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Freshwater Algae of North America Freshwater Algae of North America Ecology and Classification Edited by John D. Wehr Louis Calder Center—Biological Station Fordham University Armonk, New York, USA Robert G. Sheath Department of Biological Sciences California State University San Marcos San Marcos, California, USA J. Patrick Kociolek Department of Ecology and Evolutionary Biology and Museum of Natural History University of Colorado Boulder, Colorado, USA University of Michigan Biological Station Pellston, Michigan, USA AMSTERDAM (cid:127) BOSTON (cid:127) HEIDELBERG (cid:127) LONDON NEW YORK (cid:127) OXFORD (cid:127) PARIS (cid:127) SAN DIEGO SAN FRANCISCO (cid:127) SINGAPORE (cid:127) SYDNEY (cid:127) TOKYO Academic Press is an imprint of Elsevier Academic Press is an imprint of Elsevier 125 London Wall, London, EC2Y 5AS, UK 525 B Street, Suite 1800, San Diego, CA 92101-4495, USA 225 Wyman Street, Waltham, MA 02451, USA The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, UK Copyright © 2015, 2003 Elsevier Inc. All rights reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions. This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein). Notices Knowledge and best practice in this field are constantly changing. As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary. Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility. To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein. Library of Congress Cataloging-in-Publication Data A catalog record for this book is available from the Library of Congress British Library Cataloguing in Publication Data A catalogue record for this book is available from the British Library ISBN: 978-0-12-385876-4 For information on all Academic Press publications visit our website at http://store.elsevier.com/ Printed in USA Dedication We dedicate this volume to the phycologists and aquatic scientists who have passed away since the publication of our first edition in 2003. They were our teachers, colleagues, and friends—remarkable people who guided and inspired us. They are missed: Kostas Anagnostidis, Tony Bailey-Watts, Hilda Canter-Lund, Kathleen M. Cole, Lebaron C. Colt, Jr., David B. Czarnecki, Thamarapu V. Desikachary, Michael R. Droop, Gordon E. Fogg, John C. Kingston, Paul Kugrens, John W. G. Lund, Francis Magne, Jack L. McLachlan, Richard E. Norris, Murray J. Parsons, Ruth Patrick, Louisa P. Perestenko, Charles W. Reimer, Frank E. Round, Paul C. Silva, Eugene F. Stoermer, Francis R. Trainor, Richard A. Vollenweider, Robert G. Wetzel, and Hugh B.S. Womersley. We hope that their contributions, as well as these pages, will inspire new teachers, new colleagues, and new friends. John D. Wehr, Robert G. Sheath, and J. Patrick Kociolek Contributors Numbers in parenthesis indicate the pages on which the authors’ Richard M. McCourt (429), Academy of Natural Sciences contributions begin. of Drexel University, Philadelphia, Pennsylvania, USA Bryan W. Brooks (873), Department of Environmental Takashi Nakada (265), Institute for Advanced Biosciences, Science, Baylor University, Waco, Texas, USA Keio University, Tsuruoka, Yamagata, Japan, and Susan Carty (773), Department of Biological and Systems Biology Program, Graduate School of Media Environmental Sciences, Heidelberg University, Tiffin, and Governance, Keio University, Fujisawa, Kanagawa, Ohio, USA Japan Brec L. Clay (809), CH Diagnostic & Consulting Service, Kenneth H. Nicholls (537, 587), RR #1, Sunderland, Inc., Berthoud, Colorado, USA Ontario, Canada Thomas Friedl (485), Experimentelle Phykologie Hisayoshi Nozaki (265), Graduate School of Science, und Sammlung von Algenkulturen, Georg-August- University of Tokyo, Bunkyo, Tokyo, Japan Universität Göttingen, Göttingen, Germany Carla K. Oldham-Ott (485), School for Professional Georg Gärtner (315), Institute of Botany, University of Studies, Walsh University, Akron, Ohio, USA Innsbruck, Innsbruck, Austria Donald W. Ott (485), Department of Biology, The John D. Hall (429), University of Maryland, College Park, University of Akron, Akron, Ohio, USA Maryland, USA Hans W. Paerl (873), University of North Carolina at Scott N. Higgins (873), International Institute for Chapel Hill, Morehead City, North Carolina, USA Sustainable Development, Winnipeg, Manitoba, Canada Matthew W. Parrow (773), Department of Biological Jeffrey R. Johansen (75, 135), Department of Biology, Sciences, University of North Carolina at Charlotte, John Carroll University, University Heights, Ohio, Charlotte, North Carolina, USA USA, and Department of Botany, Faculty of Science, J. Patrick Kociolek (653, 709), Department of Ecology and University of South Bohemia, Branišovská 31, 370 05, Evolutionary Biology and Museum of Natural History, České Budějovice, Czech Republic University of Colorado, Boulder, Colorado, USA, and David M. John (375), Life Sciences Department, The University of Michigan Biological Station, Pellston, Natural History Museum, London, United Kingdom Michigan, USA Matthew Julius (653), Department of Biological Sciences, Fabio Rindi (375), Dipartimento di Scienze della Vita e St. Cloud State University, St. Cloud, Minnesota, USA dell'Ambiente, Università Politecnica delle Marche, Ancona, Italy John C. Kingston† (653), Center for Water and the Environment, Natural Resources Research Institute, Nataliya Rybalka (485), Institut für Mikrobiologie und University of Minnesota Duluth, Ely, Minnesota, USA Genetik, Georg-August-Universität Göttingen, Göttingen, Germany, and Experimentelle Phykologie und Sammlung Jiří Komárek (75, 135), Institute of Botany AS CR, von Algenkulturen, Georg-August-Universität Göttingen, Třeboň, and Department of Botany, Faculty of Science, Göttingen, Germany University of South Bohemia, Branišovská 31, 370 05, České Budějovice, Czech Republic Robert G. Sheath (1, 13, 237), Department of Biological Sciences, California State University San Marcos, San R.L. Lowe (709), University of Michigan Biological Marcos, California, USA Station, Pellston, Michigan, USA, and Department of Biological Sciences, Bowling Green State University, Elliot Shubert (315), Faculty of Science and Technology, Bowling Green, Ohio, USA The University of Westminster, London, UK † Deceased. xiii xiv Contributors Peter A. Siver (607), Botany Department, Connecticut Morgan L. Vis (237), Department of Environmental and College, New London, Connecticut, USA Plant Biology, Ohio University, Athens, Ohio, USA John P. Smol (921), Paleoecological Environmental Sue B. Watson (873), Environment Canada, Canadian Assessment and Research Laboratory (PEARL), Centre for Inland Waters, Burlington, Ontario, Department of Biology, Queen’s University, Kingston, Canada Ontario, Canada John D. Wehr (1, 13, 851, 873), Louis Calder Center— S.A. Spaulding (709), United States Geological Survey, Biological Station, Fordham University, Armonk, New University of Colorado, Boulder, Colorado, USA, and York, USA INSTAAR, University of Colorado, Boulder, Colorado, Brian A. Whitton (873), School of Biological and Biomedical USA Sciences, University of Durham, Durham, UK R. Jan Stevenson (921), Department of Zoology, Michigan David M. Williams (653), Life Sciences Department, State University, East Lansing, Michigan, USA Natural History Museum, London, United Kingdom Eugene F. Stoermer† (653), Center for Great Lakes and Aquatic Sciences, University of Michigan, Ann Arbor, Daniel E. Wujek (537), Department of Biology, Central Michigan, USA Michigan University, Mt. Pleasant, Michigan, USA Edward C. Theriot (653), Department of Integrative Bożena Zakryś (459), Department of Plant Systematics and Biology, and Texas Memorial Museum, University of Geography, Faculty of Biology, University of Warsaw, Texas at Austin, Austin, Texas, USA Warsaw, Poland Richard E. Triemer (459), Department of Plant Biology, Michigan State University, East Lansing, Michigan, USA † Deceased. Preface FIRST EDITION The organization of this book includes an introduc- tion to the freshwater algae (with a guide to the taxonomic The study of freshwater algae in North America has a long chapters that follow), an overview of freshwater habitats, and rich history, with some of the early monographic works 20 taxonomic chapters, and finally chapters on the use of dating back to the late 1800s. In recent years, there has been algae in environmental assessments and control of nuisance an enormous and remarkable level of research on this very algae. More than 770 genera are described and illustrated diverse and heterogeneous collection of organisms, making in this book, and each taxonomic chapter includes an intro- any definitive taxonomic or ecological treatise always out duction to the key terms and characteristics of the group, of date. Nonetheless, it is our goal with this book to synthe- ecological distribution, and a guide to the taxonomic lit- size and update much of this vast knowledge and to provide erature to distinguish species within each genus. While we a practical and comprehensive guide to all of the genera of have undoubtedly omitted some less common or yet unre- freshwater algae known from throughout the continent, in corded freshwater genera, this compilation represents an one volume. Chapters also provide guides to other publi- increase in the taxonomic scope and geographic coverage cations and specialized works for the identification and of the freshwater algae of North America. This compares ecological information at the species level. Our intent is to with roughly 490 genera recorded from the United States combine the necessary ecological and taxonomic informa- by Smith (1950), about 335 in Prescott’s (1962) coverage tion in a practical book that can be used by all scientists of the Western Great Lakes region, and nearly 380 genera working in aquatic environments, whether their specialty is from the southeastern United States reported by Whitford in environmental monitoring, ecology, evolution, systemat- and Schumacher (1984). Because not all algal groups are ics, biodiversity, or molecular biology. This is the first book equally well studied, coverage in the present volume varies of its sort covering the entire continent. We also hope that among taxa and chapters. We hope that students, scientists this book will serve to encourage new generations of aquatic working in water management agencies, and experienced biologists to explore freshwater algae carefully, rather than phycologists will use this book thoroughly and provide us regarding phytoplankton or benthic algae as simply quanti- with feedback, such as missing taxa or incomplete geo- ties of chlorophyll or carbon. The enormous variety of algae graphic information. We will endeavor to incorporate this in lakes, rivers, and other aquatic habitats is part of the eco- information into a future edition. logical content of aquatic communities, and their ecosystem functions vary with the species that occur there. SECOND EDITION Many of the previous monographs dealing with a broad geographic region are still useful, such as Smith’s (1950) The second edition of Freshwater Algae of North America Freshwater Algae of the United States, but most are decades occurs at a time of rapid and exciting change in the fields old and do not contain recent taxonomic changes. Our ap- of phycology and aquatic ecology. The development and proach is to include chapters authored by experts who have widespread use of molecular tools in the intervening years specialized in the study of specific groups of freshwater al- have provided remarkable insights into the evolution, clas- gae. Given the great quantity of research that has been pro- sification, and ecology of algae. Genetic data have been duced on all of the major algal taxa, it is no longer possible used to clarify phylogenetic relationships among algal for one or two authors to produce an authoritative book of groups, to discern how marine species may have evolved this kind and one that will span the entire range of taxonomic to colonize freshwater environments, to understand gene and ecological detail that is now known about all the organ- function as cells respond to their environment, and to un- isms termed algae. This volume is modeled closely after cover far greater diversity than was imagined. The chal- the book by Thorp and Covich on freshwater invertebrates lenge for algal taxonomists is this: How do we reconcile (Ecology and Classification of North American Freshwater new genetic data with traditional species concepts based Invertebrates), also published by Academic Press. on morphology and reproduction? Fortunately, some stud- xv xvi Preface ies have found agreements between gene-based and older introduction to these chapters, and Chapter 2, an overview species concepts. Notably, this includes names dating of freshwater algal habitats. We still employ common names back to Linnaeus (Hayden et al., 2003). In other cases, the for the chapters, but also provide current phylogenetic in- discovery of cryptic and, in some cases, endemic species formation. The final two chapters focus on two important not previously recognized using microscopy has both ex- applied topics in algal research; bioassessment methods and panded our knowledge of the freshwater algal flora and harmful algal blooms in fresh waters. Feedback from all us- created challenges for morpho-taxonomic work (Boo et al., ers of this edition is warmly encouraged. 2010; Guiry, 2012; Komárek and Mares, 2012; Mann and We are again exceedingly indebted to the contributors Vanormelingen, 2013). We should also note that through to this volume. Their care and expertise are evident in these these studies a few genera reported in the first edition are no pages. We also offer our sincere thanks to all of the external longer valid and have either been renamed or merged with reviewers who have provided invaluable comments for our other taxa. However, many, perhaps most, genera have yet authors: Robert A. Andersen, António J. Calado, Peter F. to be studied in any detail by molecular methods. M. Coesel, Gertrud Cronberg, Walter K. Dodds, Karolina It has been estimated that more than half of the cyanobac- Fučíková, Thomas Friedl, Jennifer L. Graham, Theodore D. teria species on earth remain to be described by any method Harris, David M. John, Ric W. Jordan, J. Patrick Kociolek, (Nabout et al., 2013) and that only 10% of all diatoms spe- Lothar Krienitz, Jørgen Kristiansen, Brian S. Leander, cies have yet been named (Guiry, 2012). Discoveries of Robert E. Lee, Louise A. Lewis, Eric W. Linton, Rex L. new species and genera will continue. There are some that Lowe, Richard M. McCourt, Kirsten M. Müller, Orlando have been reported from just a few lakes or a single pool, Necchi, Jr., Phil M. Novis, Karin Rengefors, Samuel R. or their true identity has not yet been confirmed. Other taxa Rushforth, Robert G Sheath, Alison R. Sherwood, and Alan are regarded as “uncertain” or “doubtful” and await further D. Steinman. study and molecular analysis. We contend that these are John D. Wehr, Robert G. Sheath, and J. Patrick Kociolek healthy developments for our science. This volume, while still based largely on morpho-species, has nonetheless ex- LITERATURE CITED panded from the first edition in part due to the inclusion of taxa that have been recognized through these new methods. Boo, S.M., Kim, H.S., Shin, W., Boo, G.H., Cho, S.M., Jo, B.Y., Also, several authors have described genera (and species) Kim, J.-H., Kim, J.H., Yang, E.C., Siver, P.A., et al., 2010. Complex that have been observed on other continents, but expected phylogeographic patterns in the freshwater alga Synura provide new to occur in North America, leaving the door open for further insights into ubiquity vs. endemism in microbial eukaryotes. Mol. Ecol. 19, 4328–4338. additions to our flora. Many of new genera are described Guiry, M.D., 2012. How many species of algae are there? J. Phycol. 48, in this volume, some the result of reclassifications, others 1057–1063. from discoveries of taxa not previously observed or known. Hayden, H.S., Blomster, J., Maggs, C.A., Silva, P.C., Stanhope, M.J., We predict that this growth will continue and that further Waaland, J.R., 2003. Linnaeus was right all along: Ulva and links between traditional and molecular approaches will be Enteromorpha are not distinct genera. Eur. J. Phycol. 38, 277–294. created. The present volume now describes 922 genera, an Komárek, J., Mares, J., 2012. An update to modern taxonomy (2011) of increase of more than 150 from the first edition. freshwater planktic heterocytous cyanobacteria. Hydrobiologia 698, On the whole, readers of our first edition have been very 327–351. complimentary and generous in their feedback and advice. Mann, D.G., Vanormelingen, F., 2013. An inordinate fondness? The A student carrying a well-worn book is always a welcome number, distributions, and origins of diatom species. J. Eukaryot. sign. One frequent suggestion was to include color images. Microbiol. 60, 414–420. Nabout, J.C., da Silva, Rocha B., Carneiro, F.M., Sant’Anna, C.L., 2013. This is an understandable request we are pleased to provide, How many species of Cyanobacteria are there? Using a discovery curve given that pigments are important in characterizing differ- to predict the species number. Biodivers. Conserv. 22, 2907–2918. ent algal groups and that these colors highlight the beauty Prescott, G.W., 1962. Algae of the Western Great Lakes Area, second ed. and diversity that encompass the algae. The organization of W.C. Brown, Dubuque, Iowa. this book is similar to that of the first edition, but has been Smith, G.M., 1950. The Fresh-water Algae of the United States, second ed. reorganized in recognition of some of the new classification McGraw-Hill, New York. schemes that have emerged in recent years. The result is Whitford, L.A., Schumacher, G.J., 1984. A Manual of Fresh-Water Algae, 17 taxonomic chapters, preceded by Chapter 1, a general Revised ed. Sparks Press, Raleigh, NC. Chapter 1 Introduction to the Freshwater Algae Robert G. Sheath1 and John D. Wehr2 1Department of Biological Sciences, California State University San Marcos, San Marcos, California, USA. 2Louis Calder Center—Biological Station, Fordham University, Armonk, New York, USA Chapter Contents I. Introduction 1 G. Haptophyte Algae 9 II. Classification 5 H. Synurophyte Algae 9 A. Key to the Taxonomic Chapters in This Book 5 I. Diatoms 9 III. Groups of Freshwater Algae 7 J. Dinoflagellates 9 A. Cyanobacteria 7 K. Cryptomonads 10 B. Red Algae 7 L. Brown Algae 10 C. Green Algae 8 Literature Cited 10 D. Euglenoids 8 E. Eustigmatophyte, Raphidiophyte, and Xanthophyte Algae 8 F. Chrysophycean Algae 8 I INTRODUCTION Freshwater algae are globally ubiquitous and highly diverse, with tens or perhaps hundreds of thousands of species, in a myriad of forms and sizes (Andersen, 1992; Norton et al.; 2004; Mann and Vanormelingen, 2013; Guiry and Guiry, 2014). The algae represent between eight and 12 major evolutionary lineages (Graham et al., 2008; Cock et al., 2010), and all have representatives in inland waters. Current classifications consider most algae to be protists with chloroplasts, but there are also photosynthetic prokaryotes (the cyanobacteria) and a subset of the land plants, the Charales, which have been considered to be algae in previous texts (Patterson, 2014). With new molecular tools being applied to understanding algal taxonomy, systematics, and evolution, our understanding of this diversity is rapidly changing and expanding. Efforts to characterize this biological diversity (such as the Tree of Life Project: Maddison et al., 2007) have contributed to a better understanding of many groups of freshwater algae (e.g., Lane and Archibald, 2008; Entwisle et al., 2009; Hall et al., 2010; Ashworth et al., 2013; Stancheva et al., 2013a; Fučíková et al., 2014). For simplicity, algae are treated in this book in the same sense as they are in recent phycology texts (e.g., Graham et al., 2008; Lee, 2008); that is, they are considered to be a loose (polyphyletic) group of organisms that have all or most of the following characteristics: aquatic, photosynthetic (possessing chlorophyll a), simple vegetative structures without a vascu- lar system, and reproductive bodies that lack a sterile layer of protecting cells. There are important exceptions, however, particularly with regard to their habitat (Chapter 2), colorless relatives (lacking photosynthetic pigments; Chapters 10, 12, and 18), and species that switch between photosynthesis and predation on bacteria (mixotrophy; Chapters 10, 12, and 17). Both prokaryotic (those with cells lacking membrane-bound organelles) and eukaryotic taxa (cells with organelles) are considered in this book. Within the algae, there is an enormous range of vegetative morphologies, including the following: 1. Unicells: Species that occur as solitary cells that may be non-motile or motile, the latter of which move by using one or more flagella or gliding along surfaces via mucilage or other means. A wide variety of forms exist among unicells, in- cluding those contained within a gelatinous sheath (Fig. 1A); cells with intricate shapes, walls, and markings (Figs. 1B and C); cells having flexible cell shapes (Fig. 1D); and cells with two flagella of equal length (Fig. 1E) or flagella with unequal length (Fig. 1F). Cells can be drawn out into hornlike projections (Fig. 1G) or are contained in a hardened case or lorica (Fig. 1H). Freshwater Algae of North America. http://dx.doi.org/10.1016/B978-0-12-385876-4.00001-3 Copyright © 2015 Elsevier Inc. All rights reserved. 1 2 Freshwater Algae of North America 2. Colonies: An aggregation of cells that are held together either in a loose (Fig. 1I and J) or tight well-organized pattern (Figs. 1K-L, 2A-C). Depending on the algal taxon, colonies may contain a variable number of cells, or they may be constant throughout their development (coenobium). Colonies may be composed of flagellated or non-flagellated cells. The basis for cellular connection varies among colonies, including a surrounding gelatinous matrix (Fig. 1I and J), gelatinous stalks (Fig. 1K), or a common parental wall (Fig. 1L). Cells may be arranged in a highly organized pattern (Fig. 2A), directly attached at their cellular edges (Fig. 2B), or at the middle portion of each cell (Fig. 2C). Alternatively, cells may be connected to others by their loricas (Fig. 2E). 3. Pseudofilaments: An aggregation of cells in an end-to-end fashion. The cells are not directly connected to each other; rather, they are spaced apart and may be contained within a common gelatinous matrix or sheath (Figs. 2E and F). A few pseudofilamentous cyanobacteria form macroscopically recognizable crusts on rocks (Fig. 2G). FIGURE 1 Unicellular and colonial forms of freshwater algae. A. Chroococcus giganteus (coccoid cyanobacterium), a unicell to small grouping of cells (regarded as colonial) contained within concentrically layered gelatinous sheaths. B. Micrasterias americana (conjugating green alga, desmid), a unicell with a deep incision (isthmus) that divides two semicells (clear central area is the nucleus), each of which has several deep incisions that may be subdivided into a series of lobes and lobules. C. Didymosphenia geminata (pennate diatom), a large unicell whose walls are constructed from silica, with a central raphe slit, and marked by a series of intricate pores arranged in lines (striae). D. Euglena sp. (photosynthetic euglenoid), a uniflagellate unicell with multiple green chloroplasts, red eyespot, and exterior covering composed of a series of proteinaceous strips (pellicle) that can readily change shape. E. Dunaliella sp. (flagellated green alga) a unicell with two equal flagella. F. Ochromonas sp. (chrysophycean alga), a golden unicellular alga with two apically inserted flagella, one long (tinsel) and one short (smooth). G. Ceratium hirundinella (dinoflagellate), a unicell with a theca composed of cellulose plates with cellular extensions or horns and a transverse flagellum and trailing longitudinal flagellum. H. Lagynion sp. (chrysophycean alga) a golden rhizopodial unicell within a rigid lorica. I. Woronichinia naegeliana (coccoid cyanobacterium), a colony with spherical or ovoid cells arranged at the periphery of a gelatinous matrix. J. Tetraspora lubrica (nonmotile colonial green alga), a sac-like colony of irregularly arranged special cells within a gelatinous matrix. K. Dictyosphaerium granulatum (non-motile colonial green alga), a colony with spherical cells attached together by gelatinous strands. L. Oocystis lacustris (non-motile colonial green alga), a colony with groups of four to eight cells produced inside the walls of parent cells. Scale bars = 25 μm, except E, F, H = 10 μm; B, C, G = 50 μm. (Photos A, D, K, L courtesy of Chris Carter, with permission, photo F courtesy of Peter A. Siver, Chrysophytes LLC, with permission).

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Freshwater Algae of North America: Ecology and Classification, Second Edition is an authoritative and practical treatise on the classification, biodiversity, and ecology of all known genera of freshwater algae from North America. The book provides essential taxonomic and ecological information about
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