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Using Genetic Tools to Understand the Population Ecology of Stream Fishes James Henry Roberts III Dissertation Submitted To

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Using Genetic Tools to Understand the Population Ecology of Stream Fishes James Henry Roberts III Dissertation Submitted To Using genetic tools to understand the population ecology of stream fishes James Henry Roberts III Dissertation submitted to the faculty of the Virginia Polytechnic Institute and State University in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Fish and Wildlife Conservation Paul L. Angermeier, Co-chairman Eric M. Hallerman, Co-chairman C. Andrew Dolloff J. Paul Grobler Marcella J. Kelly April 27th, 2012 Blacksburg, Virginia Keywords: darter, dispersal, endangered species, genetic diversity, landscape ecology, isolation- by-distance, metapopulation dynamics, persistence, population structure, stream fish Copyright 2012, James Roberts Using genetic tools to understand the population ecology of stream fishes James Henry Roberts III ABSTRACT Stream fishes are highly diverse, yet highly imperiled by human alterations of stream environments. Many species are poorly characterized with regard to the size and structure of populations and patterns of dispersal between populations, which complicates assessment of how human activities, both harmful and beneficial, will affect persistence. I used genetic tools to further this understanding in three case-study fish species of the southeastern United States: Roanoke logperch (Percina rex) of the greater Roanoke River basin and redline (Etheostoma rufilineatum) and greenside darters (E. blennioides) of the upper Tennessee River basin. I found that endangered P. rex persists in seven isolated populations. Within populations, individuals exhibit extensive dispersal and gene flow, which maintains connectivity throughout entire watersheds. Most populations exhibit small contemporary effective population sizes and occupy few stream channels, and thereby face an elevated risk of extinction. Genetic estimates of divergence indicate that fragmentation was recent, coincident with the construction of major dams throughout the species’ range. Close evolutionary relationships between most populations suggest that a translocation strategy could decrease extinction risks. I developed a framework to help guide the process of balancing small- population versus translocation risks when formulating conservation strategies. When the framework was applied to populations of P. rex, straightforward management prescriptions emerged. The framework also may prove useful for other fragmented species. Unlike P. rex, E. rufilineatum and E. blennioides are relatively abundant where they occur. However, both species were strongly affected by fragmentation due to hydroelectric dams and reservoirs. Populations in small streams flowing directly into a reservoir had lower genetic diversity than populations in larger, more fluvially connected streams. Furthermore, indices of watershed urbanization (e.g., percent impervious surface, road density) were negatively correlated with genetic diversity and with a genetic index of population stability. This suggests that darters occupying isolated streams and/or urbanizing watersheds experience smaller, more variable population sizes than darters elsewhere. Monitoring of such genetic responses could provide a useful early indicator of ecosystem stress and a useful complement to other biomonitoring techniques iii ACKNOWLEDGMENTS A PhD is a long journey that no one makes alone. My journey took longer than most, which enabled me to cross paths with many kindred spirits along the way. Over such a long period, some emotional ups and downs are inevitable. It was the support and fellowship of my personal and professional network that kept me progressing toward my goals. My graduate committee showed respect for my ever-evolving ideas and patience as those ideas ran their course. Committee Co-Chair Paul Angermeier has borne with me for a particularly long time, from my Master’s through my research position and now to the end of my PhD. I am forever grateful for his mentorship and friendship. My other Co-Chair Eric Hallerman, another good friend, has helped develop me into the molecular ecologist that I am. Committee members Andy Dolloff, Marcella Kelly and Paul Grobler have stuck with me through a project perched precariously at the intersection of several disciplinary frontiers – I thank them for their inquisitiveness and wisdom. While at Tech I spent over a third of my life in the water, assisted by an army of venerable field technicians, volunteers, and fellow grad students. Special praise is due to Greg Anderson, Jane Argentina, Matt Bierlein, Jackie Brown, Amy Bush, Tye DeWebber, Corey Dunn, Dan Dutton, Jason Emmel, Mark Foster, Annie Grant, Dylan Hann, Pat Kroboth, Tim Lane, Michael Lang, Bryan Neuswanger, Brett Ostby, Phil Pegelow, Brandon Peoples, Jen Philhower-Gillen, Jeremy Pritt, Bjorn Schmidt, and Chris Williams, who put in extended details on Team Logperch. Baby Blood and I bid you thanks. Once the field work was done and the fin clips were in the freezer, the tedium began. To that end, I was blessed to have the assistance of Dan Dutton and Joanne Printz, my lab-work gurus. They performed the vast majority of my extractions, PCR, and molecular troubleshooting, thereby preserving my sanity. I raise my pipette to you both. The research the reader finds in this dissertation derived from a variety of small, cobbled-together projects that several agencies were kind enough to fund. I am thankful to have had the opportunity for collaboration with these agencies and the biologists that represent them. I particularly appreciate the iv efforts of Mike Pinder and Scott Smith of VDGIF, William Hester and Kim Smith of USFWS, Phil Payonk and Michael Hosey of USACE, and Doug Beard of USGS to work with me to develop projects that met applied needs while enhancing the basic science of fish conservation. I thank my friends near and far for keeping me centered over the years. I refrain from listing names to protect the innocent, but you know who you are. Finally, my profoundest appreciation goes to my family – the Roberts women – who have shown infinite support and patience through an educational journey that seemed sometimes to have no end. My love for harlequined darters in sparkling streams is exceeded only by my love and admiration for Tonja, Holly, and Riley Roberts. I hope that they realize how much this dissertation owes to them. We in southwest Virginia at the beginning of the 21st century are fortunate to live in a time and place where spectacular wildlife still swims in our backyards. This appreciation is not widely felt. Although this dissertation took a long time to write, it was but a millisecond of ecological time. I’m aware of no fish species that went extinct during the writing of this document, though some species undoubtedly moved farther down that path. As conservation biologists, we chronicle the status of the natural world via a series of snapshots. Some day my particular snapshots will seem quaint to the future reader. My hope, however, is that my photographic subjects still will be around, going about their mysterious lives on some gravelly shoal. v TABLE OF CONTENTS GENERAL INTRODUCTION ................................................................................................................ 1 CHAPTER 1: Isolation by dams, not distance, creates discrete population structure in a riverine fish ....... 4 ABSTRACT ....................................................................................................................................... 4 INTRODUCTION............................................................................................................................... 5 METHODS ......................................................................................................................................... 7 Study species and area..................................................................................................................... 7 Sample collection ............................................................................................................................ 8 Laboratory methods ........................................................................................................................ 8 Data analysis ................................................................................................................................... 9 RESULTS ......................................................................................................................................... 12 DISCUSSION ................................................................................................................................... 15 Spatial scale and mechanisms of discrete population structure ....................................................... 15 Lack of regional IBD due to strong drift ........................................................................................ 18 Lack of local IBD due to strong migration ..................................................................................... 19 Applicability of the IBD model to riverine biota ............................................................................ 20 ACKNOWLEDGMENTS ................................................................................................................. 22 REFERENCES ................................................................................................................................. 23 CHAPTER 2: Extensive dispersal of Roanoke logperch (Percina rex) inferred from genetic marker data .............................................................................................................................................................
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