Ecology of Soil - 00 Prelims 31/7/03 10:58 Page i THE ECOLOGY OF SOIL DECOMPOSITION Ecology of Soil - 00 Prelims 31/7/03 10:58 Page ii This book is dedicated to James D. Berger Tom Cavalier-Smith David C. Coleman Max (F.J.R.) Taylor Ecology of Soil - 00 Prelims 31/7/03 10:58 Page iii The Ecology of Soil Decomposition Sina M. Adl Department of Biology Dalhousie University Halifax, Nova Scotia Canada CABI Publishing Ecology of Soil - 00 Prelims 31/7/03 10:58 Page iv CABI Publishing is a division of CAB International CABI Publishing CABI Publishing CAB International 44 Brattle Street Wallingford 4th Floor Oxon OX10 8DE Cambridge, MA 02138 UK USA Tel: +44 (0)1491 832111 Tel: +1 617 395 4056 Fax: +44 (0)1491 833508 Fax: +1 617 354 6875 E-mail: [email protected] E-mail: [email protected] Website: www.cabi-publishing.org © CAB International 2003. All rights reserved. No part of this publication may be reproduced in any form or by any means, electronically, mechanically, by photocopying, recording or otherwise, without the prior permission of the copy- right owners. A catalogue record for this book is available from the British Library, London, UK. Library of Congress Cataloging-in-Publication Data Adl, Sina M., 1964– The ecology of soil decomposition / Sina M. Adl. p. cm. Includes bibliographical references and index. ISBN 0-85199-661-2 (alk. paper) 1. Soil microbiology. 2. Soil ecology. I. Title. QR111.A34 2003 577.5Ј7--dc21 2003001601 ISBN 0 85199 661 2 Typeset in 10pt Baskerville by Columns Design Ltd, Reading. Printed and bound in the UK by Cromwell Press, Trowbridge. Ecology of Soil - 00 Prelims 31/7/03 10:58 Page v Contents Preface ix Acknowledgements xiii 1 The Saprotrophs 1 Eukaryotic Cells 2 Protists 8 Protozoa 9 Retortomonadea and Trepomonadea (phylum Metamonada) 9 Oxymonadea (phylum Metamonada) 10 Trichomonadea and Hypermastigea (phylum Trichozoa) 11 Percolozoa (phylum Percolozoa) 13 Euglenids (phylum Euglenozoa: Euglenoidea) 14 Bodonids (phylum Euglenozoa: Kinetoplastea) 16 Amoebae (phylum Amoebozoa) 17 Cercozoa and Neomonada 26 Ciliates (phylum Ciliophora) 30 Chromista 32 Bicoecea, Labyrinthulea (phylum Sagenista) 33 Oomycetes and Hyphochytrea (phylum Bigyra: pseudo-fungi) 33 Fungi 34 Chytrids (phylum Archemycota: Chytridiomycetes, Enteromycetes, Allomycetes) 38 Zygomycetes (phylum Archemycota: Zygomycetes and Zoomycetes) 41 Glomales (phylum Archemycota: Glomomycetes and Bolomycetes) 42 Ascomycetes (phylum Ascomycota) 44 Basidiomycetes (phylum Basidiomycota) 44 v Ecology of Soil - 00 Prelims 31/7/03 10:58 Page vi vi Contents Invertebrates 45 Nematodes (phylum Nemathelminthes: Nematoda) 46 Rotifers (phylum Acanthognatha: Rotifera) 51 Gastrotrichs (phylum Acanthognatha: Monokonta: Gastrotricha) 52 Tardigrades (phylum Lobopoda: Onychophora and Tardigrada) 53 Earthworms (phylum Annelida: Clitellata: Oligochaeta) 56 Microarthropods (phylum Arthropoda: Chelicerata, Myriapoda, Insecta) 60 The Bacteria (Prokaryote: Bacteria and Archea) 66 Roots, Fine Roots and Root Hair Cells 75 Summary 77 Suggested Further Reading 78 2 The Habitat 79 ‘Through a Ped, Darkly’ 79 The soil habitat 81 Soil Mineral Composition 81 Ped structure 84 Soil Air 86 Water Content 87 Natural loss of water 90 Soil temperature 92 Soil Organic Matter 93 Soil horizons 95 Soil nutrient composition 97 Dynamics of Soil Physical Structure 101 Summary 101 Suggested Further Reading 102 3 Sampling and Enumeration 103 Soil Collection 103 Soil handling 105 Soil storage 106 Site Variation and Statistical Patterns 107 Spatial distribution patterns 108 Pedon sampling and enumeration 109 Experimental design and field sampling 112 Extraction and Enumeration 114 Total potential species diversity 115 Active species at time of sampling 127 Number of Species in Functional Groups 134 Summary 135 Suggested Further Reading 135 Ecology of Soil - 00 Prelims 14/8/03 16:38 Page vii Contents vii 4 Reconstructing the Soil Food Web 137 Functional Categories 137 Primary Decomposition 139 Plant senescence and necrosis 141 Physical degradation of tissues 142 Macrofauna invertebrates 142 Litter mass loss rates 146 Litter chemistry and decomposition 148 Mesofauna diversity and climate effect on initial litter decomposition 149 Secondary Decomposition 152 Primary Saprotrophs 153 Saprotrophic bacteria 153 Saprotrophic fungi 158 Osmotrophy 162 Secondary Saprotrophs 164 Bacteriotrophy 165 Cytotrophy 171 Fungivory 175 Detritivory 180 Other Consumers 180 Nematotrophy 181 Predatory microinvertebrates 184 Earthworms 185 Omnivory 187 Symbionts 188 Symbiosis with animals 188 Symbiosis with plant roots 190 Opportunistic Parasites and Parasitism 197 Summary 199 Suggested Further Reading 200 5 Spatial and Temporal Patterns 201 Regulation of Growth 202 Prokaryotes 202 Protists 206 Invertebrates 209 Periods of Activity 211 Osmoregulation 212 Growth response dynamics 215 Why so many species? 218 Patterns in Time and Space 221 Primary Saprotrophs 223 Spatial organization in bacteria 223 Organization of fungal species 231 Ecology of Soil - 00 Prelims 31/7/03 10:58 Page viii viii Contents Secondary Saprotrophs and Other Consumers 240 Patterns in soil protozoa 240 Patterns in nematodes 243 Patterns in the distribution of soil mites 251 Collembola patterns in soil 258 Other insects 261 Earthworm distribution in soil 262 Synthesis and Conclusions 266 Summary 268 Suggested Further Reading 269 6 Integrating the Food Web 270 Global Impact of Decomposition 271 Carbon 271 Phosphorus 273 Nitrogen 275 How to Trace Nutrients 281 Tracer studies 284 Soil Food Web Models 287 Regulation of population growth 287 Regulation of nutrient flux rates 288 Effect of food web structure on decomposition 290 Summary 293 Suggested Further Reading 294 References 295 Index 327 Ecology of Soil - 00 Prelims 31/7/03 10:58 Page ix Preface This book is about the trophic interactions among species that live in the soil. These interactions are responsible for the decomposition of previ- ously living cells and tissues, for pedogenesis (from a biological perspec- tive, it is the accumulation of organic matter into the mineral soil) and for biomineralization (making the decomposing matter available as nutrients in the soil solution). The biological interactions between species that carry out the decomposition of organic matter are our primary focus. In this endeavour, we must consider the ecology of species that live in the soil habitat. The ecology of these species must take into account both the biological interactions among edaphic species and the abiotic environmental parameters which affect species composition and activity patterns. Over time, changes in the soil profile due to transformations of the organic matter affect species composition. In turn, changes in species composition affect the chemistry of new litter and decomposing organic matter. These changes are reflected in the spatial heterogeneity of the soil and in succession patterns over longer time scales. The organisms that are mostly responsible for decomposition include saprotrophic bacteria and fungi, soil protozoan species, symbi- otic protozoa in saprotrophic invertebrates, fungi in symbiosis with plant roots, Oomycetes and many specialized invertebrates (such as nema- todes, rotifers, mites, Collembola, earthworms and enchytraeids). These species are mostly microscopic, with the notable exception of earth- worms and several less abundant invertebrate groups. In this respect, the study of decomposition in the soil habitat is also the study of soil microbial ecology in its true sense, i.e. the soil ecology of all those organ- isms too small to see without magnification, the microbes. Here, I recognize that phylogenetically related species are biochemi- cally more similar to each other. This is an important consideration ix Ecology of Soil - 00 Prelims 31/7/03 10:58 Page x x Preface when comparing metabolism, regulation of behaviour and general biol- ogy of the organisms. However, from an ecological perspective, the func- tions of species in the habitat are more related in terms of what they feed on, and their spatial and abiotic preferences. One must distinguish between categories that group species according to evolutionary related- ness (systematics) and categories that group species according to ecologi- cally relevant functional groups. It is clear that taxonomic groups implicated in decomposition each contain species that belong to differ- ent functional categories. This distinction must be carried through into schematic representations of food webs and ecosystem function. Moreover, it is the amount of organic matter flux between these func- tional categories that is more significant than the actual amount of bio- mass in each category. Many aspects of the interactions between species within functional groups, and of nutrient flux rates between functional groups, are poorly quantified. In the chapters that follow, I try to pro- vide a description of the biology of taxonomic groups, and a structure for organizing these species into functional groups. From here, we must try to complete our investigation of decomposition by quantifying neglected interactions and including neglected taxa. There lies before us an exciting period for exploration and discovery, of the dark and cryptic reticulate matrix where decomposition completes the recycling of nutrients. The recycling of nutrients through decomposition is one side of the coin in ecology, with autotrophic primary production being the other. Photosynthesis-driven primary production drives much of the ocean surface and above-ground ecology.