The Micro-Ecology of Stream Biofilm Dynamics: Environmental
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THE MICRO-ECOLOGY OF STREAM BIOFILM DYNAMICS: ENVIRONMENTAL DRIVERS, SUCCESSIONAL PROCESSES, AND FORENSIC APPLICATIONS Dissertation Submitted to The College of Arts and Sciences of the UNIVERSITY OF DAYTON In Partial Fulfillment of the Requirements for The Degree of Doctor of Philosophy in Biology By Jennifer M. Lang Dayton, Ohio August, 2015 THE MICRO-ECOLOGY OF STREAM BIOFILM DYNAMICS: ENVIRONMENTAL DRIVERS, SUCCESSIONAL PROCESSES, AND FORENSIC APPLICATIONS Name: Lang, Jennifer M. APPROVED BY: ___________________________________ Ryan W. McEwan, Ph.D Faculty Advisor ___________________________________ M. Eric Benbow, Ph.D Faculty Advisor __________________________________ Robert J. Kearns, Ph.D Committee Member __________________________________ Thomas M. Williams, Ph.D Committee Member __________________________________ Heather R. Jordan, Ph.D Committee Member ii ABSTRACT THE MICRO-ECOLOGY OF STREAM BIOFILM DYNAMICS: ENVIRONMENTAL DRIVERS, SUCCESSIONAL PROCESSES, AND FORENSIC APPLICATIONS Name: Lang, Jennifer M. University of Dayton Advisor: Dr. Ryan W. McEwan Microbial activity has an essential role in ecosystem processes, and in stream ecosystems, biofilms are the base of the food web that is fueled by photosynthesis and they are integral to nutrient processing. Stream biofilms are microbial communities of algae, bacteria, fungi, and protozoa encased in an extracellular polymeric substance (EPS) (molecules secreted by the microbes) that are attached to a substrate (e.g. rocks, leaves) in an aqueous environment. The substrate categorizes the biofilm, and organic matter like leaves and carrion such as salmon carcasses are important substrates for nutrient dynamics. In special instances, human remains may be deposited into streams and colonized by biofilms; therefore, assessing these biofilms can have direct application to the forensic sciences. Stream ecologists have extensively investigated how environmental factors influence algal community composition, while environmental microbiologists have focused on the role of bacterial communities in nutrient dynamics. My dissertation marries these two approaches by considering biofilm communities as a iii functioning ecosystem and uses ecological theory as a framework to understand the dynamics of this micro-ecosystem. This framework uses aspects from landscape ecology within a larger context of community ecology to explain how the development of biofilm communities is altered by environmental factors. In addition, this framework was used to investigate biofilm development on carrion (dead animal) in a forensic science context. iv ACKNOWLEDGEMENTS I would like to thank my advisors Drs. M. Eric Benbow and Ryan W. McEwan for providing me the opportunity and support that has allowed me to develop into an independent scientist. First, I thank Dr. Benbow for inviting me into his lab and for the depth and breadth of experiences that ensued. Secondly, I am thankful to Dr. McEwan for graciously taking over and managing the final steps in finishing my degree. The unwavering support was truly appreciated. I would also like to thank my committee members Drs. Robert J. Kearns, Carl Friese, Thomas M. Williams, and Heather R. Jordan for their helpful input throughout this process. Ample waves of gratitude are designated for the extra help provided by the undergraduates, graduates, and associated individuals. Rachel Erb, Tiffany Blair, Mary Timko, Joe Rockner, Jon White, Allison Gansel, Nikki Henger, Jamie Alferi, Will Kmetz, Lauren Shewhart, Alex Calteaux, Patrick Vrablik, and Ali Wright were all undergraduates that contributed to data sampling and processing. Andy Lewis, Rachel McNeish, Kathy Gorbach, and Allissa Blystone were graduate students that provided helpful discussions and constant support. The same is true for Dr. Phil Nickell and Dr. Jen Pechal. I would also like to thank the Baudendistel family for providing a site to conduct the aquatic decomposition study in Farmersville, OH, and Dr. John R. Wallace and Rachel Erb for conducting the decomposition study in Millersville, PA. Lastly, I am v extremely thankful to my friends and family for their constant support and understanding when my dedication to this endeavor meant I could not spend as much time with them as I would have enjoyed. Additional thanks go to the University of Dayton Biology Department for financial support and utilization of equipment. This work has also been supported in part by the University of Dayton Office of Graduate Academic Affairs through the Graduate Student Summer Fellowship and the Dissertation Year Fellowship. In addition, the Penn State University Swine Research facility is acknowledged for providing stillborn fetal piglets. vi TABLE OF CONTENTS ABSTRACT ....................................................................................................................... iii! ACKNOWLEDGEMENTS ................................................................................................ v! LIST OF TABLES .............................................................................................................. x! LIST OF FIGURES ......................................................................................................... xiii! CHAPTER 1. INTRODUCTION ....................................................................................... 1! Overview ................................................................................................................. 1! Stream Biofilms ...................................................................................................... 4! Biofilm Succession ..................................................................................... 5! Biofilm Architecture ................................................................................... 7! Biofilm Function ......................................................................................... 9! Community Ecology ............................................................................................. 11! Competition ............................................................................................... 12! Predation and Herbivory ........................................................................... 15! Symbiosis: Mutualism, Commensalism, and Parasitism .......................... 16! Summary ................................................................................................... 18! Forensic Sciences .................................................................................................. 19! Forensic Entomology ................................................................................ 20! Aquatic Forensic Entomology .................................................................. 21! vii Alternative Methods for PMSI Estimates ................................................. 23! Literature Cited ..................................................................................................... 27! CHAPTER 2. ABIOTIC AUTUMNAL ORGANIC MATTER DEPOSITION AND GRAZING DISTURBANCE EFFECTS ON EPILITHIC BIOFILM SUCCESSION .... 34! Abstract ................................................................................................................. 34! Introduction ........................................................................................................... 35! Methods ................................................................................................................. 39! Results ................................................................................................................... 48! Discussion ............................................................................................................. 51! Literature Cited ..................................................................................................... 57! Tables .................................................................................................................... 66! Figures ................................................................................................................... 71! CHAPTER 3. FREQUENT DISTURBANCE FACILITATES THE EFFECT OF ENVIRONMENTAL FACTORS DURING AUTUMN ON EPILITHIC BIOFILM COMMUNITY ASSEMBLY ........................................................................................... 76! Abstract ................................................................................................................. 76! Introduction ........................................................................................................... 77! Methods ................................................................................................................. 81! Results ................................................................................................................... 87! Discussion ............................................................................................................. 90! Literature Cited ..................................................................................................... 98! Tables .................................................................................................................. 105! Figures ................................................................................................................. 108! viii CHAPTER 4. BOTTOM-UP AND TOP-DOWN INTERACTIONS BETWEEN INVERTEBRATE GRAZERS AND EPILITHIC BIOFILMS DICTATE BIOFILM COMMUNITY STRUCTURE THROUGHOUT SUCCESSION ................................. 114!