ABSTRACT Title of dissertation: STUDIES OF PERIPHYTIC ALGAE ON ALGAL TURF SCRUBBERS™ ALONG THE CHESAPEAKE BAY: COMMUNITY STRUCTURE, SYSTEMATICS, AND INFLUENCING FACTORS Haywood Dail Laughinghouse IV, Doctor of Philosophy, 2012 Directed by: Professor Patrick Kangas Department of Environmental Science & Technology, UMCP This is an ecological and systematic study of periphytic algae growing in an ecologically-engineered system used for water quality improvement: the Algal Turf Scrubber or ATSTM. This technology consists of an attached algal community growing on screens in a shallow floway through which water is pumped. The study was conducted on small-scale, experimental floways at three sites within the Chesapeake Bay watershed: on the Susquehanna River in southeastern Pennsylvania (freshwater) and on the Great Wicomico and York Rivers in Virginia (brackish water). A total of 330 taxa were identified at the sites from 2008-2011. The majority of taxa at all three sites belonged to the phylum Bacillariophyta, but a large number of taxa from Chlorophyta and, to a lesser degree, Cyanobacteria were also found at the freshwater site. Algae found in the ATSTM exhibited a diversity of life forms and modes of attachment within the community. Although these system appear to be dominated by a “canopy” of attached, filamentous species, more than half of the total abundance (cell density) were solitary, unattached taxa that grow as an “understory” within the three dimensional structure of the community. Longitudinal patterns were examined on the longest floways (90 m long) at the freshwater site. The community nutrient uptake rate (mass of nitrogen or phosphorus m-2 day-1) for the harvested algal biomass was found to decline from the top to the bottom of the floway for a system constructed at 2% slope but no distinct pattern was found for a system constructed at 1% slope. The majority of algal taxa were evenly distributed along the floway from top to the bottom, in terms of frequency of occurrence, suggesting a general lack of longitudinal specialization within the community. A detailed review of the systematics of the Order Oscillatoriales (Cyanobacteria) found on the ATSTM was undertaken since this group has not been studied much in the Chesapeake Bay watershed. Twenty-four taxa were examined, described morphologically and their nomenclature reviewed. Comparing 16s rRNA gene analyses of planktonic and periphytic Pseudanabaena, it was suggested that periphytic Pseudanabaena be revised and elevated to a new genus, Ilyonema STUDIES OF PERIPHYTIC ALGAE ON ALGAL TURF SCRUBBERS™ ALONG THE CHESAPEAKE BAY: COMMUNITY STRUCTURE, SYSTEMATICS, AND INFLUENCING FACTORS by Haywood Dail Laughinghouse IV Dissertation submitted to the Faculty of the Graduate School of the University of Maryland, College Park in partial fulfillment of the requirements for the degree of Doctor of Philosophy 2012 Advisory Committee: Professor Patrick C. Kangas, Chair Dr. Walter H. Adey, Co-Chair Professor Feng Chen Professor Charles F. Delwiche Dr. Kevin G. Sellner ©Copyright by Haywood Dail Laughinghouse IV 2012 To my life partner, Richard, for his understanding and support during this process. ii Acknowledgements This work could not have been finished without the help of many people. I would like to mention at least a few of them, and give them my heartfelt thanks. I would like to thank my advisors Dr. Patrick Kangas and Dr. Walter Adey, for their guidance and support throughout this research and my graduate journey. Dr. Kangas: thank you for your contagious enthusiasm, which was many times what I needed, friendship, and the ‘divide and conquer’ techniques to getting everything accomplished. I am also appreciative to the large ecological world, which you introduced to me. Dr. Adey: thank you for inviting me to come here, long insightful conversations over the years, and your trust. I have to thank my committee members, Dr. Feng Chen, Dr. Charles Delwiche, and Dr. Kevin Sellner. Each one of you has given personal time to help me throughout the years, and I thank you dearly, which has certainly contributed significantly to my molding. I appreciate the wonderful conversations we have all had in classroom settings, during committee meetings, and over coffee. I also appreciate the many criticisms and recommendations to perfect my work. My thanks go to several people, around the world, who have received calls and/or e-mails over the years and have always taken their time to help me in tackling scientific questions, especially: Dr. Maria Tereza Azevedo, Dr. Ricardo Honda, Dr. David John, Dr. Martyn Kelly, Dr. Cathy Kilroy, Dr. Hedy Kling, Dr. Jiri Komarek, Dr. Angelica Oliveira, Dr. Celia Sant’Anna, Dr. Vera Werner, Dr. Brian Whitton, and Dr. Annick Wilmotte. iii My thanks go out to other colleagues/friends that helped me with work and life during this process, Angélica, Karen, Maíra, Melissa, Pia, Solange, and Sue. Thanks are also extended to my previous supervisors Dr. Vera Werner and Dr. Jeff Johansen for helping show me the algal way. I am grateful to the Lewis Foundation, Statoil-Hydro, the Natural History of Natural History-SI, and the University of Maryland for financial support and/or facilities. I would like to thank my mother and father who instilled many admirable qualities in me which gave me a great foundation to take to life. I would like to thank my brother and sister, Joseph and Melissa, for the several phone calls I made when I was stressed about something or another, and having to learn about periphyton, ATSTM, cyanobacterial systematics…and the importance it is in their lives to help talk me through ideas. Last, but certainly not least, I must acknowledge with tremendous and deep thanks my partner who has gone through this rollercoaster ride with me, enduring my travels, long nights, stress, and mood changes while studying, doing the research, and writing. Richard, I thank you for patiently waiting while I finish this step in my academic journey and being there when I needed you, as always. Muito obrigado e te amo muito. iv TABLE OF CONTENTS Chapter 1: Introduction 1 General introduction 1 The algal turf scrubber (ATSTM) system 2 Periphyton 7 Site Descriptions 11 ATSTM Design 15 Chapter 2: Community composition and dynamics of periphytic algal communities of ATSTM systems along Chesapeake Bay tributaries 17 Introduction 17 Materials & Methods 20 Sampling 20 Qualitative analysis 21 Quantitative analysis 22 Statistical Treatment 23 Life History Classification 23 Diversity 24 Results 24 ATSTM at the Boat Basin of the VIMS 24 Source Communities 24 Species Diversity 28 Algal Abundance 35 Great Wicomico River ATSTM 39 v Algal Turf Scrubber Floway 1 39 Species Diversity 39 Algal Abundance 45 Algal Turf Scrubber Floway 2 50 Species Diversity 50 Algal Abundance 55 Muddy Run Reservoir ATSTM 60 Aluminum Floway 60 Species Diversity 60 Wood Floway 70 Species Diversity 70 Similarity among sites 81 Discussion 88 Chapter 3: Longitudinal patterns of periphytic algal communities of ATSTM systems at Muddy Run Reservoir, PA 97 Introduction 97 Materials and Methods 102 Study Area 102 Nutrients 103 Sampling 103 Qualitative analysis 104 Longitudinal patterns in algae: specialists vs. generalists 105 Statistical treatment 105 Results 106 Nutrients 106 vi Nutrients in Biomass 107 Algal Community Structure 114 Specialization Index 115 Discussion 119 Chapter 4: Systematic studies on periphytic Oscillatoriales (Cyanobacteria) from ATSTM floways along the Chesapeake Bay 128 Cyanophyceae/Cyanobacteria 128 Taxonomy/Systematics of Cyanobacteria 129 Order Oscillatoriales 131 Subchapter 1 135 Subchapter 2 167 Chapter 5: Final Conclusions 177 Algal Turf Communities 177 Taxonomy/Systematics in applied studies 180 Future Directions 182 Summary 184 Appendices 189 References 276 vii LIST OF TABLES Table 1.1. The different designs of ATSTM systems used during the study ………….… 15 Table 2.1. List of species found in the source communities (‘species-pool’) at VIMS ... 26 Table 2.2. Algal community structure on the VIMS Boat Basin floway during 2009-2010. Density values are numbers of individuals x 103 per square centimeter of screen surface. Numbers in parentheses are percentage of the total (diatom + non-diatom) average density. Frequency is the number of occurrence among the 7 sample dates …………………………………...….. 38 Table 2.3. Algal community structure on the Great Wicomico Floway 1 during 2010-2011. Density values are numbers of individuals per milliliter. Numbers in parentheses are percentage of the total (diatom + non-diatom) average density. Frequency is the number of occurrence among the 13 sample dates …………………………………………………………...……. 48 Table 2.4. Algal community structure on the Great Wicomico Floway 2 during 2010-2011. Density values are numbers of individuals per milliliter. Numbers in parentheses are percentage of the total (diatom + non-diatom) average density. Frequency is the number of occurrence among the 14 sample dates …………………………………………………………...……. 58 Table 2.5. Algal community structure on the aluminum floway at the Muddy Run Reservoir ATSTM, 2008-2009 ……………………………………………… 60 Table 2.6. Algal community structure on the wood floway at the Muddy Run Reservoir ATSTM, 2008-2009 ……………………………………………… 70 viii Table 2.7. List of the periphytic community at the ATSTM floways located at Muddy Run, Great Wicomico, and VIMS ………………………………….. 81 Table 2.8. Total taxa of each algal group on the ATSTM floways at the different studied sites ……………………………………………………………….… 93 Table 3.1 Mean nutrient removal midday