Fungi in Ecosystem Processes John Dighton Institute of Marine and Coastal Sciences Cook College and Rutgers Pinelands Field Station New Lisbon, New Jersey, U.S.A. MARCEL MARCEL DEKKER, INC. NEW YORK • BASEL Library of Congress Cataloging-in-Publication Data A catalog record for this book is available from the Library of Congress. ISBN: 0-8247-4244-3 This book is printed on acid-free paper. Headquarters Marcel Dekker, Inc. 270 Madison Avenue, New York, NY 10016 tel: 212-696-9000; fax: 212-685-4540 Eastern Hemisphere Distribution Marcel Dekker AG Hutgasse 4, Postfach 812, CH-4001 Basel, Switzerland tel: 41-61-260-6300; fax: 41-61-260-6333 World Wide Web http://www.dekker.com The publisher offers discounts on this book when ordered in bulk quantities. For more information, write to Special Sales/Professional Marketing at the headquarters address above. Copyright q 2003 by Marcel Dekker, Inc. All Rights Reserved. Neither this book nor any part may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, microfilming, and recording, or by any information storage and retrieval system, without permission in writing from the publisher. Current printing (last digit): 10987654321 PRINTED IN THE UNITED STATES OF AMERICA MYCOLOGY SERIES Editor J. W. Bennett Professor Department of Cell and Molecular Biology Tulane University New Orleans, Louisiana Founding Editor Paul A. Lemke 1 Viruses and Plasmids in Fungi, edited by Paul A. Lemke 2 The Fungal Community Its Organization and Role in the Ecosys- tem, edited by Donald T Wicklow and George C Carroll 3. Fungi Pathogenic for Humans and Animals (in three parts), edited by Dexter H Howard 4 Fungal Differentiation A Contemporary Synthesis, edited by John E. Smith 5 Secondary Metabolism and Differentiation in Fungi, edited by Joan W Bennett and Alex Ciegler 6 Fungal Protoplasts, edited by John F Peberdy and Lajos Ferenczy 7 Viruses of Fungi and Simple Eukaryotes, edited by Yigal Koltm and Michael J Leibowitz 8 Molecular Industrial Mycology: Systems and Applications for Fila- mentous Fungi, edited by Sally A Leong and Randy M Berka 9 The Fungal Community Its Organization and Role in the Eco- system, Second Edition, edited by George C. Carroll and Donald T Wicklow 10 Stress Tolerance of Fungi, edited by D H Jennings 11 Metal Ions in Fungi, edited by Gunther Wmkelmann and Dennis R Wmge 12 Anaerobic Fungi Biology, Ecology, and Function, edited by Douglas O Mountfort and Colin G Orpin 13 Fungal Genetics Principles and Practice, edited by Cees J Bos 14 Fungal Pathogenesis. Principles and Clinical Applications, edited by Richard A Calderone and Ronald L Cihlar 15 Molecular Biology of Fungal Development, edited by Heinz D Osie- wacz 16 Pathogenic Fungi in Humans and Animals: Second Edition, edited by Dexter H. Howard 17 Fungi in Ecosystem Processes, John Dighton 18 Genomics of Plants and Fungi, edited by Rolf A Prade and Hans J. Bohnert Additional Volumes in Preparation Clavicipitalean Fungi: Evolutionary Biology, Chemistry, Biocontrol, and Cultural Impacts, edited by James F. White, Jr, Charles W. Bacon, Nigel L Hywel-Jones, and Joseph W. Spatafora Preface Why did I decide to write this book? As an undergraduate student I could not make up my mind whether I wanted to be a zoologist or a botanist, so I decided to adopt ecology, in its broadest sense, as my area of interest. This led me to think about interactions among organisms and to try to look at ecosystems from a holistic, rather than from an autecological, point of view. As someone with little formal training in mycology, my interest in fungi started during my doctoral research, especially when attending university-wide lectures by C. T. Ingold, given at the University of London. My former job, at the then Institute of Terrestrial Ecology at Merlewood, UK, brought me into contact with the work on ectomycorrhizae, decomposition, and nutrient cycling in temperate and subtropical forest ecosystems. During this time, I had many fruitful discussions with fungal ecologists in both the British Mycological Society and the international world of mycorrhizal researchers. In particular, I remember animated discussions with Alan Rayner, who is a font of knowledge, inspiration, and encouragement. As a result of this history, I have been fascinated by the multifarious ways in which fungi interact with other organisms and function in moderating the processes occurring in ecosystems. With my move to Rutgers University, I initially taught my first graduate course, Fungi in Ecosystems, during my first semester, while all my books and notes were on a ship crossing the Atlantic. The continued development of this course has been the impetus for this book. As I could find no textbook for my students that really approached the subject of mycology from an ecosystem point of view, I decided to put my ideas on the importance of fungi in ecosystem processes into a volume that could be used by upper-level students and iii iv Preface researchers. This course and its variants have been the main thrust of my teaching at Rutgers. This has not been a sole venture as, along with my interactions with Jim White and Peter Oudemans, we are gradually building a strong and interactive series of mycology courses in our university. In this book I have started with the list of functions that Alan Rayner suggests that fungi perform in ecosystems (introduction to the second edition of The Fungal Community: Its Structure and Function, edited by George C. Carroll and Donald T. Wicklow, (Marcel Dekker, 1992)). I have attempted to elaborate on these functional roles of fungi and tried to show how the world would function less satisfactorily in the absence of fungi. Given the vast range of fungal literature I have not been able to do much more than scratch the surface of the subject. However, I hope that the more than 1300 references that I have cited will act as a means for interested readers to delve further into the literature on any specific subject area. For the upper-level students and researchers to whom this book is targeted, I hope that it will stimulate thoughts beyond the narrow confines of their immediate research questions and allow them to place their work in the wider context of the functioning of ecosystems. I believe that it is only by the greater understanding of the linkages between organisms and the processes they control in the ecosystem that we can appreciate the beauty of the living world around us, appreciate the impacts that we are having on ecosystems, and obtain the understanding of the function of component organisms that will allow us to protect and preserve nature. In attempting to summarize the vast literature, I have written the text in my own words, but have relied heavily on previously published literature for figures and tables to support my commentary. Most tables have been reconstructed and almost all figures have been redrawn from their original in an effort to simplify the information presented in the originals. For the statistical purist, I hope that my removal of error bars and indications of significant differences will be forgiven for the sake of simplicity of presentation. In the main, the data shown in figures represent statistically significant interactions. Although the figures and tables represent the key message I wish to convey, they are no substitute for the original data and publications. I encourage the interested reader to explore further by consulting the original publications to obtain more information that I can impart in this book. I dedicate this book to my uncle, Wally Champkin, whose enthusiasm for natural history fueled my interest in ecology. As a child I was constantly amazed that he could put a name to most of the plants, insects, and birds we saw on our walks. I could watch for hours his cine films and stills of birds, flowers, moths, and butterflies. I owe a debt of gratitude to my parents, who encouraged and supported me in my studies and allowed me to pursue my own interests in biology. I especially thank my wife, Joan, and daughter, Gail, who have supported my career, moved with me to the United States, and encouraged me in Preface v the writing of this book. I could not have completed this task without them. Finally, I wish to thank Bob Evans, who commented on the first drafts of my work here, and to the students and colleagues in my research group, who have both given me encouragement and tolerated my absences during the creation of this book. John Dighton Contents Preface iii 1. Introduction 1 1.1 Why Fungi? 1 1.2 What Are Ecosystems and Ecosystem Functions? 3 1.3 What Are Fungi? 8 1.4 Specific Ecosystem Services Carried Out by Fungi 15 1.5 Concluding Remarks 18 References 20 2. Fungi and Primary Productivity: Making Nutrients Available 27 2.1 Soils and Nutrient Availability 27 2.2 Nutrient Availability in Aquatic and Marine Ecosystems 69 2.3 Concluding Remarks 81 References 83 3. Fungi and Primary Productivity: Plant Growth and Carbon Fixation 93 3.1 The Role of Lichens in Primary Production 94 3.2 The Role of Mycorrhizae in Plant Primary Production 99 3.3 The Role of Fungal Pathogens in Plant Primary Production 154 vii viii Contents 3.4 Interactions Among Mycorrhizae and Plant Pathogens 157 3.5 Synopsis and Outlook 162 References 163 4. Fungi, Secondary Productivity, and Other Fungal–Faunal Interactions 185 4.1 Fungi as Food for Secondary Producers: Positive Impacts on Faunal Productivity 186 4.2 Effects of Grazing on Fungi and Fungal-Mediated Processes: Negative and Positive Feedbacks 197 4.3 Specific Fungal–Faunal Interactions 217 4.4 Fungi as Animal Pathogens: Negative Impacts on Faunal Productivity 221 4.5 Fungal–Faunal Interactions in Aquatic and Marine Ecosystems 226 4.6 Summary and Conclusions 229 References 232 5.