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INFLUENCE OF NATIVE FRESHWATER MUSSEL FUNCTIONAL TRAITS AND COMMUNITY STRUCTURE ON NITROGEN REMOVAL IN STREAM SEDIMENTS by ZACHARY LYNN NICKERSON CARLA L. ATKINSON, COMMITTEE CHAIR BEHZAD MORTAZAVI LISA DAVIS ROBERT H. FINDLAY A THESIS Submitted in partial fulfillment of the requirements for the degree of Master of Science in the Department of Biological Sciences in the Graduate School of The University of Alabama TUSCALOOSA, ALABAMA 2018 Copyright Zachary Lynn Nickerson 2018 ALL RIGHTS RESERVED ABSTRACT Animals physically and chemically modify their environment as a result of their functional traits. These effects are particularly influential in freshwater benthic environments where animal aggregations can impact the recycling and repackaging of major macronutrients. I examined the influence of native freshwater mussels (Bivalvia: Unionidae) on the removal of dissolved inorganic nitrogen (N) via the biogeochemical pathways of denitrification and annamox in freshwater sediments. In one experiment, I used continuous flow-through incubation + methods to assess the influence of individual mussel physiological traits (ammonium [NH4 ] excretion, organic matter [OM] biodeposition) on N-removal in stream sediments. In the second experiment of my thesis, I manipulated the biodiversity of mussel aggregations in their natural environment using in-situ stream benthic enclosures to assess the influence of mussel aggregations, associated functional traits, and the effect of mussel biodiversity on N-removal. + Incubation results showed NH4 excretion increased the ambient flux of dinitrogen gas (N2) across the sediment-water interface, while OM biodeposition increased the maximum N-removal potential in the sediment. Results of the in-stream enclosure experiment showed there were non- additive effects of mussel biodiversity on N-removal in stream sediments. Results suggested this effect was driven by an increase in biological activity (movement, burrowing), potentially driven by inter-specific competition among species with different niche requirements. My thesis research advances the field by linking specific mussel functional traits to an important ecosystem function, N-removal, and showing the importance of incorporating biodiversity into aggregate- scale studies of organisms’ influences on biogeochemical ecosystem processes. ii DEDICATION To my family, especially my parents Jeff and Sheryl, my siblings Tyler, Emily and Sydney, and my wonderful wife Anastasia, for their unending love and support. Also, to Drs. Joy O’keefe and Jennifer Latimer for fueling my passion for research. iii LIST OF ABBREVIATIONS AND SYMBOLS AFDM Ash-free dry mass AL Alabama ANCOVA Analysis of covariance ANOVA Analysis of variance Annamox Anaerobic ammonium oxidation ARW Artificial river water BD-EF Biodiversity-ecosystem function framework C Carbon C. asperata Cyclonaias asperata C.B. Charge balance Ca2+ Calcium ion CaCO3 Calcium carbonate Cl- Chloride ion cm Centimeter cm3 Cubic centimeter CO2 Carbon dioxide Con. Conductivity Coupled-DNF Coupled nitrification-denitrification d Day d-1 Per day iv DIN Dissolved inorganic nitrogen DISL Dauphin Island Sea Lab DM Soft tissue dry mass Dmax Strongest effect of complementarity possible for an ecosystem function DNF Denitrification DO Dissolved oxygen DT Strength of complementarity for a specific ecosystem function EF Ecosystem function e.g. exempli gratia (“for example”) F F-statistic to determine significantly different means (analysis of variance) F. flava Fusconaia flava g Gram h-1 Per hour H2O Water - NCO3 Bicarbonate ion hr, h Hour i Species i.e. id est (“that is”) IPT Isotope pairing method K+ Potassium ion K2SO4 Potassium sulfate kg Kilogram kg-1 Per kilogram v km Kilometer L Liter L-1 Per liter L. ornata Lampsilis ornata m meter m2 Square meter m3 Cubic meter m-2 Per square meter mg Milligram Mg2+ Magnesium ion MgCl2 Magnesium chloride MgSO4*7H2O Magnesium sulfate heptahydrate microcosm-1 Per microcosm MIMS Membrane inlet mass spectrometer min-1 Per minute mL Milliliter mm Millimeter mM Millimolar (Millimoles per liter) mmol Millimole n Sample size N Nitrogen N Mussel abundance (individuals m-2) N2 Dinitrogen gas vi N2-N Mole of nitrogen derived from dinitrogen gas 29 N2 Dinitrogen gas derived from anaerobic ammonium oxidation 30 N2 Dinitrogen gas derived from denitrification N2:Ar method Method to determine the concentration dinitrogen gas in water samples Na+ Sodium ion NaCl Sodium chloride NaHCO3 Sodium bicarbonate + NH4 Ammonium 14 + NH4 Naturally-abundant ammonium molecule - NO2 Nitrite - NO3 Nitrate — NO3 N Mole of nitrogen derived from nitrate 15 - NO3 Isotopically-labeled nitrate N-removal Transformation of dissolved inorganic nitrogen to dinitrogen gas N-species Any molecule containing a nitrogen atom NTU Nephelometric Turbidity Unit O2 Oxygen OM Organic matter P Phosphorus p p-value for determining significant results in statistical analyses pi,N Proportion of species i at density-level N PCA Principal component analysis pCO2 Partial pressure of carbon dioxide vii PC1 Principal component one PC2 Principal component two R2 Coefficient of determination (regression) Redox Reduction-oxidation s-1 Per second S1 Stock solution one for the synthesis of artificial river water S2 Stock solution two for the synthesis of artificial river water S3 Stock solution three for the synthesis of artificial river water SE Standard error of the mean SLR Simple linear regression 2- SO4 Sulfate ion Sp. Con. Specific Conductivity species-1 Per mussel species t Symbol representing the beginning of an incubation trial T0 Start of sediment slurry incubation T6 End of sediment slurry incubation Tukey HSD Tukey’s Honest Significant Difference multiple comparison test UA University of Alabama vol-1 Per volume of solution w/v Percent of molecule in total volume of solution 푥̅ Mean ZnCl2 Zinc chloride 2D Two dimensional viii 1.1x One and one tenth times 2x Two times 3x Three times 1000x One thousand times α Alpha value defining confidence interval for statistical analysis ΔEF Net effect of biodiversity ε(EFpoly) Expected effect of biodiversity on an ecosystem function σ Standard deviation ΣAZ- Sum of concentrations (in microequivalents) for all anions in solution ΣCZ+ Sum of concentrations (in microequivalents) for all in solution µeq Microequivalent µL Microliter µm Micrometer µmol Micromole µS Microsiemen °C Degree Centigrade << Much less than < Less than > Greater than ≥ Greater than or equal to = Equals ≠ Does not equal ~ Approximately ix ± Plus or minus + Plus - Negative x By % Percent [ ] Concentration in millimoles per liter # Number of → Forward reaction x ACKNOWLEDGEMENTS I would like to sincerely thank my advisory committee Carla L. Atkinson, Behzad Mortazavi, Lisa Davis and Robert H. Findlay for their valuable support and advice throughout my time at the University of Alabama. Thank you to the Mortazavi lab at Dauphin Island Sea Lab, including Alice Kleinhuizen, Dr. Corianne Tatariw, Derek Tollette and Taylor Ledford, for helping me learn how to run chamber incubations, analyze sediment and water samples, and analyze the data that formed the bulk of my thesis. Also, thank you to our collaborators in the Davis lab at the University of Alabama Department of Geography, especially Matt Koerner, for working hard to make the in-stream enclosure experiment a success. Thank you to my lab mates Brian van Ee and Monica Winebarger, without whom my fieldwork would not have been possible. I would like to send a huge thank you Anne Bell to whom I owe a debt of gratitude for teaching me the use of and care for the analytical instruments used in our lab, and for helping me analyze hundreds of water and sediment samples. I would like to acknowledge the Birmingham Audubon Society and the Conchologists of America, Inc. for funding the majority of my thesis research. Also, thank you to the University of Alabama’s Department of Biological Sciences, College of Arts and Sciences, and Graduate School Association for providing some research and travel funding. Thank you to Dauphin Island Sea Lab for providing lodging while I conducted research in the Mortazavi lab. I would like to thank the Weyerhaeuser Company for allowing us to access their land along the Sipsey River to conduct our in-stream experiment, and to collect mussels, sediment and site water for the incubation trials. Last but not least, thank you to my family and friends for always supporting me even when they found out I studied mussel poop. xi CONTENTS ABSTRACT.................................................................................................................................................ii DEDICATION............................................................................................................................................iii LIST OF ABBREVIATIONS AND SYMBOLS...................................................................................iv ACKNOWLEDGEMENTS......................................................................................................................xi LIST OF TABLES...................................................................................................................................xiii LIST OF FIGURES.................................................................................................................................xiv CHAPTER 1: CONCEPTUAL FRAMEWORK AND SUMMARY OF OBJECTIVES.................1 CHAPTER 2: USING FUNCTIONAL TRAITS TO DETERMINE THE INFLUENCE OF BURROWING BIVALVES ON NITROGEN REMOVAL
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