The Spatial and Temporal Distribution and Environmental Drivers Of
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THE SPATIAL AND TEMPORAL DISTRIBUTION AND POTENTIAL ENVIRONMENTAL DRIVERS OF SAXITOXIN IN NORTHWEST OHIO Callie A. Nauman A Thesis Submitted to the Graduate College of Bowling Green State University in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE May 2020 Committee: Timothy Davis, Advisor George Bullerjahn Justin Chaffin © 2020 Callie A. Nauman All Rights Reserved iii ABSTRACT Timothy Davis, Advisor Cyanobacterial harmful algal blooms threaten freshwater quality and human health around the world. One specific threat is the ability of some cyanobacteria to produce multiple types of toxins, including a range of neurotoxins called saxitoxins. While it is not completely understood, the general consensus is environmental factors like phosphorus, nitrogen, and light availability, may be driving forces in saxitoxin production. Recent surveys have determined saxitoxin and potential saxitoxin producing cyanobacterial species in both lakes and rivers across the United States and Ohio. Research evaluating benthic cyanobacterial blooms determined benthic cyanobacteria as a source for saxitoxin production in systems, specifically rivers. Currently, little is known about when, where, why, or who is producing saxitoxin in Ohio, and even less is known about the role benthic cyanobacterial blooms play in Ohio waterways. With increased detections of saxitoxin, the saxitoxin biosynthesis gene sxtA, and saxitoxin producing species in both the Western Basin of Lake Erie and the lake’s major tributary the Maumee River, seasonal sampling was conducted to monitor saxitoxin in both systems. The sampling took place from late spring to early autumn of 2018 and 2019. Monitoring including bi-/weekly water column sampling in the Maumee River and Lake Erie and Nutrient Diffusing Substrate (NDS) Experiments, were completed to evaluate saxitoxin, sxtA, potential environmental drivers, and benthic production. Overall, saxitoxin and sxtA was found throughout the entirety of the Ohio’s portion of the Maumee River and east of the Lake Erie Islands during both years. Detections included sxtA peaks in July and saxitoxin detections as early as May and as late as October for planktonic samples. However, benthic experiments suggested higher saxitoxin production in iv September and October. In general, low correlations were found between qPCR detections, nutrients, and toxin detections, however; ELISA and qPCR results in the river possibly suggests that benthic cyanobacteria are a potential source for saxitoxin in the Maumee River. Planktonic trends suggest nitrogen and dissolved reactive phosphorus may influence saxitoxin production, while benthic results highly correlated low light availability with saxitoxin production. v To my family and friends for their love and support throughout my academic career and life. I could not have done this without you. vi ACKNOWLEDGMENTS Thank you to Dr. Timothy Davis, Dr. George Bullerjahn, and Dr. Justin Chaffin for the support through my graduate career and my thesis project. I greatly appreciate all the expertise, opportunities, and overall passion for the Great Lakes. Dr. Doug Kane, Keara Stanislawczyk, Halli Bair, Audrey Laiveling, and Crista Keiley for the field sampling and proccessing, this project could not have happened without you. Heather Raymond for the advice and help with field sampling difficulties. The Ohio Department Of Higher Education for funding support. The BGSU Lab: Michelle Neudeck, Kaitlyn McKindles, Laura Reitz, Emily Beers, Matthew Kennedy, Seth Buchholz, Daniel Peck, Jay DeMarco, Dr. Paul Matson, Melanie Edwards, Jacob Yager, and Valerie Montgomery. Thank for all the help, insight, motivation, and laughs. vii TABLE OF CONTENTS Page CHAPTER 1: INTRODUCTION ............................................................................................. 1 1.1: Algal Blooms and Eutrophication.......................................................................... 1 1.2: Cyanobacteria Harmful Algal Blooms .................................................................. 2 1.3: Cyanotoxin Background ........................................................................................ 3 1.4: qPCR and sxtA Monitoring .................................................................................... 5 1.5: Benthic Cyanobacterial Blooms ............................................................................ 6 1.6: Cyanotoxin Monitoring in Ohio ............................................................................ 6 1.7: Chemical- and Molecular-based Saxitoxin Monitoring in Ohio ........................... 7 1.8: Cyanotoxin Production Drivers ............................................................................. 7 1.9: Project Objectives ................................................................................................. 8 CHAPTER 2: METHODS ........................................................................................................ 10 2.1: Field Sampling- Site Background ......................................................................... 10 2.2: Planktonic Field Sampling- Collection Methods ................................................... 11 2.3: Planktonic- Laboratory Processing and Analysis .................................................. 11 2.4: Nutrient Diffusing Substrate- Site Background ..................................................... 13 2.5: Nutrient Diffusing Substrate- Experimental Design .............................................. 14 2.6: Nutrient Diffusing Substrate- Field Sampling ....................................................... 16 2.7: Statistical Analysis ................................................................................................. 16 CHAPTER 3: RESULTS .......................................................................................................... 17 3.1: Nutrients- Planktonic ............................................................................................. 17 3.2: Fluorometric Parameters- Planktonic .................................................................... 18 viii 3.3: Molecular Parameters- Planktonic ......................................................................... 19 3.4: Nutrient Diffusing Substrate Experiments ............................................................. 22 CHAPTER 4: DISCUSSION .................................................................................................... 23 4.1: Planktonic Monitoring and Saxitoxin Detections .................................................. 23 4.2: Nutrient Diffusing Substrate Experiments ............................................................ 27 4.3: Conclusion ............................................................................................................. 29 4.4: Future Work .......................................................................................................... 30 LITERATURE CITED ............................................................................................................. 32 APPENDIX A. FIGURES ........................................................................................................ 47 APPENDIX B. TABLES .......................................................................................................... 66 1 CHAPTER 1: INTRODUCTION 1.1: Algal Blooms and Eutrophication Aquatic systems and their organisms play an important role in the interactions and dynamics of Earth’s physical, ecological, and economic structure (Steffensen, 2008; Dodds et al, 2009). At the lower trophic level, microscopic photosynthetic autotrophs, or phytoplankton, supply the world with half of its photosynthetic biomass (Houghton & Woodwell, 1989). Phytoplankton not only supply the world with oxygen, but play an active role in the planet’s carbon, nitrogen, and phosphorus cycles (Falkowski, 1994). While phytoplankton are a vital food source for the aquatic food web, certain types of phytoplankton can experience uncontrollable growth, also known as harmful algal blooms (Hallegraeff, 2004). While some algal blooms are naturally occurring and crucial to maintaining a healthy food web, overwhelming algal concentrations and species shifts have led to destructive blooms creating with hypoxic zones and high toxin production, thus damaging the system and those who use it (Anderson et al., 2002). For example, both the Baltic Sea and the Benguela Current off the southern coast of Africa are both seeing temporal and community shifts of their natural diatom dominated blooms to dinoflagellate-dominated blooms, impacting their fisheries and altering the nutrient cycling of the system (van der Lingen et al., 2016; Spilling et al., 2018). Some of the dominating factors in the formation of freshwater algal blooms include availability of nitrogen and phosphorus (Carpenter et al., 2001; Schindler et al. 2008; Gobler et al. 2016). High enrichment of nutrients and subsequent aquatic plant and algae growth is otherwise known as eutrophication and is thought to be increased with human activity (Smith et al., 2006). Eutrophic water supplies plants and phytoplankton with warm and nutrient rich water allowing for optimal growth (Schindler, 2006; Smith et al, 2006). At the turn of the century, an estimated 40% of 2 available freshwater in America, Europe, and Asia had the eutrophic conditions to support algal blooms (Chorus & Bartram, 1999). A 2007 National Lake Assessment data showed chlorophyll concentrations sustaining bloom conditions in 44%