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Disturbance in the Anchialine Ecosystem: Ramifications for Ecology and Physiology

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Disturbance in the Anchialine Ecosystem: Ramifications for Ecology and Physiology Disturbance in the anchialine ecosystem: ramifications for ecology and physiology by Justin Chase Havird A dissertation submitted to the Graduate Faculty of Auburn University in partial fulfillment of the requirements for the Degree of Doctor of Philosophy Auburn, Alabama May 3, 2014 Keywords: ecophysiology, invasive species, crustacean, osmoregulation, gene expression Copyright 2014 by Justin Chase Havird Approved by Scott R Santos, Chair, Associate Professor of Biological Sciences Raymond P. Henry, Professor of Biological Sciences Mark R. Liles, Associate Professor of Biological Sciences Alan E. Wilson, Associate Professor of Biological Sciences/Fisheries, Aquaculture, and Aquatic Sciences Abstract Habitats in the anchialine ecosystem are defined as coastal ponds, pools, and caves that lack surface connections to the open ocean, but possess both seawater and freshwater influences due to subterranean connections to the ocean and groundwater. Such habitats are rare worldwide, but are concentrated in the Hawaiian Islands. Organisms that live in these habitats must cope with changing salinities, variable oxygen regimes, high levels of UV radiation, and anthropogenic effects such as pollution and invasive species. Accordingly, such organisms represent an opportunity to shed light on environmental physiology and invasive species biology. However, few studies have investigated physiology or response to invasive species in anchialine organisms. Accordingly, the objective of this dissertation is to examine the effect of natural and anthropogenic disturbances on the physiology and ecology of anchialine organisms. Chapter 1 provides an introduction to the anchialine ecosystem and outlines the specific aims of the dissertation. Chapter 2 presents a series of field and laboratory based experiments investigating how endemic Hawaiian anchialine organisms have responded to invasive fishes. Based on its results, endemic anchialine organisms largely avoid predation by invasive fishes by adopting an alternative strategy of diel migration in fish-invaded habitats. Chapter 3 provides a quantitative, statistical review of how previously-studied animals respond to changing salinity via altering gene expression. The results of this meta-analysis suggest that up-regulation of a suite of genes is typical for crustaceans undergoing salinity transfers, although studies have mostly been confined to a narrow taxonomic range of decapod brachyurans (i.e., crabs). Chapter 4 seeks to remedy this ii lack of knowledge by examining how the endemic Hawaiian anchialine atyid shrimp Halocaridina rubra responds to fluctuating salinity at the organismal, tissue, cellular, and molecular level. These results suggest H. rubra (and possibly other anchialine crustaceans) has continually expressed osmoregulatory mechanisms, including high, constitutive levels of osmoregulatory gene expression, which is in stark contrast to previously studied crustaceans. Chapter 5 examines how H. rubra and anchialine shrimps from the Ryukyus Archipeligo of Japan respond to low-oxygen conditions. By examining metabolic characteristics under varying oxygen regimes, it is concluded that H. rubra has gills that are specialized for osmoregulation, but not respiration, requiring a high resting ventilation rate and resulting in a strategy of oxyconformation. The other species have a different strategy more consistent with previously described mechanisms in crustaceans. Lastly, Chapter 6 provides conclusions, synthesis of the preceding chapters, and future directions. iii Acknowledgments I am extremely grateful to my dissertation committee for challenging me to develop and undertake this dissertation research: Drs. Ray Henry, Mark Liles (oh, hi Mark), Alan Wilson, and especially my advisor, Scott Santos. Scott, during my time here you’ve served many roles: mentor, role-model, teacher, critic, arch-nemesis, and stereotypical Hawaiian. We have not always seen eye to eye on things, but this experience has prepared me for the challenges ahead. Members of the Molette lab have provided me with both academic and liquid encouragement (ample of the latter). The guilty parties include Pam Brannock, Kevin Fielman, Alexis Janosik, Matt Galaska, Damien Waits, Amanda Shaver, Franzi Franke, Stephanie Irvin, David Branson, Li Yuanning, and Kevin Kocot. I’m especially indebted to my academic brothers in the Santos Lab, David Weese and Nathan Kirk, for laying the tracks that allowed my train to gradually plow through Mt. Santos. I’ve been extremely fortunate to mentor several undergraduates during my PhD tenure: Jennifer Heim, Jeffrey Weeks, Kiley Seitz, Rebecca Vaught, and Katelyn Hatfield. I am very grateful for the assistance they’ve provided me and very proud of the independent research they’ve undertaken. My research has involved many collaborators across the world, and I have tried to acknowledge them in each chapter as appropriate, but I especially thank Drs. Michio Hidaka and Yoshihisa Fujita for hosting me in Japan during Summer 2013. Many funding agencies have also been unwittingly duped into giving me money to pursue the research presented here, and I am especially grateful to the National Science Foundation, the PADI Foundation, EPSCoR Alabama, and The Crustacean iv Society. I also wish to extend a heartfelt thanks to all the staff in the Dept. of Biological Sciences, especially Sandra Abate, Jo Ann Broach, Paula Norrell, and Anjali Dabhade for helping me navigate the bureaucratic hellscape that is Auburn University. Thank you to my friends Ankur Shukla, Anthony Rodriguez, Ryan McCleary, Reni Kaul, Shanna Hanes, Stephen Sefick, Emily Kirk, Kathy Morrow, and all the lab members mentioned above (as well as many others) for your support during times of both commiseration and celebration. I’m also very lucky to have Joshua Havird as a brother and Kurt and Dawn Havird as parents. Although my choice to pursue this degree may have seemed questionable at times (a sentiment I have shared), your support and encouragement have hopefully prepared me to finally enter the real world. Finally, the biggest thanks go to my fiancée, Jennifer Parker. She has constantly sacrificed her own ambitions in order for me to pursue mine. She has been there every step of the way during this ordeal, from my interview as a potential student, through the long nights and weekends in the lab, while I’ve been at some tropical field site and she’s been forced to stay in Auburn, and now, finally, at the end of this journey. She’s been my primary shoulder to cry on, my biggest advocate, and even a collaborator. There is no doubt that without her support, I would not have been able to accomplish a fraction of what I have, and I’m most grateful that she has agreed to continue to stick by my side as my “future wife”. This dissertation is dedicated in memory of Aleene Markham Havird (1927-2011), whose love is deeply missed. Meme: there’s finally a doctor in the family. v Table of Contents Abstract ......................................................................................................................................... ii Acknowledgments........................................................................................................................ iv List of tables ................................................................................................................................. xi List of figures .............................................................................................................................. xii List of abbreviations ................................................................................................................... xv Chapter 1. Introduction to dissertation.......................................................................................... 1 1.1 Introduction to the anchialine ecosystem .................................................................... 1 1.1.1 Environmental characteristics of anchialine habitats .......................................... 2 1.1.2 Invasive species in the Hawaiian anchialine ecosystem ..................................... 3 1.1.3 Physiology of Hawaiian anchialine organisms ................................................... 5 1.2 Objectives ................................................................................................................... 8 1.3 Importance and relevance of dissertation research ..................................................... 9 1.4 References ................................................................................................................. 13 Chapter 2. Invasive fishes in the Hawaiian anchialine ecosystem: investigating potential predator avoidance by endemic organisms ................................................................................... 21 2.1 Abstract ..................................................................................................................... 21 2.2 Introduction ............................................................................................................... 22 2.3 Materials and methods .............................................................................................. 24 2.3.1 Study sites ......................................................................................................... 24 vi 2.3.2 Diel surveys of anchialine shrimp..................................................................... 25 2.3.3 Gut content analyses of invasive fishes ...........................................................
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