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ABSTRACT POPP, ANAKELA. Advancing the Tools of Freshwater Mussel Conservation: Determining the Relative Chemical Sensitivity of In Vivo and In Vitro Propagated Juvenile Mussels (Under the direction of William Cope). Freshwater mussels of the family Unionidae are ecologically important and globally imperiled, and research is urgently needed to guide their protection and conservation. Identifying and mitigating chemical stressors is an important part of the process, as is assessing mussel-specific sensitivity to pollutants to establish protective concentrations (e.g., establishing suitable habitat condition, effluent permit limits, state water quality standards, and water quality criteria). The newly transformed juvenile life stage has been shown to be sensitive to certain toxicants and is often used in toxicity testing. A ready supply of recently transformed juveniles are needed to conduct laboratory-based toxicity studies. Over the past several decades, host-fish (in vivo) propagation techniques have significantly advanced, as have long-term growth and maintenance of propagated mussels. Alternative media-based (in vitro) culture methods have made laboratory rearing of juveniles more efficient and cost- effective. However, ASTM International guidelines caution against using in vitro propagated juveniles in toxicity tests unless their relative chemical sensitivity to in vivo juveniles is described. The first objective of this study was to evaluate the relative sensitivity of juvenile mussels produced from both propagation methods to selected chemical toxicants. We conducted 96-hour acute toxicity tests according to the ASTM International guidelines with three species (Lampsilis cardium, L. abrupta, and Utterbackia imbecillis) and six chemicals: chloride, nickel, ammonia, copper (as copper sulfate), and aquatic herbicides Clearigate and Nautique. We calculated the median effective concentration (EC50) for each species- chemical combination and compared the EC50s of in vitro and in vivo juveniles. Statistically significant differences in EC50 between in vitro and in vivo propagated juveniles were observed in 8 of the 17 trials. In 7 of the 8 statistically different tests, in vitro juveniles were more sensitive than in vivo juveniles. There was also a significant effect of the interaction between propagation method and concentration on survival in 6 of the 17 tests. Among all species, EC50s varied between in vitro and in vivo juveniles by a factor of 1.6 for ammonia, 1.1 for chloride, 1.4 for Clearigate, 2.1 for copper, 1.2 for Nautique, and 1.0 for nickel. All of these statistical differences were within the variation for between-laboratory comparisons for a given chemical demonstrated in a recently published evaluation of results of mussel toxicity tests, and therefore, indicate that in vitro propagated juvenile mussels may be appropriate for use in ASTM-based toxicity testing. The second objective of this study was to examine the effect of age on relative chemical sensitivity for one toxicant (copper). Mussels from each of the three species previously mentioned were tested during the first, second, and third week post-transformation and the EC50s of in vitro and in vivo juveniles were compared for each age group. Of the 8 EC50 comparisons, 4 statistically significant differences between in vitro and in vivo juveniles were observed, and in all of these instances, in vitro juveniles were more sensitive than in vivo juveniles. However, these differences were evenly distributed across all ages, and further analysis revealed the lack of a significant relationship between age and relative chemical sensitivity, indicating in vitro juveniles may be appropriate for use in toxicity testing regardless of age. © Copyright 2017 by Anakela Popp All Rights Reserved Advancing the Tools of Freshwater Mussel Conservation: Determining the Relative Chemical Sensitivity of In Vitro and In Vivo Propagated Juvenile Mussels by Anakela Popp A thesis submitted to the Graduate Faculty of North Carolina State University in partial fulfillment of the requirements for the Degree of Master of Science Fisheries, Wildlife, and Conservation Biology Raleigh, North Carolina 2017 APPROVED BY: _______________________________ _______________________________ William Cope Thomas Augspurger Committee Chair _______________________________ _______________________________ Thomas Kwak Jay Levine ii DEDICATION To my parents and wonderful family: for loving me well, for supporting my endeavors (academic and otherwise), and for taking me camping so often that I was shocked when I found out people stayed in hotels for vacation. I love you. And to the wonderful mentors who have taught, inspired, and encouraged me: Sandy Stowe, who used her days off to impart scientific knowledge to middle school minds; Bill and Kelli Schuyler, whose passion for their students and the sciences still inspires me to keep studying this amazing world we live in; Robert Bringolf, Jay Shelton, Susan Wilde, and Andrea Fritts, for sharing their love and knowledge of aquatic resources; Brett Albanese, Jason Wisniewski, and Deb Weiler, for showing me the amazing diversity of my home state and for training me as a field biologist; and Greg Cope, for introducing me to the world of ecotoxicology and training me as a researcher. Thank you for investing in me. iii BIOGRAPHY Anakela Popp was born and raised in the suburbs of Atlanta, Georgia. Though their day-to-day lives were centered in suburbia, her family made a point to spend time outdoors. Family vacations were spent camping, hiking, canoeing, and fishing along various rivers, mountains, and beaches throughout the Southeast. Science and the outdoors have always been her passions, and Anakela was thrilled to discover that the two combined could become a career. She attended the University of Georgia, earning a Bachelor of Science in Forest Resources with dual concentrations in Wildlife and Aquatic Sciences. Upon graduation in 2013, she worked as a Nongame Aquatics Technician for the Georgia Department of Natural Resources before beginning her graduate career in 2014. iv ACKNOWLEDGEMENTS I would first like to thank my adviser, Dr. Greg Cope, and the rest of my committee, Drs. Tom Augspurger, Tom Kwak, and Jay Levine, for their guidance, support, insights, and advice throughout this process. Your mentorship as I begin my professional career has been invaluable. Thanks to my lab mates, Jennifer Archambault and Sean Buczek, for showing me the ropes and offering endless support along the way. Joseph McIver and Mary Silliman were my excellent technicians—thank you for your diligent work and patience, even when mussels kept dying. Thanks also to Emilee Wooster, Mike Walter, Spencer Gardner, and Dylan Owensby for additional laboratory assistance. Additional gratitude is for Casey Greishaber, Tiffany Penland, Megan Thoemmes, Mary Henson, and the rest of DCL 258 for support, encouragement, and laughter along the way. Special thanks to Dr. Monte McGregor and the rest of the group at the Kentucky Center for Mollusk Conservation for producing the mussels for these experiments and for providing insight at various stages through the project. Thanks to Dr. Mac Law for offering time and expertise on options for potential histological analysis. Masaki Miyazawa provided technical expertise and laboratory space for biomarker assays. My gratitude goes out to Chris Ingersoll and Ning Wang for chemical advice, and to West Bishop for additional chemical consultation and analysis of copper samples. Funding for this research was provided by the U.S. Geological Survey (USGS) and U.S. Fish and Wildlife Service through the Science Support Partnership Program via Research Work Order No. 211, administered through the USGS North Carolina Cooperative Fish and Wildlife Research Unit. In addition to Drs. Tom Kwak, Greg Cope, Chris Ingersoll, v Ning Wang, and Monte McGregor, I would like to thank Dr. Damian Shea, Dr. Christopher Owen, and Anthony Velasco for submitting the initial research proposal. vi TABLE OF CONTENTS LIST OF TABLES………………………………………………………………………….vii LIST OF FIGURES…………………………………………………………..……………..ix Chapter 1: A Comparison of the Chemical Sensitivities of In vitro and In vivo Propagated Juvenile Freshwater Mussels: Implications for Standard Toxicity Testing Guidelines………………………………………………………………………………….1 Abstract……………...………………………………………………………………………..2 Introduction……….………………………………………………………………………….3 Methods………….……………………………………………………………………………8 Results…………….…………………………………………………………………………13 Discussion……………….…………………………………………………………………..15 Acknowledgements……………...………………………………………………………….20 References……………………...……………………………………………………………21 Tables………………………………………………………………………………………..25 Figures……………………………………………………………………………………….29 Chapter 2: Influence of Age on Juvenile Freshwater Mussel Chemical Sensitivity: A Comparison of Progeny from Two Propagation Methods……………………….……….30 Abstract……………………………………………..…………………………………....….31 Introduction……………………………….………………………………………………...32 Methods…………………………………….………………………………………………..35 Results…………………………………….…………………………………………………39 Discussion……………………………………….…………………………………………..40 Acknowledgements…………………………………...…………………………………….44 References…………………………………………...………………………………………46 Tables………………………………………………………………………………………..49 Figures……………………………………………………………………………………….50 Appendix A………………………………………………………………………………….54 Appendix B………………………………………………………………………………….60 Appendix C………………………………………………………………………………….61 Appendix D………………………………………………………………………………….62 Appendix E……………………………………………………………………….…………68
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