by: Dissertation Director, Dr. James Haney, Professor of Zoology in the Department of Biological Sciences Dr. Alan Baker, Associate Professor Emeritus of Plant Biology in the Department of Biological Sciences Dr. Larry Harris, Professor of Zoology in the Department of Biological Sciences Dr. Leland Jahnke, Professor Emeritus of Plant Biology in the Department of Biological Sciences Dr. Marianne Moore, Frost Professor Emerita in Environmental Science & Professor Emerita of Biological Sciences, Wellesley College On July 8, 2019 (Date of Defense) Original approval signatures are on file with the University of New Hampshire Graduate School. ii I dedicate this dissertation to my husband John, daughters Oryah and Skylar, and dog Ava. Thank you for your love, support, and encouragement. iii Acknowledgements There are many people to thank and acknowledge for the completion and support of this research. I will be forever grateful for my advisor, Dr. James Haney, who has always believed in me. Thank you for being you; an energetic and positive role model in my life, who has led me through an interesting and rewarding path in limnological research. Your knowledge and optimism are always inspiring. I must also thank my doctoral committee (Dr. Alan Baker, Dr. Lee Jahnke, Dr. Larry Harris and Dr. Marianne Moore) and those who contributed on my guidance committee (Dr. C. Callieri, Dr. C. Burns and Jeff Schloss) for their continued support. I appreciate the combined knowledge of these incredible researchers, who provided invaluable feedback during the course and evolution of this research. Many thanks to the University of New Hampshire. The students, faculty and staff who have helped me along the way were kind and reassuring. There are too many people to individually list, but I hope you know how much you each helped me through this process. The UNH graduate school and support provided through research and teaching assistantships were also vital in the completion of my degree(s). This research was funded, in part, by the USDA Agricultural Experiment Station (HATCH grants). Finally, I would like to thank my family and friends who have encouraged me along the way. My parents John and Robin, and my sister Jessica, have always been loving and supportive. Additionally, I am so grateful for the family I have grown since the start of my research. John, Oryah, Skylar, and Ava; you are my world and I am the luckiest woman. I love you all so much. iv TABLE OF CONTENTS DEDICATION …………………………………………………………………………………. iii ACKNOWLEDGEMENTS …………………………………………………………………… iv LIST OF TABLES ……………………………………………………………………………..vii LIST OF FIGURES …………………………………………………………………………….x ABSTRACT ……………………………………………………………………………………xv CHAPTER ……………………………………………………………………………..…. PAGE I. Chapter 1: Seasonal Succession of Cyanobacteria and the Bioaccumulation of Cyanotoxins in Lake Zooplankton ………………………………………………………... 1 Abstract ……………………………………………………………………………….. 1 INTRODUCTION …………………………………………………………………….. 2 MATERIALS AND METHODS ……………………………………………………. 21 RESULTS …………………………………………………………………………… 28 DISCUSSION ………………………………………………………………………. 69 LIST OF REFERENCES …………………………………………………………..100 II. Chapter 2: Seasonal Abundance and Microcystin-Toxicity of Picocyanobacteria in Lakes of Contrasting Trophic Conditions ………...…………………………………………….111 Abstract ……………………………………………………………………………...111 INTRODUCTION ………………………………………………………………….. 112 MATERIALS AND METHODS ……………………………………………………116 RESULTS …………………………………………………………………………...120 DISCUSSION ……………………………………………………………………….135 LIST OF REFERENCES …………………………………………………………..155 v III. Chapter 3: Tracking Lake Food Web Interactions and the Pathway of Cyanotoxins to Zooplankton using Stable Isotope Analyses of 13C and 15N ………………………...163 Abstract ……………………………………………………………………………...163 INTRODUCTION …………………………………………………………………...164 MATERIALS AND METHODS ……………………………………………………169 RESULTS …………………………………………………………………………...176 DISCUSSION ……………………………………………………………………….211 LIST OF REFERENCES …………………………………………………………..249 vi LIST OF TABLES CHAPTER 1 TABLES ……………………………………………………………………………15 Table 1: Common cyanobacteria and cyanotoxins of New Hampshire………………...15 Table 2: Cyanotoxins and common modes of action (modified from Handbook of Cyanobacteria Monitoring and Cyanotoxin Analysis, First Ed. 2017)…………………..16 Table 3: Common cyanobacteria and toxins by detection method, modified from Pearl and Otten 2013……………………………………………………………………………….17 Table 4. From Codd et al. 2005; on the approximate LD 50 levels for toxic cyanobacteria via i.p. injection in mice…………………………………………………….18 Table 5. Seasonal water quality characteristics (Secchi Disk Depth (SDD), Chlorophyll (CHL), Color-Dissolved Organic Matter (CDOM)) of oligotrophic, Christine Lake and meso-eutrophic, Willand Pond (located in New Hampshire, USA) during 2012………31 Table 6. Seasonal water quality characteristics (Total Nitrogen (TN), Total Phosphorus (TP), TN:TP ratios (mass and molar), Nitrates/Nitrites (NN)) of oligotrophic, Christine Lake and meso-eutrophic, Willand Pond (located in New Hampshire, USA) during 2012……………………………………………………………………………………………31 Table 7. Seasonal conditions of lake chemistry throughout the water column of Christine Lake in 2012 (as measured from YSI sonde 6600 multi-parameter probes)…………..32 Table 8. Seasonal conditions of lake chemistry throughout the water column of Willand Pond in 2012 (as measured from YSI sonde 6600 multi-parameter probes)………….33 Table 9. The relative composition and density of major phytoplankton phyla, with emphasis on net cyanobacteria (bold) in Christine Lake………………………………...38 Table 10. The relative composition and density of major phytoplankton phyla, with emphasis on net cyanobacteria (bold) in Willand Pond………………………………….38 Table 11. The relative composition and density of major zooplankton taxa in Christine Lake by season……………………………………………………………………………….44 Table 12. The relative composition and density of major zooplankton taxa in Willand Pond by season………………………………………………………………………………44 vii Table 13. Weight-specific microcystins (ng MCs g-1 dwt) from plankton compartments; net zooplankton, net phytoplankton, nanoplankton, and picoplankton. Comparison of ratios of MCs in zooplankton (consumer) to phytoplankton fractions (diet) in Christine Lake……………………………………………………………………………………………52 Table 14. Weight-specific microcystins (MCs) from plankton compartments (ng MC g-1 dwt); net zooplankton, net phytoplankton, nanoplankton, and picoplankton. Comparison of ratios of MCs in zooplankton (consumer) to phytoplankton fractions (diet) in Willand Pond…………………………………………………………………………………………...53 Table 15. BMAA (ng g-1 dwt) detected from net phytoplankton and net zooplankton communities from Christine Lake. Replicates, averages, standard error (SE) and ratios (zooplankton to net phytoplankton) reported……………………………………………...54 Table 16. BMAA (ng g-1 dwt) detected from net phytoplankton and net zooplankton communities from Willand Pond. Replicates, averages, standard error (SE) and ratios (zooplankton to net phytoplankton) reported……………………………………………...55 CHAPTER 1 APPENDICE TABLES ………………………………………………………...96-99 Table A-1. The pair(s) of variables with positive correlation coefficients and P values below 0.050 tend to increase together. For the pairs with negative correlation coefficients and P values below 0.050, one variable tends to decrease while the other increases. For pairs with P values greater than 0.050, there is no significant relationship between the two variables (SigmaPlot 12.0)…………………………………………..96-98 Table A-2. Whole lake water (WLW) microcystins (MCs), < 50 m filtrate of lake water MCs, < GFA (2 m) MCs, and < GFF (0.2 m)…………………………………………...99 CHAPTER 2 TABLES ………………………………………………………………………….126 Table 1. Picocyanobacteria in Willand Pond and Christine Lake in 2012…………...126 Table 2. Percent abundance of picocyanobacteria (PCY) to total autotrophic picoplankton (APP) enumerated by season. Under epifluorescence with excitation at 435 nm wavelength, picoeukaryotes reflect red and PCY reflect orange and yellow. Under epifluorescence with excitation at 572 nm wavelength, PCY reflect red……..127 Table 3. Seasonal concentrations of net cyanobacteria
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