Ecology of Protozoa

Brock/Springer Series in Contemporary Bioscience Ecology of Protozoa Brock/Springer Series in Contemporary Bioscience Series Editor: Thomas D. Brock University of Wisconsin-Madison ECOLOGY OF PROTOZOA: The Biology of Free-living Phagotrophic Protists By Tom Fencbel Forthcoming in this series: ROOT-ASSOCIATED NITROGEN-FIXING BACTERIA By johanna Dobereiner Fabio 0. Pedrosa Tom Fenchel Ecology of Protozoa The Biology of Free-living Phagotrophic Protists With 4 7 Figures ' Springer-Verlag Berlin Heidelberg GmbH Prof. Tom Fenchel Department of Ecology and Genetics University of Aarhus DK-8000 Aarhus Denmark Library of Congress Cataloging·in-Publication Data Fenchel, Tom. Ecology of Protozoa. (Brock/Springer series in contemporary bioscience) Bibliography: p. Includes index. 1. Protozoa-Ecology. 1. Title. II. Series QL366.F46 1987 593.1'045 ISBN 978-0-910239-06-6 ISBN 978-3-662-25981-8 (eBook) DOI 10.1007/978-3-662-25981-8 © 1987 by Springer-Verlag Berlin Heidelberg Originally published by Springer-Verlag Berlin Heidelberg New York in 1987 Softcover reprint ofthe hardcover lst edition 1987 AII rights reserved. Neither this book nor any of its contents may be translated or reproduced in any form, including electronic or digital means, without the written permission of the publisher. ISBN 978-0-910239-06-6 Production and editorial supervision: Science Tech Publishers Interior design: Thomas D. Brock Cover design: Katherine M. Brock Media conversion and typesetting: Impressions, Inc., Madison, Wisconsin 10 9 8 7 6 5 4 3 2 1 Preface This book is written for ecologists and protozoologists. Ecologists who study environments and biotic communities in which protozoa are imponant should find this book especially useful. During the last decade it has become clear that protozoa play important roles in natural ecosystems, but few ecologists have a feeling for the functional properties and the diversity of these organisms. Protozoa pose or exemplify many general problems of population and community ecology, and of evolutionary biology. In most respects the general ecological propenies of protozoa are not fundamentally different from those of larger organisms; yet, due to their small size, short generation times, and ubiquitous occurrence they often present ecological phenomena in a new and different light. To this should be added that protozoa are well-suited for experimental work. Despite these advantages, the study of protozoa has played a relatively modest role in the development of ecology and evolutionary biology, primarily, I believe, because most ecologists are unfamiliar with these organisms. I hope this book will attract more attention to these favorable characteristics of protozoa. I also hope that this book may make protozoologists aware of new aspects of their pet organisms. For a long time (that is, until the fundamental distinction between prokaryotic and eukaryotic cells was recognized) protozoa were believed to represent the simplest form of life. They were therefore extensively used for the experimental study of basic questions of cell biology. Protozoa (and not least the ciliate Tetrahymena) are still used in the laboratory as cell models, but prokaryotes and plant and animal tissue cultures have to a large extent taken over this role. Protozoa are eukaryotic cells which are exposed directly to v vi Preface the environment and they are subject to natural selection as individual organisms. Protozoan cells therefore show a variety of specialization and complexity of structure and function which are unchallenged among other types of eukaryotic cells. Cell biology may therefore still harvest much from the study of protozoan cells, not because of their ''primitive'' or "generalized" nature, but because of their specializations, which permit the study of certain features of cells which are somehow amplified in a particular species. However, in order to fully exploit this aspect of protozoa, it is necessary to understand the relationships between the organisms and their environments and the adaptive nature of the studied traits. Throughout this book I emphasize the role of physiological and structural constraints for understanding the role of organisms in nature and the close relationship between cell physiology and ecological insight. This book is divided into twelve chapters. The first one gives a general introduction to the nature of unicellular eukaryotic organisms in general and to protozoa (defined functionally as phagotrophic, unicellular organisms) in particular. The following five chapters are devoted to the functional biology of protozoa: how they move and orient themselves in the environment, their bioenergetics, symbiotic relationships with other organisms, etc. These chapters serve as a necessary background for understanding protozoa in their natural environments. Chapter 7 treats general ecological principles (dynamics of food chains, environmental patchiness, niche diversification and biogeography) with special reference to protozoan populations and communities. Together with the physiological properties of protozoa, the considerations offered in this chapter explain properties of protozoan ecology which are common to all types of ecological systems. The following four chapters discuss protozoan communities belonging to different types of habitats. The treatment emphasizes the role of environmental patchiness in time and space, food resource specialization, and protozoan diversity, as well as the role of protozoa in food chains and in the flow of carbon and other elements in a particular ecosystem. The book is concluded by a chapter which offers some general considerations. I believe that the publication of this book is worthwhile. Although protozoan diversity has recently been monographed (Lee et al., 1985) and many aspects of protozoan physiology and biochemistry have been reviewed by Levandowsky & Hutner ( 1979-81), there is no general treatment of the ecology of protozoa. I have tried to write a book which will be easy to read and which will inspire the readers with new ideas (rather than a reference book or an annotated bibliography). Consequently, I have chosen to discuss some examples in more detail but I have not attempted to be comprehensive. I apologize to colleagues who may feel that their work is inadequately cited, although it may be as Preface vii interesting and illuminating as the examples I do discuss. A recent comprehensive bibliography on the ecology of free-living protozoa is found in Finlay & Ochsenbein-Gattlen ( 1982). I have not treated methodology in any detail, but the reference list should be helpful. The section on protozoa in Bums & Slater (1982) treats methods of collecting, enumerating, culturing, and identifying protozoa and gives additional references. Acknowledgements I am grateful to Dr. Thomas D. Brock who suggested that I write this book; it was something I had wished to do for some time, but clearly I needed an external stimulus. Several of the micrographs (primarily the best ones) have been made by various colleagues to whom I express my gratitude for allowing me to use their micrographs: Dr. Hilda Canter-Lund (Figures 9.1,A; 9.2,A-D; 9.5,A); Dr. Bland J. Finlay (Figures 2.3,C; 9.1,B,C; 9.6); both of the Freshwater Biological Association, Windermere Laboratory, United Kingdom; Dr. Barbara Grimes, Department of Zoology, University of North Carolina, M.Sc., Ringk0bing Raleigh (Figure 5.1); and Helene Munk S~uens, Amtsvandva:sen, Denmark (Figure 8.4,A-K). I am also grateful to Ms. Ilse Duun Jensen and Ms. Annie Jensen for their assistance with photographic work. Above all I am grateful to my friends and colleagues Bland J. Finlay (Windermere Laboratory) and David J. Patterson (Department of Zoology, University of Bristol) for reading the entire manuscript; their comments, critical remarks, and suggestions have, I feel, greatly improved the form and contents of the book. TOM FENCHEL Contents Preface ...................................................................................... v 1 What is a Protozoan? 1.1 1.2 1.3 1.4 1.5 1.6 1 Historical Views on the Nature of Protozoa ... .. ... .. ... .. ... ... ... . 1 The Origin and Diversification of Protists ............................ 3 Unicellularity, Death, and Sex ............................................. 5 The Species Concept in Protozoa ........................................ 7 The Structural Complexity of Protozoa ............................... 9 The Size Range of Protozoa ............................................... 11 2 Ecological Physiology: Motility 15 2.1 Introduction . .. ... .. .. ... ... .. .. ... .. ... .. .. ... ... .. .. .. ... .... .. ... ... ... ... ... . 15 2.2 How Protozoa Move: Life in Syrup .................................... 16 2.3 Orientation in the Environment ........................................ 24 3 Ecological Physiology: Feeding 32 3.1 General Considerations ..................................................... 32 3.2 Feeding in True Protozoa .............................. :................... 41 4 Ecological Physiology: Bioenergetics 4.1 4.2 4.3 4.4 Balanced Growth: The Efficiency of Conversion ................ Balanced Growth: The Rate of Living ................................ Nonbalanced Growth: a Feast and Famine Existence ......... Anaerobic Metabolism ....................................................... ix 53 53 56 59 61 x Contents 5 Ecological Physiology: Other Aspects 63 5.1 Polymorphic Life Cycles ................................................... 63 5. 2 The Adaptive Significance of Sexual Processes ................... 68 5. 3 The Physical and Chemical Environment .......................... 72 6 Symbiosis 76 6.1 The Definition of Symbiosis .............................................. 76 6.2 Associations with Photosynthetic Organisms ..................... 77 6.3 Non photosynthetic Symbionts ........................................... 83 86 7 The Niches of Protozoa 7.1 7.2 7.3 7.4 7.5 Introduction ..................................................................... Steady-State Phagotrophic Food Chains ............................. Patchiness and Successional Patterns ................................. Niche Differentiation and Coexistence .............................. Biogeography of Protozoa ................................................. 8 Protozoan Communities: Marine Habitats 86 87 90 92 97 102 8.1 Introduction .. .. .. ... .. ... .. ... .. ... ... .. ... .. .. ... .. .. .. ... ... .. ... .. .... .. .. . 10 2 8.2 Marine Pelagic Protozoa .................................................. 103 8.3 Marine Sediments ............................................................ 116 9 Protozoan Communities: Freshwater Habitats 9.1 9.2 9. 3 9.4 9.5 Differences from Marine Communities ............................ Pelagic Protozoa ............................................................. Sediments, Detritus, and Solid Surfaces ........................... Running Waters .............................................................. Organic Enrichment and Polluted Waters ........................ 10 Protozoan Communities: Terrestrial Habitats 134 134 136 141 145 149 152 10.1 The Nature of Terrestrial Protozoa ................................ 15 2 10.2 The Role of Protozoa in Soil Ecosystems ....................... 157 11 Symbiotic Protozoa 161 12 Concluding Remarks 167 References 171 Index 195