HARMFULCYANOBACTERIA AQUATIC ECOLOGY SERIES Volume3 The titles published in this series are listed at the end of this volume. HARMFUL CYANOBACTERIA Edited by JEF HUISMAN Institute for Biodiversity and Ecosystem Dynamics,University of Amsterdam, TheNetherlands and HANSC.P. MATTHIJS Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, The Netherlands and PETRAM. VISSER Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, The Netherlands AC.I.P. Catalogue record for this book is available from the Library of Congress. ISBN 1-4020-3009-6 (HB) ISBN 1-4020-3022-3 (e-book) Published by Springer, P.O. Box 17, 3300 AADordrecht, The Netherlands. Sold and distributed in North, Central and South America by Springer, 101 Philip Drive, Norwell, MA02061, U.S.A. In all other countries, sold and distributed by Springer, P.O. Box 322, 3300 AHDordrecht, The Netherlands. Printed on acid-free paper Cover photo: Dense bloom of the cyanobacterium /Microcystis/, Wann See, Germany (photo taken by Gertrud Schlag). springeronline.com All Rights Reserved © 2005 Springer No part of this work may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording or otherwise, without written permission from the Publisher, with the exception of any material supplied specifically for the purpose of being entered and executed on a computer system, for exclusive use by the purchaser of the work. Printed in the Netherlands. To Professor Luuc R. Mur For his leading contributions to European research on harmful cyanobacteria For his guidance of a new generation of aquatic scientists AQUATIC ECOLOGY SERIES Aquatic ecology is an extraordinarily broad and diverse discipline. Aquatic ecology is the study of the functional relationships and productivity of organisms and communities of waters as regulated by their physical, chemical, and biotic environment. The marine environment extends broadly from the complex land-water coastal environments to the open ocean. Limnology encompasses all inland aquatic environments, including streams, rivers, lakes, reservoirs, and wetlands. Research has accelerated in certain areas andbeen less active in others. Reassessments and syntheses are stimulating to the discipline as a whole, aswell as enormously useful to students and researchers in ecological sciences. A series of succinct monographs and specialized evaluations in aquatic ecology has been developed. Subjects covered are topical (e.g., lake hydrodynamics, microbial loop in aquatic ecosystems) rather than broad and superficial. The treatments must be comprehensive and state-of-the-art, whether the topic is at the biochemical, mathematical, population, community, or ecosystem level. The objectives are to advance the topics by the development of arguments, with documented support, that generate new insights, concepts, theories to stimulate thought, ideas, directions, controversies. The books are intended for mature as well as emerging scientists tostimulate intellectualleadership in the topics treated. Receipt of manuscripts approximately 18 months after an agreement is desired, for publication within 10 months thereafter. Electronic submission is essential with hardcopy. Format and manuscript guidance will be provided. For further information and book proposal details please contact: Prof. Robert G. Wetzel, Series Editor Dr. Anna Besse, Publishing Editor Department of Environmental Sciences Aquatic and Biogeosciences and Engineering Springer The University of North Carolina Van Godewijckstraat 30 Chapel Hill, North Carolina 27599-7431 P. O. Box 17 USA 3300 AA Dordrecht Email: [email protected] The Netherlands Phone: 919 + 843-4916 Email: [email protected] Phone: 31 (0) 651 33 86 01 CONTENTS PREFACE ix CONTRIBUTORS xi 1. HARMFULCYANOBACTERIA 1 From mass mortalities to management measures G.A. Codd, J. Lindsay, F.M. Young, L.F. Morrison & J.S. Metcalf 2. MOLECULAR BIOLOGYOFCYANOBACTERIAL TOXINS 25 Genetic basis of microcystin production T. Börner & E. Dittmann 3. DYNAMICS OF CYANOBACTERIAL TOXINS 41 Sources of variability in microcystin concentrations W.E.A. Kardinaal & P.M. Visser 4. NUTRIENT LIMITATIONOF FRESHWATERCYANOBACTERIA 65 Tools to monitor phosphorus limitation at the individual level M. Dignum, H.C.P. Matthijs, R..Pel, H.J. Laanbroek & L.R.. Mur 5. NUTRIENT LIMITATION OF MARINE CYANOBACTERIA 87 Molecular ecology of nitrogen limitation in an oligotrophic sea A.F. Post 6. THE ECOPHYSIOLOGYOF THE HARMFUL 109 CYANOBACTERIUMMICROCYSTIS Features explaining its success and measures for its control P.M. Visser, B.W. Ibelings, L.R. Mur & A.E. Walsby 7. POPULATION DYNAMICSOF HARMFULCYANOBACTERIA 143 Factors affecting species composition J. Huisman & F.D. Hulot 8.OPTICAL DETECTIONOFCYANOBACTERIAL BLOOMS 177 Shipboard observation and remote sensing H.J. Gons, H. Hakvoort, S.W.M. Peters & S.G.H. Simis 9. WATER SAFETY PLANS 201 A better approach to prevent human exposure to harmful cyanobacteria I. Chorus INDEX 229 PREFACE Innocently, the white dog looks up: ‘What ‘s all that fuss about? Why am I called back ashore, when I ‘m having so much fun in this green soup?’ Indeed, it is a wise decision of the owner to call this dog backk ashore without delay. The green soup the dog is standing in is a dense surface bloom of Microcystis. The cyanobacterium Microcystis is a cosmopolitan species of freshwater lakes. It can produce microcystins, a toxic substance that has caused numerous illnesses and deaths of dogs, cattle, birds, and even humans. Are all cyanobacteria harmful? No, not at all. Cyanobacteria are phototrophic microorganisms that convert sunlight into organic biomass by means of photosynthesis. As such, cyanobacteria are the aquatic equivalents of grasses and trees on land. In fact, cyanobacteria were the first organisms in the evolutionary history of our planet to produce oxygen. They are the evolutionary ancestors of all modern plants. Together with the eukaryotic phytoplankton, cyanobacteria form the basis of the aquatic food web. However, a few cyanobacterial species are capable of producing powerful toxins. Several of these harmful species are quite widespread. They occur throughout the world, especially in fresh and brackish waters, and may occasionally reach high population densities, as the cover of this book illustrates. Waters dominated by such harmful cyanobacteria are often closed for recreation, and cannot be used for the intake of drinking water or agricultural purposes. During the past few years, much new knowledge on harmful cyanobacteria has been acquired, owing to scientific advances in molecular biology, genomics, and the computational sciences and also owing to an increased recognition of the problems caused by harmful cyanobacteria. In fact, it is fair to say that we now know a lot more about harmful cyanobacteria than only five years ago. The aim of thisbook, therefore, is to provide an up-to-date review that makes this recently acquired knowledge accessible to a broad readership. The first chapter (chapter 1) in this book introduces the subject, and explains the problems associated with harmful cyanobacteria. Two subsequent chapters (chapters 2 and 3) focus on the molecular biology and physiology of toxin production, with emphasis on the genetic regulation and variability in toxin production. Next, modern approaches are discussed that allow rapid assessment of the extent to which nutrients, such as nitrogen and phosphorus, limit the growth of cyanobacteria (chapters 4 and 5). The subsequent chapter (chapter 6) reviews our current knowledge of the physiology and ecology of Microcystis, one of the most widespread and extensively studied harmful species. This is followed by a state-of- the-art review of the population dynamics of harmful cyanobacteria, with particular attention to environmental factors that favour cyanobacteria over other phytoplankton species (chapter 7). Chapter 8 introduces novel techniques in remote sensing, which allow monitoring of the development of cyanobacterial blooms from aircraft and satellites. The final chapter (chapter 9) discusses how improvements in water management, based on the new Water Safety Plans introduced by the World Health Organization, may reduce human exposure to harmful cyanobacteria. ix x PREFACE The idea for this book came up during a farewell symposium, organized at the University of Amsterdam in September 2003, on the occasion of the retirement of Professor Luuc Mur. For more than 40 years, Luuc Mur has been active in phytoplankton biology, first as lecturer and later as Professor in Aquatic Environmental Biology at the University of Amsterdam. He has educated numerous undergraduate and graduate students on water management, the marvellous beauty of the phytoplankton, and the potential trouble of harmful cyanobacteria. Many of these former students are still very active in aquatic research and water management today. During the 1970s and 1980s, Luuc Mur was among the first scientists to recognize that advances in microbiology could be made useful in aquatic ecology. In particular, phytoplankton species such as the cyanobacteria and green algae could be studied in the laboratory using continuous-culture techniques. This culture technique enabled detailed investigation of the growth kinetics of these microorganisms under controlled laboratory conditions. In the 1980s and 1990s, with the increasing eutrophication of many European lakes, the problems caused by harmful cyanobacteria became widely apparent. With funding provided by the fourth framework program of the European Committee, Luuc Mur initiated two research projects (CYANOTOX and TOPIC) to study the toxicology, molecular biology, physiology, and ecology of harmful cyanobacteria. These two research projects brought together a diverse group of European scientists that have stood at the basis of much of what is currently known about harmful cyanobacteria. It is our pleasure - on behalf of all colleagues, students and friends - to thank Luuc Mur for his leading contributions and guidance of a new generation of aquatic scientists. This book would not have been possible without the financial support provided by the Earth and Life Sciences Foundation (ALW), the Netherlands Organization for Scientific Research (NWO), and the University of Amsterdam. Special thanks go to all chapter authors, whose work provides the backbone of this book, and to all reviewers that have been of great help in sharpening the chapters. We thank Bibi Krot and Pascale Thiery for helping us in organizing the symposium, and for their invaluable assistance during the development of this book. We thank Gertrud Schlag for providing the beautiful photograph that illustrates the cover, and Ellen Spanjaard for the cover design. Last but not least, we are most grateful to Professor Robert Wetzel and the staff at Springer, especially Anna Besse- Lototskaya and Judith Terpos, for their stimulating guidance. Jef Huisman, Hans C.P. Matthijs & Petra M. Visser (editors) Amsterdam, August 2004.
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