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Abstract Poteat, Monica Deshay ABSTRACT POTEAT, MONICA DESHAY. Comparative Trace Metal Physiology in Aquatic Insects. (Under the direction of Dr. David B. Buchwalter). Despite their dominance in freshwater systems and use in biomonitoring and bioassessment programs worldwide, little is known about the ion/metal physiology of aquatic insects. Even less is known about the variability of trace metal physiologies across aquatic insect species. Here, we measured dissolved metal bioaccumulation dynamics using radiotracers in order to 1) gain an understanding of the uptake and interactions of Ca, Cd and Zn at the apical surface of aquatic insects and 2) comparatively analyze metal bioaccumulation dynamics in closely-related aquatic insect species. Dissolved metal uptake and efflux rate constants were calculated for 19 species. We utilized species from families Hydropsychidae (order Trichoptera) and Ephemerellidae (order Ephemeroptera) because they are particularly species-rich and because they are differentially sensitive to metals in the field – Hydropsychidae are relatively tolerant and Ephemerellidae are relatively sensitive. In uptake experiments with Hydropsyche sparna (Hydropsychidae), we found evidence of two shared transport systems for Cd and Zn – a low capacity-high affinity transporter below 0.8 µM, and a second high capacity-low affinity transporter operating at higher concentrations. Cd outcompeted Zn at concentrations above 0.6 µM, suggesting a higher affinity of Cd for a shared transporter at those concentrations. While Cd and Zn uptake strongly co-varied across 12 species (r = 0.96, p < 0.0001), neither Cd nor Zn uptake significantly co-varied with Ca uptake in these species. Further, Ca only modestly inhibited Cd and Zn uptake, while neither Cd nor Zn inhibited Ca uptake at concentrations up to concentrations of 89 nM Cd and 1.53 µM Zn. Ca, Cd and Zn bioaccumulation parameters all varied across orders of magnitude within the two families examined. Familial differences were striking across uptake rate constants and bioconcentration factors, however not across efflux rate constants. Body size was an important driver of uptake rate constants (and consequentially, bioconcentration factors). While the variation in Cd uptake and efflux rate constants was previously shown to be heavily influenced by phylogenetic position in species from orders Ephemeroptera, Plecoptera and Trichoptera, the tremendous variability displayed by these two families effectively erased the phylogentic signal. In analyses of all available Cd uptake and efflux rate constants for aquatic insects from this study and from the literature, we discovered clade (as genus) to explain significant amounts of variation across metal bioaccumulation parameters. Analyses across more taxonomically-divergent aquatic organisms identified phylogenetic signal in efflux rate constants across four aquatic phyla. Further, the strong co- variation of Zn and Cd efflux rate constants in hydropsychids and ephemerellids led to successful predictions of Zn uptake rate constants from known Cd values in five of six aquatic insect species. This work has led to two overall conclusions which should be taken into consideration when using aquatic insect data in regulatory toxicology. First, aquatic insects appear to have trace metal physiologies which differ from other aquatic organisms (e.g., fish, Daphnia) regarding the trafficking of dissolved metal. Hypocalcemia does not appear to be the mechanism of toxicity in dissolved Cd/Zn as evidenced by the lack on interactions between Ca and Cd/Zn. This potentially contributes to their acute metal tolerance in the laboratory (as opposed to their observed metal sensitivity in the field). Second, aquatic insects, particularly within families Hydropsychidae and Ephemerellidae, have highly variable physiologies. This has important implications in that we need to better understand how well “surrogate species” represent their fellow congeners and account for the variation in aquatic risk assessments aimed at protecting insect diversity. © Copyright 2014 by Monica Deshay Poteat All Rights Reserved Comparative Trace Metal Physiology in Aquatic Insects by Monica Deshay Poteat A dissertation submitted to the Graduate Faculty of North Carolina State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Toxicology Raleigh, North Carolina 2014 APPROVED BY: _______________________________ ______________________________ Dr. David B. Buchwalter Dr. Gerald A. LeBlanc Committee Chair ________________________________ ________________________________ Dr. Tom Augspurger Dr. Eric A. Stone BIOGRAPHY Monica Deshay Poteat was born in Kannapolis, NC, on July 6, 1988, to parents Pat and Judy Poteat. After graduating from A.L. Brown High School in 2006, she stayed in North Carolina to pursue a biology/pre-med degree at Elon University (because what else can you do with a biology degree other than go to medical school?). While at Elon, Monica quickly became interested in environmental research. She was able to conduct independent research projects on tree allelopathy in Great Smoky Mountains National Park and nitrogen cycling at the Virginia Institute for Marine Sciences. It was during these research experiences that Monica decided that the laboratory was where she would rather base her career. During her last year and a half at Elon, Monica began researching graduate programs in the biological sciences. It was during this time that she stumbled upon the field of Environmental Toxicology. She began emailing faculty in programs of interest to her, and became especially interested in the comparative, interdisciplinary work in Dr. David Buchwalter’s laboratory (despite never having even thought about aquatic insects before). Monica joined the Buchwalter lab in June of 2010, 10 days after graduating from Elon University with a B.S. in Biology. She hit the ground running and hasn’t looked back since. ii ACKNOWLEDGMENTS First and foremost, I’d like to thank my advisor, Dr. David Buchwalter. He has been an exemplary major (and life) advisor. Under his guidance, I have become a better scientist, better writer, better presenter, and I’ve learned to better balance work and play. Through his confidence in me, I gained confidence in myself. I would also like to thank my committee members Dr. Gerald LeBlanc, Dr. Tom Augspurger and Dr. Eric Stone. I greatly appreciate their input and assistance throughout my time at NC State. I am indebted to the members of the Buchwalter laboratory, past and present, including Dr. Justin Conley, Allison Camp, Jeanne Burr, Shane Scheibener, Beth Dittman, Dr. Kyoung Sun Kim, and Dr. Lingtian Xie, for their assistance in the field and laboratory. Other Toxicology folks were also extremely helpful throughout my time at NC State. Janet Roe kept me on track with what forms to fill out and when to do it. Jackie Broughton was especially helpful with funding questions and the many travel authorizations that took me from Raleigh to the Smokies. Other outside collaborators were invaluable to this project. Dr. Ted Garland, Jr. provided assistance with learning phylogenetic statistics and the software programs used to calculate the statistics. Dr. Luke Jacobus provided invaluable aid in insect identification throughout my research and drove many (many many) miles to aid in insect collection in the Smokies. Luke also was also always willing to lend an open ear or a helping hand on anything I asked. Eric Fleek provided many spur-of-the-moment insect identifications that were greatly appreciated. iii I thank my family and friends for their support and never-ending encouragement throughout this journey through graduate school. I thank my parents for always encouraging me to follow my dreams, for cheering me on throughout my academic career, and for always being supportive of any decisions, good or bad, along the way. I especially thank my husband, Graham Medlin, for his love and patience throughout my graduate career. He made many trips to the Smokies with me as an extra pair of hands, and he was always willing to keep me company during the many late nights spent in lab running long time course experiments (and was always up for a Cook-Out run after a late night in the lab). Last, but certainly not least, this work would not have been possible without my funding sources. The National Science Foundation, the SETAC/ICA Chris Lee Award for Metals Research, and North Carolina State University generously provided funding which made the completion of this project possible. iv TABLE OF CONTENTS LIST OF TABLES .................................................................................................... vii LIST OF FIGURES ................................................................................................... ix General Introduction ...................................................................................................1 Overview on aquatic insects ..........................................................................................1 Aquatic insects in ecological assessments .....................................................................2 Trace metals and their effects on aquatic insects in the laboratory and field ................3 Modeling of trace metal bioaccumulation .....................................................................5 Areas of concern in regulatory toxicology .....................................................................8 Comparative phylogenetic methods .............................................................................10
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