E.-D. Schulze · H. A. Mooney (Eds.

Biodiversity
and Ecosystem
Function
Professor Dr. Ernst-Detlef Schulze
Lehrstuhl fur Pflanz.enokologie
Universitat Bayreuth
Postfacl1 1021 51.
D -95440 Bayreuth, Germany

Professor Dr. H arold A. Mooney

Department. of Biological Sciences
Stanford University
Stanford CA 94305, USA

ISBN 3-540-58103-0 Springer-Verlag Berlin Heidelberg New York

Title of the original edition (hardcover)

Ecological StllClies. Volume 99
ISBN 3-540-55804-7 Springer~Verlag Berlin Heidelberg N~·w Yrrrk
ISBN 0-387-55804-7 Springcr-Verla.g New York .Berlin Heid.c lberg

Ubrary of Congress Cataloglng-io-Publication Data

Biodiversity and ecozystent function I Ernst·D<tlef Sc.hulze, H<Irold A. Mooney (eds.).
p. em. - (Bcologic31 studies; v. 99)
'"Sprioger study edic.ion~
Includes bibliographical references and indexes.
ISBN 3-540-58103-0 (soft cover). - ISBN 0.387-58103-0
I. Biologlcal diversity. 2. Biotic communities. 3. Biological diversity conservation. I. Schulze, B.-D.
(E.rnst-Detlef), 1941- n. Mooney, Harold A. ID. Series.
QH3l3.B54 t994 574.5 - dc20 94- t2948 CIP
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Contents

Section A: Ecosystem Function

1 Biological Diversity and Terrestrial Ecosystem

Biogeochemistry
P. M. Vitousek and D. U. Hooper .......... . ...... . 3
1.1 Introduction .................................... . 3
1.2 Sema.ntics ........................... .. ......... . 4
1.3 Biological Diversity and Biogeochemistry .......... . 5
1.3.1 Ex erirnental Tests . .. . . .... . . . .. . .. . ..... .. . . .. . . 6
1.3.2 Biogeographic Patterns .......................... . 9
1.4 Other Potential Effects of P lant Diversity on
Bio eochemist . . . . .... .. .... . ... . ... . ... . ..... . 10
1.5 Conclusions .................................... . 1I
References ..................................... . 12
2 Biodiversity and Ecosystem Function in Agricultural
Systems
M. J. Swift and J. M. Anderson ................... . 15
2.1 Introduction .................................... . 15
2.2 Characteristics of Agricultural Ecosystems ......... . 16
2.2.1 Diversity and Complexity ........................ . 16
2.2.2 Classification in Relation to Diversity and Complexity 19
2.2.3 Sustainability ................................... . 21
2.3
Cro in S ems ... . . .... ... ... .... . . . . .. ...... . 22
2.4 Biodiversity and the Function of the Decomposer
Subsystem ..................................... . 25
2.4.1 Biodiversity in Relation to Function ............... . 25
2.4.2 Decomposer Diversity and Function in Agricultural
Systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28
2.4.3 Inte.ractions Between P.lants_and the Soil Biota .... . . 30
2.5 Biodiversity and the Function of the Herbivore
Subsystem ...... . .............................. . 32
2.6 Conclusions ................. .... ............... . 33
2.6.1 A Hypothesis of the Importance of Plant Diversity in
Ecosystem Regulation ........................... . 33
XIV Comcnts

2.6.2 T he Importance of Increasing Plant Species Number 36

2.6.3 The Importance of Plant Species Composition . . . . . . . 37
2.6 .4 Assessment o f Long-Term Trends . . . . . . . . . . . . . . . . . . . 38
References . . . . . . . . . . . . . . . . . . . . . . . . . ... . . ' • t 38

3 Biodiversity and Interactions W ithin Pelagic Nutrient

Cycling an d P roductivity
C. E. W. Steinberg and W. G eller . . . .. . ... .. .. . .... . 43
3.1 Introduction: Explanations to the Paradox of the
Plankton . ... . . .. . .. . . ...... . . . . .. . . .. . . . . ... .. . . 43
3.2 Further D eterminan ts of Biodiversity ... .. ... . . . .. . . 44
3.2.1 P lasticit a nd Cell Sha e .... . ... . ..... . . .. . . ... . . 44
3.2.2 Thrbulence . . . .... . .. . .. . . .. . ..... .. . . . . ... . .. . . . 45
3,3 Selection a nd Succession ...... . . . . . ... . .. . .. . .... . 46
3.3.1 Descr iptive M odel of Plankton Succession . .. . .... . . 47
3.4 M icrobial Loop: Structure and Function . .... . .. . . . . 50
3.4. 1 Stn1cture .............. . . . . . . ...... . ... . .. . . . .. . . so
3.5 Structural Diversi Indices . .. . ... . .. . ...... . . . .. . . 55
3.6 Ataxonomic A pproach to Assess Ecosystem Stability . 57
3.7 ConcJusions .................... .. .............. . 60
References . . . ....... . .. . ... . ... .... . .. . .. ... .. . . 61

Section 8: Functional Groups

4 Functional Groups of Microorganisms

0. Meyer ......................... . ........ . ... . 67
4.1 Introduction .................................... . 67
4.2 Free-Ljving Components of the Soil Microbiota . . . . . 68
4.3 M etabolic Txpes of Bacteria .. . ...... . ..... .. .... . . 71
4.4 T he Role of Microorganisms in the Decomposition of
.Org_anic Material . .. . . . . . .. .. . ... . . . .. .. .... . . . .. . 73
4.4. 75
..
4.4.2 L 1 run . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 76
4.4.3 Proteins, P~tides, and ~no_Acids . . ... . ... . .. . . . 77
4A.4 Pectin . .. . . .. . . . .. . . . . . .. . . . .. .. . . . . •.. . . . . . . . .. 78
4.5 The Role of Microorganisms in the Biogeochemical
C cle of N itro en ... . . . . . . . . . .. . . .. . . . .. ...... . . . 79
4.5.1 . 'fi catiOn
N 1tn . ...•. ... . . ... . . • . . .... .. .. . . ...... • . . . 19
4.5.2 . 'fi .
n emt n catJOD . ... . .. . .. . ... . . .. . . . . .. .. . . . . ... . . 82
4.5.3 N Fixation .. . ...... . ...... . ...... . .... .. . .... . . 84
4.6 The Role of Microorganisms in the Biogeochemical
C cle of Sulfur .... . . . ...... . .. .... .. .. ..... ... . . 86
4.6. 1 The Oxidation of Reduced Sulfur Compounds . .. .. . . 86
4.6.2 Oesnlfurication ...... . . . .... . .... . .... . . ... . . ... . 88
Contents XV

~4~.1---C~anwc~lwllwun~s-----------------
·-··-·-·-·-
·-··-·-·-·-
·-··-·-·-·-·--~90
References ... .. ............................. 93

5 Plant Iraits and Adaptive Strategies: Their Role in

Ecosystem Function
0 . T. Solbri ........ . ......... ............. .. ... . 97
5.1 Introduction . . ... .. .. ..... .. . ..... . ...... . . ..... . 97
5.2 Schemes to Classify Plants on the Basis
of Their Ecolo ·cal Traits . .. ...... .. . ...... . ..... . 97
5.2.1 Single-Character Functional Classification
of Vascular Plants .............................. . 99
5.2.2 Attempts to Classify Species Based on T heir Overall
101
5.3 101
5.3. I Optimization ................................... . 103
5.3.2 Plant Adaptive Strategies ........................ . 103
5.3.3 Why Optimality Criteria Are Not Always Sufficient .. 106
5.4 Definition of Ecosy.§tem Functional P ro erties . . .. . . . 108
5.5 The Meaning of Adaptive Strategy in a Complex,
Nonlinear World . .... . . . ....... .. .. . .... ... ..... . 108
5.6 Conclusions: The Importance of Diversity
in a Noneguilibrium Situation . ...... . .. .. .. . ..... . 11 0
References ..................................... . III

6 Scaling from Species to Vegetation: The Usefulness of

Functional Groups
Ch. Korner . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I I7
6. I Introduction: What Are Functional Groups
and W hy Use Them? ............................ . ll7
6.2 Selecting Functional Groups ...................... . 118
6.3 Narrow or Wide Grouping: The Dilemma of
Experimental Safety and Ecological Applicability 120
6.4 Grouping of P lant Species with Respect to Their
Structural, Physiological, and Life Strategy
Characteristics .................... . ............. . 121
6.4. I Life-Forms and Structures: The Morphotype ....... . 121
6.4.2 Dry Matter Partitioning: Investment 'JYpe .......... . 122
6.4.3 T he Physiotype ................................. . 123
6.4.4 T he Physiomorphotype .......................... . 124
6.4.5 Life Strategies .................................. . 12$
6.5 T he Spatial Definition o f Functional Groups within
Plant Communities .............................. . 127
6.6 Ecosystems: The Largest Functional Group ......... . 130
6.7 lntegration of Contrasting Levels of Complexity:
A Compromise ................................. . 131
XVI Contents

6.8 A Promising Tool: Using FunctionaJ Groups in

Controlled Ecosystems . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13 3
6.9 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 136
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 137

Secrion C: Species Interaction

7 Evolution of Functional Groups in Basidiomycetes

(Fungi)
F. Oberwinkler .. . . . . .. . . .... . . . .. . .. . .. ... . .. . . . 143
7 .l lntroduction . .. . ..... .. ... . .... .. ... . ........ . .... . 143
7.2 What Are Fungi? . . ..... . ....... . ..... . . .. . . .. .. . 143
7.2.1 Yeasts and Dimorphic Fungi . . . . ............. . .. .. . 144
7 .3 FunctionaJ Fungal Groups .. .... .. ... . . . . .. . .. .. . . 145
7.4 Evolution of Fungal Parasites of Plants . .. .... . .... . 145
7.5 Evolution in Diverse Wood-Decaying Fungi .. ... .. . . 148
7.5.1 Saprobic Fungi .... .. ... . .......... . .. . . ........ . 149
7.6 Evolution in Symbiontic Basidiomycetes . . ......... . 149
7.6.1 Basidiolicbens .. ... ... ... . . ... ...... . ... .. . .. ... . 150
7.6.2 M'ycorrhizae . ................ . ... .. .. .. ... .... . . . . 150
7.7 Diversity and Coevololionary 'fiends in
Septobas:idiales ................ . ..... . .. .. .. . .. . . 151
7.8 Conclu.sion_s .. . ...... . .. . .. . . . .... .. .. . .. . ..... . . 162
Referen cec; . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 163

8 The Role of Parasites in P lant Populations and

Communities
J.J. Bu_rdo_o . . . . ........ . . . ... .... . ... .. .. . . ... .. . . 165
8.1 Introduction .. .... . . . . . .. . ... . . . .. . . .. . . . . . .. .. . . 165
8.2 The Diversity and Specialization of Parasites and
Their Effects on the Fitness of t he Host Plant . . .. .. . 166
8.2.1 Parasitic Plants .. . .... . . . . . . .. . . . . ....... .. . .. . . . 166
8.2.2 Fungal and Viral Pathogens . .. .. . . .. . .. .. .. ..... . . 167
8.3 The Hidden Effects of Parasite Attack -
Changes in the Genetic Structure of Plant
Populations . . ... .. .. . .. .... ... .. ... .. . .... . ... . . 170
8.4 Parasite Attack as a Determinant
of Ecosystem Struct ure .... . .. . . .. . . . .. .. .. . .. . .. . 1.71
8.4. 1 Lessons from Exotic Pathogens and Severely Disturbed
Natural Systems . .. ... ... . .. .. .. .. ..... . .. . .... . . 172
8.4.2 Evidence from Natural Parasite-Host Associations . . . 1.75
8.5 Conclusions ............. . . . ..... ..... .. .. . .. . .. . 177
Reference..c; . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 177
Contents XVII

9 Plant-Microbe Mutualis.ms and Community Structure

D.J. Read . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . JS·t
9.1 Introduction .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. . 181
9.2 Plant-Microbe Mutualis.ms in Grassland Communities 183
9.3 Plant-Microbe Mutualisms in Savanna
and Tropical Forest Communities . . . . . . . . . . . . . . . . . . 188
9.4 Plant-Microbe Mutualisms in Boreal
and Temperate Forest Communities . . . . . . . . . . . . . . . . 190
9.5 Plant-Microbe Mutualisms in Heathland
and Related Wetland Ecosystems . . . . . . . . . . . . . . . . . . . 196
9.6 The Role of Mutualisms i.n Succe.~sional Processes . . . 199
9.7 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 202
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 203

10 The Evolution of Interactions and Diversity in Plant-

Insect Systems: The Urophora-Eury toma Food Web in
OaJls on Palearctic Cardueae
H. Zwolfer and J. Arnold-Rinehart . . .. . . . . . . .. .... . 211
10.1 Introduction . .. . .. . . .... .. .. .. . . . . .. . . . .. . . . .. .. . 211
10.2 The Urophora Food Web .. . . . ... . ... . .... .. ..... . 212
10.2.1 General Ecological Characteristics of the Urophora-
Eurytoma System ... . .......... . . .. ..... . . . .. . . . . 214
10.2.2 Structure and Evolution of the Urophora Gall .. .... . 215
10.2.3 The Effect of the Gall Size on the 1\vo Eurytoma spp. 219
10.3 Resource Exploitation, Interactions, and Evolution . . . 22t
10.3.1 The Evolution o f Diversity at the Herbivore Level of
Plant-Insect Systems ... . . . . ... ... . .. . ... . . . .. . . .. . 221
10.3.2 Host Plants as Underexploited Resources .... . .... . . 222
10.3.3 Exploita tion Strategies in the Urophora-Eurytoma
Syste·m . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 223
10.3.4 Intera.c tion Patterns at the Second and Third Trophic
Level: Evolutionary Adjustments in Food Webs ... . . . 224
10.4 Conclusions . ...................... ... .. ... . ... . . 226
Referen.ces . ..... .. . .. . . . ....... .... . . . . .. .. .. .. . 227
Appe.ndix 0 0 ••• 0 0 • 0 0 0 • • • •• 0 ••• 0 0 • • • 0 0 • 0 • • 0 ••• 0 •• • 231.

Section D: Commu nity Interactio ns

11 Keystone Species
WOJ. Bo.nd . 0 •• 0 • ••••• • •••• • 0 • • •••• • •• •••• • •• • • 0 0 237
1t.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 237
11.2 H ist ory of the Concept . . . . . . . . . . . . . . . . . . . . . . . . . . . 238
11.3 The Different Kinds of Keystone Species . . . . . . . . . . . . 238

....... .........,,...
:
XVIII Contenu

11.3. 1Keystone Predators .. . . ... ... . .. ... . . ... . . .. . . .. . . 239

t 1.3.2Keystone Herbivores .. . . ...... . .. ........ . . .. . .. . . 241
l L3.3 Keystone Pathogens · . ..... . .. .. ... . . . . . .. . . . .. . .. . 242
U .3.4 Keystone Competitors . . ...... . . . . . .. . ... . . .. . . . . . 242
1J .3.5Keystone Mutualists ...... . .. .. ... .. .. .. .. .. ... .. . 243
t 1.3.6BartJ1-movers ... .. .. . .. . ..... . .. . . . ...... . . ... . . . 245
11.3.7 System Processes .. . ... . . . . . .. .. .. .. . .. . . . . .. . .. . . 245
11.3.8 Abiotic Processes . .. .... .. .. .. . . ... .. .. ... .. . ... . 246
11.3.9 Summary of 'JYpes of Keystone Species . .. . .. .. .. . . . 246
1'1.4 Identifying Keystone Spede.s . .. .. . .. . .. .. .. . • . . ... . 247
11.4.1 Towards a General Protocol . .. . ..... ... . .. . . . . . . . . 248
11 .5 Which Keystone Species Are Vub1erable'l . . . . . . . . . .. . 249
1 t.6 Conclusions .. ... . . . . ... .. .. .. .. .. .. . .. . . . .. ... . . 249
Rei-:-erences ... .. ....... . .... . ........ . ... . .. ... . . 250

12 Redundancy in Ecosystems
J. H. Lawton and V. K. Brown 255
12. 1 Introduction . . . . . . . .. ... ... . . .. . . .. .. ... .. .. . . . . . 255
12.2 Evidenc.e from the Fossil Record ... ...... .. ...... . . 256
12.3 Patterns of Energy Flow, Biomass and the Structure
of Food Webs ...... . .... .. .. .. . . ... .. .. .. ... . . . . 257
12.3.1 Productivity and Biomass . .. . . .. .. .. ... .. . . ... .. . . 257
12.3.2 Food Webs . .. .. .. . . . .. . . . . ... . . . . .. . . .. .. .. . . . . . 258
1.2.4 Theoretical Models of Ecosystem Stability and
ResilieJlC·e .... ... . . . . ... . . . .. .. ... .. . .. . ~ . ~ . . .. . . 2.59
12.4.1 Species Deletion Stabibcy .. ... . ... ... .. ... . ... .. . . 260
l2.4.2 Poss.ible Modelling Approaches .. . . . . .. .. . . .. . .. .. . 261
12.5 Observations and Experiments on Real Systems . . .. . . 261
12.5. 1 Species Richness and Population Fluctuations .. ... . . 261
12.5.2 Keyswne Spe.cies . . ... .. . ... .. . ... . . . .. .. .. .. .... . 262
12.5.3 Manipulation Ex;periments: General Considerations . . . 263
12.5.4 Manipulation Experiments: EX'amples . ...... . .... .. . 264
12.6 Conclusions .. . . . . ... ... ... . .. ... .. . ... . ..... . .. . 266
References . ..... .. .. . .. .. . .. . ... . .. . .. . .. ..... . . 268

13 How Many Species Are Required

for a Functional Ecosystem?
F. 1. \Voodward .. . . .. ..... . . .. .. . . . .. ... . .. . .. .. . 271
13. 1 Introduction ... . . . ... .. ... ... . . ..... . .. . ..... .. . . 271
13.1.'1 Ecosystems .. ... ... .. ... . .. . . . . . .. . ..... . .... . .. . 271
·13..2 Species Diversity and Ecosystem Properties .. ... . . .. . 272
13.2.1 Introduction . . . . .. .. ... ... .. ........... .. ... . . .. . 272
13.2.2 ~pecies Enumerations and Ecosystem Functions . .. . . . 273
13.23 The Inequality of Species in Ecosystem Function .. . . 276
13.2.4 Species Diversity and Ecosystem Stability . . .. .. . . .. . 277
13.2.5 Spe.cie,s Numbers and Dynamics: Year-to-Year Averaging 279

•• ·•:h ·"'!"''"' .
Contents XX1

18 Resource Supply and Disturbance as Controls over

Present and Future Plant Diversity
S. E. Hobbie, D. B. Jensen, and F. S. Chapin, III . . . . . 385
18.1 introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 385
18.2 Future Resource and Disturbance Regimes . . . . . . . . . . 385
18.3 Plant Genetic Diversity . . . . . . . . . . . . . . . . . . . . . . . . . . . 3S7
18.3.1 Patterns of Genetic Diversity . . . . . . . . . . . . . . . . . . . . . . 388
18.3.2 Land-Use Changes and Habitat Fragmentation . . . . . . 389
18.3.3 Climatic Effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 390
18.3.4 Resource Availability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 391
18.4 Plant Species Diversity . . . . . . . . . . . . . . . . . . . . . . . . . . . 392
18.4.1 Regional Patterns . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 392
18.4.2 Latitudinal Patterns . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 394
18.4.3 Paleoecological Patterns . . . . . . . . . . . . . . . . . . . . . . . . . . 394
18.4.4 Future Changes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 395
18.5 Diversity of Plant Functional Groups . . . . . . . . . . . . . . . 396
18.5. 1 General Con.~iderations . . . . . . . . . . . . . . . . . . . . . . . . . . . 396
18.5.2 Control by Resources and Disturbance . . . . . . . . . . . . . . 398
18.5.3 Types of Functional Groups . . . . . . . . . . . . . . . . . . . . . . . 399
18.5.4 Climatic Predictors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 400
1.8.5.5 Future Diversity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 401
18.6 Landscape Diversity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 403
18.7 Consequences of Changing Biodiversity . . . . . . . . . . . . . 403
1.8.8 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 404
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 405

19 Ecosystem Stability, Competition,

and Nutrient Cycling
F~ Berends.e . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4()9
19.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 409
19.2 Stability of Model Ecosystems . . . . . . . . . . . . . . . . . . . . . 410
1.9.3 Competition and the Loss of Diversity . . . . . . . . . . . . . . 413
19.4 Stabilizing Consequences of COmpetitive Interactions 414
19.5 Effects of Organisms on T heir Physical Environment . 419
19.6 Features Affecting Plant Fitness Under Different
Nutrient Supply Conditions . . . . . . . . . . . . . . . . . . . . . . . 421
19.7 Consequences of the Different Effects of Plant Species
on the Nutrient Cycle . . . . . . . . . . . . . . . . . . . . . . . . . . . . 423
19.8 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 427
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 428

20 Modelling Biodiversity: Latitudinal Gradient

of Forest Species Diversity
Y. Jwasa, K. Sato, M. Kakita, a.nd T. Kubo . . . . . . . . . . 433
20.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 433

....... .........,,...
:
XXII Contents

20.2 Hypotheses Explaining the Variation

of Species Diversity .. ... ...... ... ... .... .... .... . 434
20.2.1 Specialization of Resource Use ........... ...... .. . 434
20.2.2 Mode of Disturbance ............................ . 434
20.2.3 Smaller Opportunity for Competition ............. . 435
20.2.4 Productivity .. . ........................ . ........ . 436
20.2.5 Specific Herbivores and Pathogens ............ .. .. . 436
20.2.6 Evolutionary/ Ecological History .......... ........ . 436
20.3 Tree-by-Tree Replacement: Finite Population Models .. 437
20.3.1 Spatial Scale of Disturbance and Dispersal ......... . 438
20.3.2 Inhibited Regeneration .......................... . . 439
20.3.3 Temporal Fluctuation of Regeneration Ability ...... . 441
20.4 Species Packing to Temporal Niches:
Infinite Population Models ..................... • .. 441
20.4.1 Model ................. .. ....... .. .. .. ....... . . . 442
20.4.2 Species Diversity Versus the Length
of the Unfavorable Season ......... .... . .... . .... . 443
20.4.3 Species Diversity Versus Niche Width ............. . . 444
20.4.4 Phenology of Coexisting Species .................. . 445
20.5 Conclusions ..................... . .... .......... . 447
References ..................................... . 449

21 Functional Aspects of Landscape Diversity:

A Bavarian Example
E.-D. Schulze and P. Gerstberger .................. . 453
21. 1 Introduction ................. .. .. ........ . ...... . 453
21.2 Geology and Vegetation .......................... . 453
21.3 Land Use in Northeast Bavaria ................... . 454
21.3.1 Hedgero\vs ........................... . ......... . 456
21.3.2 Grasslands .. . ................................ . . . 461
2'1.3.3 Forests .......................... . ............ . . . 462
21 .4 Conclusions ........ . .......... 0 • • ••••••••••••••• 464
References . . 1 t t 1 0 0 0 • 0 0 0 0 1 1 0 • 0 1 1 t 465

Sect.ion F: Industrial Analogy and Policy

22 Biodiversity Issues in Computing: A Study of

Networked Computer Viruses
C. Partridge and C. Malmstrom ... . .............. . 469
22.1 Introduction .................................... . 469
22.2 Stable Distributed Computer Systems .............. . 470
22.3 Computer Viruses ............ . .................. . 471
220301 Duff's Virus 0... 00... ... .... ... 0. ... 0 ... 0 ... 00 . . 471
22.3.2 The Morris Virus ............................... . 472
Contents XXIII

22.4 Diversity and the Spread of a Networked Virus . . . . . . 473

22.4. .I A Simple Mathematical Model . . . . . . . . . . . . . . . . . . . . 473
22.4.2 Functional Diversity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 475
22.4.3 Species Diversity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 477
22.5 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 479
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 479

23 Biodiversity and Policy Decisions

L. F. Pitelka . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 481
23.'1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 481
23.2 Conserving Biodiversity . . . . . . . . . . . . . . . . . . . . . . . . . . . 482
23.3 Global Climate Change . . . . . . . . . . . . . . . . . . . . . . . . . . . 483
23.4 Ecological Research and Policy Decisions . . . . . . . . . . . 485
23.5 Providing Policy-Relevant Research Results . . . . . . . . . . 486
23.6 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 492
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 492

Conclusion

24 Ecosystem Function of Biodiversity: A Summary

E.-D. Schulze and H . A. Mooney .................. . 497
24. t lntroduction ......... . . . .. ... ........ ... .... ... . . 497
24.2 What Is an Ecosystem? .. ................. ... .... . 497
24.3 The Regulation of Ecosystem Processes .. .. ........ . 499
24.4 Are There Functjonal Groups? .................... . 501
24.5 Determinants of Species Numbers ................. . 503
24.6 Ecosystem Integrity .......... .... .......... .... . . 506
24.7 Effects of Global Change on Land Use and Climate . 506
24.8 Conclusions .. . ............. . ........ . .......... . 507
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 509

S ecies Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 51 1
S11b ·ect Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 52 1
Section A
Ecosystem Function

.......... ... .... .....

; ~ _
6 P .M. Vitousek aod D .U. Hooper

c
0
~
u
c Type2
:J

E
-Q)
VI
>.
VI
0
u
w Type3
5 10 15 20 25
Number of species
Fig. I.J . Possible functional relationships between biological divcnity and ecosystem-
level biogeochemical functions . Type I curve implies a linear effect of diversity , type 2
suggests an asymptotic relationship, and type 3 suggests ihat' there is oo effect of dive.rsity

each additional species having a constant effect on ecosystem function <~cross

a broad range of diversity (type 1, Fig. 1.1). It may be asymptotic, with
a decreasin.g and ultimately disappearing effect of adding species to an
ecosystem (type 2). F inally, at the other extreme the relationship could be
t10n-existent, with additional species (beyond one represen tative of each
sign.ificant group , such as plants or decomposers) having no effect (type 3).
Lawton and Brown (Chap. 12) suggest similar patterns. Figure 1.1 illustrates
the influences of biological diversity in isola.t ion from the many oth.er factors
that affect ecosystem biogeochemistry, in mauy cases more strongly ·than
does diversity. These include both abiotic {climate, soils, nutrient inputs in
precipitation) and biotic (competition with microbes for nutrients, grazing,
disease) controls. Additionally, for convenience, Fig. 1.1 is drawn as if
maximizing the biological diversity in a site !llaxim.izes some aspect of.
biogeochemistry in that site. Wh.ile that cou.ld occur, it is not necessary to
our discussion of the effects of biological diversity.
We anticipate that, in practice, the type 2 pattern wiU prove to be most
widespread in natural ecosystems. Adding species until all major functional
groups (i.e., nitrogen fixers, successional pioneers, deeply rooted plants) are
represented should have a larger effect on a given proc.ess than would
furt.her additions of representatives of those groups. While the type 2 pal-
tern could also apply to d.iversity within functional groups, within-group
diversity might affect the persistence or sustainabd.ity of ecosystem functions
more t11an their rate or regulation in the short term.

1.3.1 Experimental Tests

Experimental studies of the effects of bi.ological diversity on ecosystem

hi geochemistry are sparse outside of agriculmral ecosystems (Swift , Chap.

! .I ,." " + + ._ +
10 P.M. Vitousek and D.U . Hooper

1984), and high altitude fir forests in Japan and the northeastern United
States turn over in wave fo rm and othe r die backs (Sprugel 1976; Tadaki
et al. 1977; R eine rs and La ng 1979). Substantial ecosyste m-level bio-
geochemical consequences of some of these die backs have been docu me nted
unambiguously (Sprugel 1984; Ma tson and Boone 1984).
lt is difficult to demo nstrate that low diversity itself is the cause of these
die backs and their biological consequences, as dieback mjght be expected
to be mo re prevalent in the e>.1reme e nvironme ntal situations in which
monospecific systems predominate. Ho wever , Muelle r-Do mbois (1987,
1988) has described o ne plausible but as yet unproven example of the effects
of low diversity on dieback in a wet tropical forest environment in Hawaii.
The native flo ra and fauna of the H awajjan Isla nds are strikingly depaupe rate
(Carlquist 1980), and a single tree species, M etrosideros polymorp ha,
occupies an extraordinarily wide e nvironme ntal range, often as a dominant
(Muelle r-Do mbois et al. 1981; Ste mmermann 1983; Vito usek et al. 1990) .
M e1rosideros is ofte n the sole cano py do minant in lower mo nta ne rainfo rest
areas, although it is accompao.ied by a rather diverse array of subcanopy
and understory species. (Comparable a reas on continents could support a
hundred o r more canopy species per hectare.) In such sites, Metrosideros
stands a re subject to a stan d-level dieback of unknown etiology that removes
the canopy mo re o r less synchrono usly ove r te ns of thousands of hectares
(Mueller-Dombois 1.987, 1988). No measureme nts of the biogeochemical
conseque nces of this dieback have been carried out, but they are likely to be
as significant as those in o ther die backs that have been evaluated.
This situation might re prese nt an appro priate o ne for de termining the
effects of biological diversity o n lo ng-term ecosystem functioning. The
Hawaiian Islands are a t the end of a series of tropical high islands that
stretch from the Indo-Malayan source area across the Pacific Ocean. These
intermediate archipelagos are also inte rmediate in species diversity. Con-
sequentl y, the tropical Pacific mo ntane forests may provide a rela tively clear
gradie nt in diversity that is little complicated by variation in other e nviron-
mental factors (Mueller-Dombois 1990) . This gradient could re present a
usefu.l resource for evaluating the lo ng-term interactions between biological
di versity and ecosystem function.

1.4 Other Potential Effects of Plant Diversity on Biogeochemistry

The purpose of this sectio n is to identify specific biogeochemical processes

that could be influe nced by plant species and functio nal group diversity. Our
aim is not to pro vide an exha ustive list , but ra ther to suggest po te ntial
mechanisms that might be particularly amenable for study. Primary
productivity is the most obvio us of these, and it is discussed by Swift and
Andersen (Chap. 2) and MacNaughton (Chap. 17) .
14 P. M. Vitousek and D.U. Hooper

Singer FJ , Swank WT, O.ebsch EE C (1984) Effects of wild pig rooting in a deciduous
forest. J Wilde Manage 48: 464-473
Smith OL (1982) Soil microbiology: a model of decomposition and outriem cycling. CPC,
Florida
Sprugel DO ( 1976) Dynamic struct ure of wave>generated Abies btzlsamea (orests in the
northeastern United States. J Ecol 64: 889- 911
Sprugel DG (1984) De nsity, biomass. productivity, and nutrient cycling changes during
stand developme·n t in wave-regenerated balsam fir forests . Ecol M.o uogr 54: 164- 186
Staat H (1980) ln1l uence of chemica.! composition, addition of raspberry leaves, and
nitrogen supply 011 deco mposition rate and dy.n amics of nitrogen a11d phosphorus in
beech leaf lin er. Oikos 35: 55- 62
Stemmermann L (1.983) Ecologica l studies of Hawai.ian Metr osideros iu a successional
context. Pac Sci 37: 361 - 373
Tadaki Y , Sato A, Sakurai S, Takeuchi I, Kawahara T ('1977) Studies on the producrion
structure of forests: structure and primary production in subalpine " dead t ree strips"
Abies forest near Mt Asahi . Jpo J l~col 27: 83- 90
Vitousek l'M , Walker LR (1989) Biological invasion by Myrica faya in Hawaii: plant
demography, ni trogen fixation. and ecosystem effects. Ecol Monogr 59: 247- 265
Vitousek PM, Wal.ker LR, Whiteaker LD, MueUe:r-Dombois D , Matson PA (1987)
Biological invasion by Myrica faya alters ecosystem development in Hawaii. Science
238: 802-804
Vitousek PM, Field CB, Matson PA ( 1990) Variation in foliar o13C in Hawaiian
Metrosideros polymorpha: a case of internal resistan.c e? Occolob.j.a 84: 362- 370
Wedin DA, Tilman D (1990) Species effects on nitroge n cycling: a test with perennial
grasses. Oecologia 84: 433-441
Wel.ls JM, Hughes C, Boddy L (1990) lbe fate of soil-derived phosphorus in nJycelial
cord systems of Phanerochaete ve/uti11a and Plwllos impudicus. New Phytol lJ4: 595-
606
Woods l.E , Cole CV, Porter LK , Coleman DC (1987) Transformati<rns of added
indigenous nitrogen in gnotobiotic soil: a comment on the prlmin,g effect. Soil Bioi
Biocbem 19: 673- 678
Woodwe U GM , Smith HH (eds) (1969) Diversity and stability in ecological systems.
Brookhaven Symposium. vol 22 264pp Techmical l nformation Center, Atomic Emergy
Commission , Spring field , Virginia
Zak DR, Grofman PM, Pregitzer KS, Christensen S, T iej e JM (1.990) The vernal dam:
plant-microbe competition for nitrogen in northe rn hardwood forests. Ecology 71:
6541 - 656 .

! .I ,.;.,. + + ._ +
18 M .J . Swift and J .M. Anderson

manure, leaf litter and even soil , for the arable fields (Swift et al. 1989) . In
such a system the di versity of plants in the savanna has an influence. on the
crop production subsystem as well as on the cattle production subsystem.
The biotic components of agricultural ecosystems can be classified .in
re.lation to the role they play in the productive function of the system, as
well as in conventional ecosystem function terms (Fig. 2.2). Thus, species
may be regarded as productive, beneficial or dcstru,:tive components,
depending on the target of the farmer. Management will be directed towards
maintain ing the former two categories and destroying the thi rd, although
management tools are often relatively indiscriminate in thei r target and can
result in the destruction of beneficial species as a side effect of agricultural
production activities. Some species are introduced to agricultural ecosystems
by deliberate choice, others arise by changing the resource base (up or
down), the internal environmeut (irrigation, tillage, fertilisation , etc.) or the
scale of the agricultural operation.
We can usefully group the biota into three categories on this basis:
The productive biot11: tbe crop plants and livestock, producing food , fibre
or other products for consumption, use or sale; we employ this term in the
broad seuse of an y product used outside the production syst em (e.g. to
include medicinal product1>, construction materials, etc.). This component of
the biot.a is deliberately chosen by the farmer and is the main determinan t of
the diversity and complexity of the system (Fig. 2.1).
The resou.rce biota: these are the organisms which contribute positively to
the productivity of the system but do not generate a product directly utilised
by the fanner; examples are many of the plant species of fal lows or cover
crops used to manage soiJ ferti lity, pests and weeds (e.g. legumes in Fig.
2.2); often it is the function , rather than the particular species, that is
subject to conscious management, and the species which develop may have
both beneficial and deleterious effects. For instance, a common dominant of
short-term fallows in the humid forest zone is Chromolaena odorata. Whilst
this species is thought to have beneficial effects on soil fertility and is often
used by farmers as an indicator of th.is, it also acts as a weed during the
succeeding crop cycle.
The fauna and flora of the decomposer subsystem also come into this
category (Fig. 2.2), but the diversity and composition of this group are
seldom subject to deliberate management. An exception at the interface
between the decomposer and plant subsystems is the symbiotic microflora
such as nitrogen-fixing bacteria and mycorrhizal fungi which increasingly are
being deliberately introduced into low input agricultural systems.
The predators of pests are beneficial resources which may be a product of
management, either indi.rectJy by the inclusion of plants which encourage
diversity in the herbivore sub~-ystem, or by direct attempts at biological
control by the deliberate release of predators.
The destructive biot11: weeds, animal pests and microbial pathogens.
Management is aimed at lowering the diversity of this component.

'·:t> .......,~ ...

22 M.J . Swift and J.M. Anderson

probability norm (e.g. within a 95% climatic probability range) wo uld be a

more appro priate target.
Furthe rmo re, most concepts o f sustainabili ty require both continuing
yield and the avo idance of enviro nmental degradation. T aken in the starkest
way, these t.wo demands are often pictured as being mutua.lly incompatible .
Agricultural production depends on resource utilisation, whils t e nviro n-
mental pro t:eclion requ ires some acceptable exte nt of conservation. A major
aim for the scientist designing sustainable cro pping systems is thus 1he
reconciliatio n of these two factors. T he target in this case would seem to be
t he maintena nce of resources withi n re newable limits a nd the mechanism,
~ -
controlling the e fficie ncy o f resource use.
T his brief discussio n of sustainabi.lity suggests that ecological questions
o n the re lationship between biod iversity and ecosystem functio n are also
pertine nt to the concerns of p ractical agricultu re . For instance, tJ1e time-
ho no ured de bate on t11e re latio nship between diversity a nd stability has a
particular implication for agricultw·al syste ms. So does the li nk between
inte rna l complexity (e.g. of nutrient cycling) and effici e ncy of resource use
( Hobbie et a l. , Chap. 18). Fo r tbe ecologist the concept of sustainability,
a lthough yet poorly defined , may provide a focus for t11e conside rat ion of
certa.in aspects of ecosystem studie-; in response to global change. An altera-
tion in land use is recognized by the Interna tio nal Geosphere Biosphe re
Programme (IGBP) as a majo r feature of globa l change but is as yet not
addressed very direct ly in the research programme. Important feedback
etfects result from agricultural inte nsification. T raditional agricultural prac-
tices such as shifting cultivatio n have gained a bad re putation because
the clearing of new land for agriculture leads to high e missio ns of C0 2
from bio mass burning. Equally, however, the intensificatio n of cultiva tion
increases the o utput of C 0 2 from soil o rganic matte r oxidation and from the
e missio n of o the r greenhouse gases. Sustainable systems should be o nes
which mi nimize t hese effects as well as meet the aspira tions of the farmers.

2.3 Productive Attributes of Low Number Multiple Cropping Syst.ems

Our genera l paradigm (Fig. 2.1) ide ntifies control of the plant species as the
point of primary regulation of biodiversity in agricultura l systems- the
farme r decides which produ ctive plants she or he will grow in a given field ,
and whether they will be combined with any resource plants. For the
peasant farmer of the tropics, multiple cropping is the usual patte rn of
cultivatio n. The numbe r of crop species is usually at leas1 2- 4, fre que ntly
greater tlHin 10, a nd sometimes an o rder of magnitude more. T he main
reason is the desire for multiple products, including those of significant
cultural va lue such as medicines or food additives. Inte nsificatio n of agJ·i-
culture, particularly under the less favou rable e nvironme ntal conditions of

' •," >;••·~· '" ,.. • .

30 M.J. Swift and J.M. Anderson

i:lHI 3 .1
Cultures /

TS~~K15.5 G Pontoscolex coreth

Other earthworms

Termites
u 8.5
c::::J Ants

Coleoptera
PK 93.9 c m.9
Fallows Myriapoda
20.5
_______________-r []I[] Arachnida
80 1592 c::::J Others
Forests Pastures

Fig. 2. 7. Biomass of different groups of soil fauna in various land-use systems 10 the
Peruvian Amazon. The relative biomass is shown by the area of the circles and sectors
thereof. The mean total biomass is given next to each land-use system which are defined
as follows: Forests, primary ( PF) and secondary (TF); fallows ; peach-palm plus kudzu
(PK) and Centrosema pubescens (C); cultures, low input (L/), high input (HI) ,
traditional fallow (TS) and kudzu fallow (K) ; pasture, improved by inclusion of
Brachiaria and Desmodiwn (B D) . (After Lavelle and Pashanasi 1989)

which they might disperse in an unbounded plot, and if the animals die, the
regulating nutrient released from the biomass can have significant effects on
plant growth in nutrient-limited systems. Second, there is a stimulatory
effect of disturbance by soil fauna which cannot be sustained in the absence
of additional resource inputs, as shown in the control treatments. Nonethe-
less, earthworm introduction on the field scale have been carried out with
some spectacular results.

2.4.3 Interactions Between Plants and the Soil Biota

The activities of soil biota are closely regulated by the plants, both directly
and indirectly. The direct effects are th rough the type and amount of
organic matter inputs above and below ground. [ndirect effects include the
physical effects of shading, soil protection and water uptake by roots. These
feed back directly to plant growth because the activities of the soil biota
affect water and nutrient availability both spatiaiJy (e.g. localised under
mulches) and temporaJJy (during the cropping season). At the beginning of
the rains, seeds are planted into the seed bed which has either been tilled or
mulched for weed control and improved rooting conditions. The initial
stages of seed germination and seedling establishment largely depend upon
soil microclimatic conditions. The mulch cover provides physical protection
34 M.J. Swift and J.M. Ande rson

·A. Natural Ecosystem

Plant Subsystem

..
Helbivore Subsysem
lnpu I
0 0
··-·
d'o d-'o
---·-··········· -----··-··----------
Above ground
..... .
-·-···~------------

.. o0 o BelOw ground

0
Oulll\11

Oecomposy
SubsySiem
t -~
r
0· 0

B. Intensive Agricultural System

lllpul
• Plant

Output -
IHWeSt) Aba\l'e ground

Oeeompo~c•
SubsySiem ..0~
oll------=o

Control of Ecosystem Function

Fig. 2.8A,B. The influence of plant dive rsity on ecosystem function in (A) nantml
ecosystems (with high plant biodiversity) as compared with (B) intensive. abrriculrural
ecosystems (with low plam biodiversity). A rrows represent control pathways whicb may
comprise eoergy, matter aod infonnational exchanges, with the thickness of the anow
represe nting the importa nce of the e:xch:mge to d1e control of ecosys te m function.
lmeracrion circles on 1he boxes are a symbol for diversity in that sector o f the ecosyste m
community

Even under circumstances in which the input of energy and nu trient

from Lhe plant subsystem to the decomposer subsystem is not significantly
affected , lowered diversity in the plant community will nonetheless have
profound effects on the decomposer community and its function.
36 M.J. Swift and J. M. Anderson

Ecosystem !unction
and s1ability

?
,
/
/
/ ?

/
/
/

Land
Equivalent 2
Ratio

1 2 3 4 5 10 100 n.
Nu.mb&r o1 plant species

Frg. 2.9. The retarionsbip between plant biodivers.ity and the productive function and
stabi)jry of ag:riculn•ra.l systems. Data points ror land eguivalent ratio (LER) are for
Central American multiple cropping systems (Moreno and Han 1979). The lines are
hypotberical, postulating possible relationships betweeu p.laot species number a-nd t.hc
efficiency and stability of ecosystem function. lt sbould be emphasised that yield gain
(LER) is unlikely ro increase beyond 3 species, however; improved ecosystem function
will be invested in other aspects such as greater nut6.eut retention

2.6.2 The Importance of Increasing Plant Species Number

There seem to be very few examples where invest igations have been made
of multiple cropping (i.e. of the i11teraction of more than 2 species), even
though this is the practice adopte<l by a large majority of tropica] farmers. A
rare example is given in the lower left part of Fig. 2.9.
It is a valid question as to whether in these very simple systems with only
2, 3 or even 4 species, there is a significan t extent of integrated ecosystem
function. Our hypothesis of uncoupling of the plant-decomposer control
mechanisms suggests that the only significant inte!,rration of function in such
systems may lie in the decomposer community. This may be particularly so
where the species are all annual. Is there time during the brief occupancy of
the space for any thing but the most general of physical and spatial interac-
tions to be established between plant species? Or do the plants behave
essentially as they would in mouocrops, i.e. the plant-plant interactions are
essentiaJiy characterisable as density dependent (in a broad space-occupancy

' •.• ·• h·· ' .~.

38 M.J. Swift and J.M. Anderson

Table 2.1. Differences in the planHO-St)iJ "signa l" in

different two-plam mixtu res of crop plant

Cropping systems Change in

Chemical s.ignal Physical signal

Maize
Maize + millet Low Low
Maize + melon Low High
Maize + pro:;tmte cowpea High · Same
Maize + Leucnena ffigh High
Maize + Acioa High Same

Chemical signrll, Influence of chemical composition on

decomposer activity.
Physicnl signal, ln Ouence of plant o n 01icroenviro nments at
surface or within soil. Chemical and physical signals chan ge
as the accompanying pla nt is changed.

2.6.4 Assessment of Long-T erm Trends

Wh ich is more important, the number of species or tbe continuity of inter-

action between them? Sy~;terns that have some constancy in ti me may develop
positive feedback relationships between the associated species and between
the subsystems which facilitate the stability and continuity of function. For
instance, a long-term alley cropping system may become more stable as
microclimates are stabilized , integrated nutrient cycles are established , and
soil resources reach stable equilibria. May there a.lso be more subtle rela-
tionships? If maize is grown year after year, is thai crop more facilitated
th an any other by some " memory" in the system?

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Anderson JM ( 1978) In ter- and in tr·a-habitat reJations hips betwe.e n woodland
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Anderson JM (1987) The r-ole of soil fauna in agricultural systems. In: Wilson J R (ed)
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Environ 24: 5- 19
Biodiversity and Ecosystem Function in Agricultural Systems 39

Ande rson JM , Spencer T ( 1991) Carbon, nutrient and water balances of tropical
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Christensen M ( 1989) A view of f1mgal ecology. Mycologia 81: l - 19
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savan na. In: Tothill JC, Molt JJ (eds) Ecolo!,ry and management of ibe worlds 's
savannas . Australian Academy of Science, Canberra, pp 200- 206
Frost P, Menaut J-C. Wal.ker BH, Medina E, Solbrig OT, Swift MJ (1986) Responses of
savannas to stress and disturbance: a proposal for a collaborative programme of
research. Biology lnt.ernation al , Special Issue lO, IUBS , Paris
Grigg DB (1974) The agricultural syste ms of the world: an evolutiollllry approach .
Cambridge University Press, Cambridge
Grime .J P (1977) Evidence for the ex.iste nce of three primary strategies in plants and its
relevance to ecological and evol utionary theory. Am Nat 111: 1169- 1194
Heal OW, Dighton J ( 1985) Resource quality and trophic structure in tbe soil system ; In:
Fitter AH, Alkinson 0 , Read OJ , Ushe r MB (eds) Ec.:ological interactions in soil.
(Special Public-iltion No. 4), British Ecological Societ·y, Blackwell , Oxford
He ndrix PF, Parrn ilee RW . Crossley DA, Coleman DC , Odum E P. Groffman PM ( 1986)
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374-380
Hunt HW , Coleman DC, I ngham ER, Ingham RE, Elliott RE, Moore JC, Rose SL, Reid
CP, Morleg CR (:1987) T he detrital food was in a short grass prairie . Bioi Faitil Soils 3:
57- 68
Ingham RE, Trofymow JA , Ingham EA, Coleman DC (1985) Interactions of bacteria,
fungi and their nematode grazers: effe.cts o n nutrient cycli ng and plant growth. Ecol
Mo nogr 55: 119- 140
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I.zac AMN, Swift MJ (1992) C'-Ommon property resources in West AfTican agriculture:
sustainability and improved tecboologics. Proceedings Second Annual Conference ,
International Assoc.iatioo for the Study of Common Property, Winnipeg (in press)
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Kung .BT, Reynolds L, Atta-Krah AN (1990) Alley farming. A.dv Agron 43: 315- 359
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E.cosyst Envi.ron 24: 104- 116
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Earthworm ecology: from Darwin t O vermicultme. Chapman & Hall, London , pp
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Lavelle P, Pashanasi B (1989) Soil macrofauna and land manage me nt in Peruvian
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syste ms. Adv Soi.l Sci 13: 241 - 2501
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University Press, C.1mbridge, pp 307-338
3 Biodiversity and Interactions
Within Pelagic Nutrient Cycling
and Productivity
C.E.W. Steinberg and W. Geller

3.1 Introduction: Explanations to tbe Paradox of the Plankton

T he high biodiversity in plankton communities led Hutchinson (1961) to

pose his classical question: " How [is it] possible for a number of species to
coexist in a relatively isotrophjc or unstructured envir onment, aU competing
for the same sorts of materials?" Indeed, the almost ubiquitous existence of
multispecies communities, especially on the microorganism level, is one of
the few firm facts in ecology (Pimm, Chap. 1.6).
Wilson (1.990) notes that are at least l2 mechanisms which can serve as
answers to the paradox. With phytoplankton, the most frequently accepted
concept of ecosystem and community organization is centered around the
nutrition needed for survival and reproduction (see Hobbie et al. , Chap.
18). The implication of this concept is that organism s have to compete for
common resources and/or to feed on each other. lnteractions between
populations are therefore primarily negative (competition, predation,
parasitism , allelopatby) (Darwi nian concept), with symbiosis as a ratJ1er
exotic case (Sommer 1989) .
Current views explaining the species composition of phytoplankton fa ll
on a continuum . One extreme position holds that phy toplankton species
composition can be explained by species-specific requirements of resources,
the abilities to harvest resources, the abilities to withstand mortality, and the
dependence of these requirements and abilities on physical conditions. This
view has gained conside rable momentum from T ilman's (1982; Chap. 1.5 ,
this Vol.) competition theory and from increasing knowledge about grazing
selectivities (Sterner 1989). According to this view, p hytoplankton com-
munities will be dominated by species best Sllited to the current combination
of growth and loss factors.
The other extreme position denies that there will ever be enough time for
" best swted'' species to replace less suited ones until conditions change and
invert the competitive hierarchy. Community composition will therefore
be more determined by it.s history than by the comparative abiliti.es and
requirements of species. Harris (1986) used the term "founder effects" to
characteri ze tl1is phenomenon.
44 C.E.W. Steinberg and W. Geller

3.2 Further Determinants of Biodiversity

3.2.1 Plasticity and Cell Shape

An interesting observation on plankton diversity was published rather

recently by Duarte et al. (1.990), referring to the size plasticity of individual
algal genera or species. A survey of the phytoplankton communities in
Florida lakes indicated that onl y a minority of the populations were at or
very close to their maximal achievable densities. Non-nutrient constraints
including self-regulation by the algaJ community may be playing an im-
portant role in the maintenance of di versity .
T his self-regulation mechanism may be the size plasticity of ind.ividual
species or genera . The size of phytopla nkton algae is recognized to be of
great adaptive value because it constra.ins phytoplan kton growth a.nd loss
rates, thereby significantly influencing the abundance and contribution to
community biomass of individual taxa. U nicellular algal speci.es are remark-
ably variable in cell size both individually and within the population; further,
colony-forming species, notably cyanobacteria, may modulate some of their
functional characteristics by changing colony size, thereby increasing their
operational size ra.nge (Duarte et al. 1.990).
The average size of phytoplankton cells in lakes tends to increase with
increasing community biomass, and larger algae tend to develop greater
biomass than smaJJer a1gae. Small algae seem to be better competitors in
sparse communities, and conversely, large algae are superior competitors
i.tl dense communities. Sparse to dense phytoplankton populations may
be brought about either by corresponding nutrient conditions (bottom-up
effect) or by the grazing pressure of herbivorous zoopla.nkto o (top-down
effect). Furthermore, physical factors, such as turbulence, can act as selec-
tive forces on the phytoplankton community composition (MargaJef 1978;
Steinberg and Hartmann 1988; Reynolds 1989). These mechanisms are by
no means mutually exclusive.
In fre.<;bwater systems of high turbulence, such as dam med rivers, even
nano- and microplan.ktonic forms (nu"linly colony-formin g cyanobacteria)
appear in very minute-sized forms. Extreme size plasticity was found within
Microcystis aeru.ginosa or Coelosphaerium k.uetzingianum, which appeared
as rather sm all single cells within the picopla.nkt"ic fraction (definition see
below) (Chang and Steinberg 1987) .
Grover (1989) combined allometric relations between physiological
processes and ceiJ volume and surface area with the variable internal stores
model of growt.b to predict the ability of hypothetical phytoplan kton to
compete for phosphorus at equilibrium. The analysis shows that for spherical
cells, sma11er cells are better competi tors than large ones. For cells that are
very elongated in shape, however, large cells are often better competitors
than small o.nes. The cells predicted to be the best competitors compare
Biodiversity and Interactions Within Pelagic Nutrient Cycling and Productivity 45

favorably in size and shape witll the species observed to domjnate in

phosphorus-limited chemostats at equilibri um.
In another study, Grover (1991) suggests that competitive tre nds can be
rapid in both equmbrium and non-equilibrium habitats. The traits that
confer competitive ability in equilibrium habitats can also confer competitive
ability in non-equlibrium habitats .

3.2.2 Turbulence

Succession in phytoplankton commumt:Jes is initiated by some physical,

hydrographic event; its capacity for progress is also subject to physical
controls, but the di rection and eventual outcome of the successio.n, so
long similar physical conditions persist, will be primarily influenced by
interspe.ci.fic interactions of the developing community (Reynolds 1989).
T his can be demonstrated with cyanobacterial appearance as a function of
both nutrients and turbulence (Steinberg and Hartmann 1988). Eutrophica-
tion of freshwater bodies involves the enrichment of plant nutrients, often
followed by significant shifts in the phytoplankton towards cyanobacteria.
When comparing different aquatic systems, even with similar nutrient con-
tents an d in the same climatic region, inverse deductions are not valid, i.e.
(a) the presence of cyanobacteria does not necessarily indicate eutrophic
freshwater condi tions, or (b) eutrophic or even polytrophic conditions do
not necessarily support cyanoba.c terial development .
Above a threshold of l O~Lgl - 1 total phosphorus, the development of
cyanobacteria can be described by physical factors , such as water column
stability . By characterizing qualitatively different forms o'f turbulence, the
presence or absence of cyanobacteria in lakes and rivers can be predicted.
When the turbulence of the water column is rather low, as it is in
sheltered or meromictic lakes, cyanobacteria can build up dense popula-
tions. In nutrient-poor systems, species of Oscillat.oria!Limnothrix and
(seldom) Aphanizomenon are dominant. Jf the turb ulence of the water
column is high (mixing depth much greater than euphotic depth) or the
mixing pattern is irregular, as in slowly flowing or regulated rivers,
cyanobacteria are outcompeted.
In the presence of frequent or permanent turbulence, but with mi>dng
deptl1s lower or not much greater than the euphotic zone (as is the case
in shallow, unstratified lakes, mostly eutTopbic or even hypertrophic),
cyanobacteria can outgrow normally dominant r-strategists under condi-
tions of low N : P ratios, high water temperatures, pH > 9 or low light
availabilities. If the mixing depth is comparatively great (10 to ~15 m) and
stable for a longer period of time, some cyanobacteria are able to adapt.
In geueral, turbu.lence appears to have a diverti.ng influence on
phytoplankton species. For instance, during induced intermitt.ent artificial
mixing, diatoms, desmids and t11e cyanobacteria Oscillatoria achieved rapid

''" 'f '" ',_•••

46 C.E.W. Steinberg and W. Geller

Table 3. J. Maximmn growth rates of plan.ktonic ri ve r diatoms. Pbotoo flux density:

45 1-UllOlm- 2 day- • (PobJmano J989)

Species (complex) Diameter (pm) Temperature River

("C)
Main I M ain 1.1 Regnitz lsar

Cy'clorella 3- 12 14 0.68 0.83 1.02 Ll8

Cyclotella 13-30 22 0.80 1.10 1.30 1.45
Cyclostephanos > 30 20 0.70 089
dubit.IS
Skeletonema 21 1.08 1.35
s11bsal!mm

ra tes of growth during mixing wbich then declined or were overtaken by loss
rates during "quiescent", restratifyh1g episode.<;. Eudorina and Sphaerocystis
grew well during quiescence but declined during mixing episodes. During
mixing phases, r-strategists (e.g. Rhodomonas and A nkyra) reached maximum
"true" growth rates not exceeding 0.75 d - :l. The growth rates of oth er
"summer species" (A nabaena, Ceratium , Volvox, Microcyst.is) were de-
pressed duri ng mixing, though they generally maintajned their existing
biomass. By thus contro lling the biomass of r-sel.ected species and delaying
the crop maxima of the K-selected "summ er species" , the total stand-
ing crop of phytoplankton was below the mean nutrient-carrying capacity
(R eynolds et al. 1984).
On the other band, in phytoplankton-s upporting stretches of rivers,
turbulence obviously favors certain phytoplankton species with high growth
rates or is even the cause for such growth rates. ln several south German
rivers, Poh lmann (1989) found maxjmum growth rates ranging from 0.68 to
1.45 d - 1 (Table 3.1) . Such growth rates are typical of ftesbwater picoplankton
(Table 3.2) .

3.3 Selection and Succession

The concept of r - and K-selection bas been profitably appl.ied to marine and
freshwater phytoplankton. This concept is particularly usefuJ if one wishes
to relate the physicochemical characteristics of the environment to the
biological properties of planktonic algae. Even though r-and K-selection are
often referred to as separate entities, they represent a continuum of Life-
history strategies. The r-selected organisms are considered to have evolved
in unstable or newly formed habitats. They have high population growth
rates, but they cannot maintain high population densities for long: either the
environment changes (including grazing), or they are outcompeted by other
Biodiven;ity and Interactions Within Pelagic Nutrient Cycling and Productivity 47

organisms. The K-selected species are thought to have evolved at or near

the carrying capacity of the environment. As a resuJt, they use resources
efficiently, and their competitive ability is high. Small r-selected algae
aUocate resources primarily to reproduction, while K-sel.e cted algae allocate
resources to a variety of non-reproductive activities that maximise the
genetic survival of individuals. These include activities that enhance an
individual's ability to obtain and store resources and adaptations tbat reduce
mortality (e.g. large size, manufacture of toxi ns, body armour, symbiosis,
etc.).

3.3.1 Descriptive Model of Plankton Succession

ln order to understand how concepts of r- and K-selection can be applied to

plankton, it is instructive to present the model of the seasonal succession
i.n a temperate lake, the PEG model (Plankton Ecology Group of the
lnt'ernationale Vereinigung flir theoretische und angewandte Limnologie;
Sommer et al. 1986). By abstracting from individual case studies, tl1is model
emphasizes possible mechanisms of succession (bot:tom-up as well as top-
down) instead of descriptions of successional sequences.
The model seqllence has a total of 24 steps. To demonstrate the principal
mechanisms, we focus on the spring events, as it is the most interesting
phase of the year. In the original PEG model (Sommer et aL 1986) neither
bacteria nor the microbial loop (see below) are considered. Based on studies
on bacterial plankton in Lake Constance, Gi.ide (1989) fi lled parts of this
gap.
L Toward tbe end of winter. nutrient availability and increased light
permit unli mited gtowth of phytoplankton. A spring crop of small ,
fast-growing algae such as cryptophyceae and small centric diatoms
develops. Soon after the beginning of the algal spring bl.oom , bacteria
recover from tl1eir «wi nter dormancy'' because of the increased sub-
strate supply from the development of primary producers.
2. The crop of small algae is grazed upon by herbivorous zooplankton
species that soon become abu ndant. As a consequence of the increased
supply of bacterial food , phagotrophic microflagellates soon reach high
densities. Thus, the structure of the zooplankton community is now also
influenced by the availability of bacterial food. AJthougb the estimated
grazing rates on bacteria are high at this time, bacteria can maintain
elevated population densities because the grazing losses can be offset by
high bacterial reproduction .
3. Planktonic herbivores with short generation times increase their popula-
tions first and are followed by slower-growing species. The result of
increased gtazing is a reduction in substrate limitation and a stimulation
of bacterial growth rates.

l ·v1o.-n..h<';"- ,
50 C. E . W. Ste in berg and W. Geller

;""\
of \
..
(/)
(/)

::!
41
/
\
\
0
Cll

PHYSICAL FACTORS

LIMITATION

..
(/)
(/)

::!
..
(/)
(/)

::!
-
0
Cll -
0
Cll

PHYSICAL FACTORS
PREDATION

- FOOD LIMITATION

Fig. 3.2. The seasonal development of the phytoplankto n (top panel) and zooplankton
(bouom panel) in an idealized , stratify ing , slightly e utrophic (left) and in an idealized,
stratifying, oligotrophic lake (right). Top panel: small algae (dark shading) ; large algae
(light shading) ; large diatoms (hatching; in small lakes only); zooplankton biomass
(dashed line). Bouom panel: small herbivores (dark shading); large he rbivores (light
shading); phytoplankton biomass (dllShed line). Horizomal diagrams indicate the periods
when major environmenta l constraints a re important. (Sommer e t al. 1986)

3.4 Microbial Loop: Structure and Function

3.4.1 Structure

3.4.1.1 Phototrophic Picoplankton

.
According to Stockner (1988) , the terminology follows the logical size
boundaries for pelagic plankton as defined by Sieburth et al. (1978) and Klut
and Stockner (1990): microplankton (20- 200 ~tm), nanoplankton (2.0-
20 11m), picoplankton (0.2-2 11m) and femtoplankton (0.02- 0.2 J.lm).
The discovery of minute (0.2-2.0 J.lm) phototrophic picoplankton in the
late 1970s in great abundance in both marine (Johnson and Sieburth 1979)
and freshwater (Paerl 1977) ecosystems led to a resurgence of research
activity. Two major groups of algal picoplankton may be distinguished by
thei r cellular structure: prokaryotic (cyanobacterial , with Synechococcus)
Biodiversity and Interactions Within Pelagic Nutrient Cycling a nd Product ivity 51

and eukaryotic (minute Chlorella or Rhodom.onas spp.) (Srockner ru1d An tia

1986).
Apart from their enumeration by e piAuorescence microscopy, which
e nables a preliminary separation into e ukaryotic and cyanobacterial groups,
surprisingly little taxono mic work has been done. Because of their extremely
small size, the ultimate identification of a utotrophic picoplankton will
require ultrastructural methods. Usi ng scanning and transmission electron
microscocopy Klut and Stockner ( 1990) have found femtoplankton (0.02-
0.21-!m) sized , virus-like particles and bacterial and au totrophic picoplankton
(0.2- 2 J.Un) associated with larger forms and in the p hytoplankton com-
muuiry of a Canadian lake. These associations suggest the prevalence of
ecological interactions, e.g. commensalism, symbiosis or para<;iti.sm.

3.4. 1.2 Mixo- and Heterotrophic Constituents

In the past decade, a view of plankton dynamics in which phototrophic

and hete rotrophic microorganisms can play an important and sometimes
dominati ng role in the cycling of matter has begun to emerge (Azam et <tl.
1983; Porter et al. 1985). Population dynamics of flagellates include periodic
blooms of both pigmented and heterotrophic fomt.s. Dur ing these periods,
the total impact of flagellate grazing on picoplankton can be high. Further-
more, the transfer of materials and energy from tl1e microbial into the
classic food web via the crustacean ingestion of nanoflagellates at th~;..-se
times is potemially great , especially in Jakes in which Cladocera dominate
the zoo plankton (Be nnett et al. 1990). Aquatic bacterial production is
currently thought to be largely controlled by bacterivore predation, with
rnicroflagellates and small ciliates being Ule most important consumers (see
Sherr and Sherr 1984; Porter et al. 1985). Pelagic bacteria and Protozoa are
components of the " microbial loop" (Azam et aL 1983), which is an integral
part of a more complex food web.
Most heterotrophic nanop.lank.ters are small (2-5 1-!m), colo rless,
flagellated protists. They grow at about the same rate as bacteria (It =
0.01 - 0.02 h- 1) and are capable of consuming the entire bacterial produc-
tion. They also regenerate significant amounts of nutrieuts and serve as prey
for micro- and mesozooplankton. Some photosynthetic flagellates are also
bacterivorous; for inst!mce. mixotrophic Dinobryon has been shown to
be one of the most important bacterial removers (Bird and Kalff 1987;
S~ndergaard et al. 1988) .
Be rninger et al. (1991) have quantified the bacteria, heterotrophic
nanoplankton and other microorganisms in various lakes, ponds, rivers
and bogs worldwide. These water bodies spa.n the range of biological pro-
ductivit y fou nd in freshwater. Numbers of heterotrophic nanopla nkters
and bacteria Rre correlated over 4 orders of magnitude in each, aud both
increase wit h the productivity of the water body.

''" 'f '" ',_•••

52 C.E. W. Steinberg and W. Geller

3.4.2 Functioning of the Microbial Loop

3.4.2.1 .Autotrophic Picoplankton Production

Table 3.2 summarizes published estimates of photoautotrophic picoplankton

growth, production and biomass from both marine and freshwater eco-
systems. The contribution by picoplankton to the tota l carbou production
ranged from 1 to 90% , with a tendency for substantially higher contributions
in more oligotrophic regions of the world's oceans. Estimates of algal
picoplankton biomass (chlorophyll) were generally less variable than pro-
duction, contributing from 1 to 90% to the total chlorophyll biomass.
Reported assimilation numbers for algal picoplankton were quite high,
indicative of a rapid turnover of carbon per unit chlorophyll. Rates of
picoplankton carbon production from freshwater are lower than marine
values.
In both freshwater and marine ecosystems, the algal picoplankton con-
tribution to total primary production tended to increase with depth in the
euphotic zone, reflecting the greater efficiency of their photopigments
to utilize blue-green light (Stoclmer 1988 with references) . Rates of
picoplaokton carbon production showed little variation along e utrophic
gradients, but the percentage contribution by picoplankton was considerably
higher in oligotrophic open oceans (50-80%) than in meso-eutrophic coastal
marine waters (2- 25%) . Similar trends were also noted in lakes of varying
troph]c states, with some exceptions. One exception is some e pisodic mid-
summe r cyanobacterial picoplank'ton blooms that seem to occur in some
eutrophic lakes (i.e. Cronberg and Weibull 1981). Another exception
is cyanobacter.ial dominance in eutrophic dammed rivers during v.'inter
months, when minute cyanobacteria ( <5 ~1m) were the only phytoplankters
(Chang and Steinberg 1987) (Fig. 3.3).
l11 Lake Constance, autotrophic picoplankton production varies between
less than 1 up to 10 mg C m - J h - t . The relative contribution of autotrophic
picoplankton production to total phytoplankton primary production varied
between 5 and 65% of total 14 C incorporation in Lake Constance in 1988.
Maximum percentages were measured in late spring and in summer (Weisse
and Schweizer 1991).

3.4.2.2 Nutrient Cycling

Nitrogen and phosphorus limit the growth of primary producers in many of

the world's oceans and lakes. Since relevant aspects of phosphorus cycling
were dealt with in the description of the PEG model above, the focus now
will be on nitrogen.
Suttle et al. (1990) demonstrated with 13N that clissolved NH4+ pools,
often undetectable with standard chemical methods, may turn over in as
54 C. E. W. Steinberg and W. Ge ller

bacteria, picophytoplankters) . If l'.'l-14 + is supplied in patches, a 1.5-fold

increase in the amoun t of C reaching the mesozooplankton occurs. In
P-limited freshwa te r environ ments when POi - is distributed in a patchy
manne r, the net result is about a 3.6-fold increase in the amount of C in
mesozooplankton (see also Sommer 1984) . Pulsing nutrie nt release by graz-
ing zooplankto n is thought to be one main reason for the high diversity
within t he phytoplankton. In their study o n Paraphysomonas imperforatn,
a marine colorless cbrysophyceae feeding on mixed bacteria, Nagata and
Kirchman (1991) found that even di~-sol ved (free and combined) amino acids
were released in considerable quantities (up to 22% ).

3.4.2.3 Pelagic Productivity

The study of Weisse et al. (1990) is t.he first to report o n the productivity
of all components of the microbial food web including a utotrophic and
heterotrophic microorganisms (Fig. 3.4). They found in Lake Constance
that more than 50% of the primary production was channelled thro ugh
the microbial loop. Bacteria a nd ciliates responded rapidly to increasing
phytoplankton biomass and productio n. Maximal growth rates of bacteria
and protozoa were slightJy lo wer than those of the dominating phytoplankton
species. Ave raged over U1e spring bloom, bacterial C amounted to 21%
of phytoplankton C, bacterial production to 18% of particulate primary
production. An io.crease in heterotrophic flagellate populations was pre-
vented by grazing within the microbial loop. A lthough the ciliates con-
trolled flageJJate production, they satisfied their food de mand primarily by
feeding on algae and consum ed -14% of primary production. Me tazoan
microzooplanktoo (copepod, nauplii and rotifers) removed only - 7% of the
phytoplankto n production. Herbivorous me tazooplankton ingested slightly
less.
Plankton diversity and productivity was studied by Stockner and Shortreed
(1989) in the pelagic communities of contrasting oligotrophic lakes of British
Columbia. The question was why an interior, dim.ictic (rwo turnover ti mes
per year) lake (Quesnel} supports a greate r biomass of zoopla nkto n and
produces larger planktivorous sockeye salmo n (Oncorhynchus nerka) than a
coastal, warm, mo uomictic (one turnover tim e per year) lake (Sproat). The
ultra-oliogotrophic status a nd differing planktjvore densities in. Sproat Lake
increased the relative impo rtance of algal picopla nkto n, diminish ed the
abundance of large zooplankton and increased the significa nce of rotifers
a nd other small-bodied zooplankto n. These picoplauk-ron-based food webs
result in longer , indirect and less efficient path ways of carbon flow from
phytopla nkton to fish. In contrast, Quesnel Lake is a more productive
ol.igotrophic lake, and its pelagic food webs are based more on nauoplankton
and s maJJ microphytoplankton that support larger-bodied zooplankton
(Daphnia, Diaptomus) and a more direct and ef.ficie nt two-step trans fe r to
Biodiversity and lnteraclions WitJ1in Pelagic Nutrient Cycl.ing and l'roductivity 55

M!crozoopl .
CLASSIC PELAGIC FOOD WEB Q (Metaz . l

~.?
Phyto-
planKton:..--- - · fl ··..:.._ Macro-
.•••: <:::. zoop l .
14 1.'•(6 .911
5655
:
.: .• ?
615 •• •
539 ••
(301) I

.. ,-'•-~~
126 .311 •
••
+205 •••• ?
\ ..•
314
l lS . 3Xl
93
SeOi l!lentatlon 37
537
119 1
37
Ci l i ates
Bacter i a
MICROBIAL LOOP
I~ Aup lrotlon I
Fig. 3.4. Carbon tyudget £rom the euphotic zone of Lake Constance (Bodensce~ duri~
the spring 1988 ph>•toplan ktoo bloom (pools in mg C m- l and fluxes io mg C m- day- ,
averaged over 0- 20 m and the study period; Weisse et al. 1990). HNF. Heterotrophic
nanoflageUates

fish . The presence of substantial populations of Daphnia, which occur only

in the more productive oligotrophic lakes, provides an efficient tw<rstep
transfer of phytoplankton (nanopla nkton) carbon to fish, and one of the
consequences of this higher production is the ability of these lake.-; to
support a greater biomass of planktivorous fish. DaphnitJ occurs in Sproat
Lake because the epilimnehc temperature exceeds 20°C for much of the
summer, and the main planktivore juvenile sockeye will have much reduced
acce.-;s to Daphnia because of their known avoidance of waters with tem-
perature >l7 °C (top-down effect).

3.5 Structural Diversity lnd.ices

ln general, diversity arises from a balance between growth processes and

loss processes for aU the species in the assemblage. In an equilibriwn
community, predation may actually increase divers.ity if it .f alls mainly on the
numerically dominant organism. l.t1 a noo-equilibri.um community, however,
the greatest diversity wiJI arise when many sp ccit:s grow rapidly one after the
other and persist between growth periods.
Biodiversity and Interactions Within Pelagic Nutrient Cycling and Productivity 57

this finding. According to Margalef (1980), low diversity .indices may

indicate immaturity, whatever this may mean for the 6800-year-old Crater
Lake .
Several problems exist with diversity indices. Diversity of individuals, of
biomass or of production suggests quite different degrees of maturity of a
given community. Low diversity as a measure of immaturity of a system has
to be proven in each single case under consideration . Furthermore, it seems
unacceptable that static figures, such as species numbers and abundances,
can be a measure of a dynamic process, such as the interrelation ships of
species with their abiotic and biotic environment , competition, succession,
species shift or reversio n and evolution, even if the indices are calculated on
the basis of short-term plankton analyses. Several examples suggest that it
might be misleading to draw ecological conclusions from diversity indi.ces, if
functions in the community are unknown (for example Statzner 1981).
Apart from these considerations, there are further, rather practical
reasons why an application of diversity indices seems to be inappropriate.
Discus~ion of diversity and calculation of diversity indices in plankton com-
munities require qualitative analysis of bacteria, protozoa, autotrophic
and heterotrophic flagellates as well as of photoautotroph.ic picoplankters.
Owing to insu fficient methods and taxonomic knowledge, th.is is difficult
and - at present - in many instances impossible .

3.6 Ataxo.nomic Approach to Assess Ecosystem Stability

Sheldon et at. {Sheldon and Parsons 1967; Sheldon et al 1972) used elec-
tronic counters to sort and count automatically size-classified planktonic
particles in the ocean. U nexpectedly, they found a near-equal biomass of
differently sized "p articles", meaning organisms, when subsequent classes of
size were ordered on a logarithmic scale. h is known that physiological rates
of respiration, growth or generation time are first-order dependants of body
size (e.g. Peters .1983). These allometric relationships ho.ld over about 20
orders of magnitude of body weights from unicells to big mammals, includ-
ing the planktonic organisms. Feochel (1974) gave the first comprehensive
overview in which both rates of respiration and of growth were treated as a
common th.e me. With these relationships quantified in operational form, aiJ
the nece.<>sary pieces were available to establish a theory on a continuous size
distribution in the pelagic ecosystem, both marine and freshwater. Progress
towards the development of a continuous model depended on leaving behind
the notion of discrete trophic levels (Platt 1985), demanding organisms to be
assigned to one trophic level and stipulating that only a small number of
mutually exclusive trophic categories exist. Quantitative conclusions about
overall food chain efficiencies furthermore require simplified assumptions
58 C.E.W. Stei nberg and W. Gel.ler

about the ratio between the body sizes of predators and their prey, say a
factor o f 10 in body length or HP by weight (Kerr 1974). Adverse to this
assumption are the facts that (1) tl1e autotrophs in the sea cover a broad
range of cell size of at least 107 by weight, and (2) a given predator,
probably feeding on all particles of su.itable size, is assigned to only one
trophic level. The lan er fact appears to be an unjustified simplification of
the pel ~t.gic system (Plan 1985). Also, in nutrient-rich systems with high
concentrations of food p articles, new predator ty pes appear and dominate,
which are not do mina6 ng or even present in nutrient-poor systems. T hese
fi lter-feeders make use of filtering apparatuses to acquire their food , which
are much smaller relative to their own size tha n they should be accordi ng to
the above-mentioned predator type. These filter-feeden; may show a rela-
tion of body sizes of 102 to HP by length, or 106 to 108 by wei.ght (Geller
1991) . The existence of different types of predators feedi ng on very dif-
ferently sized food leads to more complex food webs, ma king obsolete the
idea of simple food chains.
Within the context of the Rize distribution in the sea, Azam et al. (1983)
have analyzed the ecological role of heterotrophic microorganisms. T hey
conclude that abo ut 25% of tl1e net primary production passes via dissolved
organ ic matter th rough bacteria, which are then grazed by microzooplankton
(principally heterotrophic flagellates in the size range of 3- 10 11m). Tltis
microbial loop may be seen as an example of the material flowing in
the troph.ic continuum against the general direction of small to large.
Microzooplankton, through their excreted metabolites, thus become im-
plicated as playing a major part in the remineralization of nutrients in the
sea , a ro le traditionally assigned to bacteria.
In the literatu re considering the relationship between the microbial loop
and the known classical components of the planktonic food web, some kind
of artificial separation emerged . Fenchcl (1988) pointed out the unsuitability
of th is separation and showed the microbial loop to be a normal consti111ent
of planktonic food webs. The planktonic food web consists of multiple,
parallel pathways o( energy flow, the basic organizational trait being the
size-specific feeding. Consequently, the separation of herbivorous grazers
and carnivorous predators appears to be artificial, be<.~ause both types feed
on all organic particles, which are about one order of magnitude smaller
than the consumer organism. AJI c.onsumers, therefore, should be con-
sidered as omnivorous: they feed on equally siz.ed green (= autotropbs) and
" non-green" food ( = heterotrophs} as well. Tltis basic structure of th e
planktonic food web appears to be a sufficient description of nutrient-poor
plan ktonic systems. Other systems with higher levels of nutrients and denser
suspensions of food are amended by the appearance of additional fi lter-
feeders as mentioned above .
This view of ru1 organismic food web structure and the fi nding of Sheldon
and his c.oworkers rhat an ataxonomic conti1mous distribution of planktonic
B.iodiversity and lntcraclions Within Pelagic Nutrient Cycling and Producti\~ty 61

10 ~--------------------------------.

8
X
lr:":"a-.
ut~um=nl

6
Plankton 0
Biomass
[gC/m*2] lsprin9j
4 0

0+------r----~~----~----~------4
0 0.5 1 1.5 2 2.5
Plankton Production
[gC/m*2 d]
Fig. 3.7. Relation between mean daily produc:rioo and biomass of tbe total plao.kton
c:ornmunity in Lake Constance, during 10 seasona.l pbases in 1987 (Geller et al. 1991):
winter and summer relationships follow the eq ua tion:
biomass == 4.68 x production - 0.48; r ~~ 0.998.
PlB is high durio.g spring with turnover times of 2 days, PfB is low during autumn witb
turnover times of 6-7 days and is nearly conStant over all other phases of the year with
turoover t:irnes of 4 days, irrespective of levels of biomass

advantage might be the automatic counting and smng with electronic

devices. The allometric relationships between physiological rates and body
size furthermore lead t:o first-order estimates of energy flows through the
system, even where these rates were not. or cannot be directly measured .

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Oceanogr 35: 1821 - 1832
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''" 'f '" ',_•••

64 C.E.W. Steinberg and W. Geller

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Section B
Functional Groups
 0. Meyer

Primary producers
(Plants and Oestruenls
mlcroorganisms) (Mlcroorganisms)

Consumers
(Animals a.nd
microorganisms}

f'tg. 4 . 1.
. Key func6ons of microorganisms, pl.ants. and animals in tbe global carbon cycle.
l11e main primary producers aod consumers are plants and animals, respectively

Earth would soon come to an end if the physiological groupings of micro-

organisms discussed in this article did not function properly or became
ex-tinct.

4.2 Free-Lh·i ng Component.; of the Soil Microbiota

The free-living components of the soil mjcrobiota are the bacl.eria, fungi,
and algae. Bacteriophages and viruses, wbjch are additionally there, grow
only within the ljving cells of soil organisms and are metabolically inert but
genetically active, e.g., they can facilitate or effe.c t the spread of genes
between different microorganisms. The role of plasmids u1 microbia.! ecology
(Berringer and Hirsch 1984) , evolution of new phenotypes (Clarke 1984) ,
genetic interactions in microbial communities (Slater 1984), and the conjugaJ
plasmid transfer in natural bacterial communities (Fteter 1984) have been
treated elsewhere and are not discussed here.
Bacteria are the most abundant of the microorganisms in soils (Table
4.1), aJtbough their actual number may vary considerably with soil type,
depth, water content, temperature, nutrition, and location. Indeed , bacteria
are the most common of all living organisms on the earth. The next most
common organisms in soil are fungi, algae, protozoa, and earthworms, in
that order but at much lower numbers (Table 4.1). The biomass of soil
(micro)organisms shows a djfferent sequence (mg dry weight per kg of soil):
fungi ('1750)_, bacteria (750), earthworms (280), protozoa (125), and aJgae
(5; Gisi et al. 1990). Since microbia] activities are related to the cell surface
Functional Groups of Microorganisms 69

Table 4.1. Microbial cell counts in soils (Gisi et al. 1990)

Organisms Viable cell counts in soils"

Rhizosphere Root-free

Bacteria 5.3 X 1010

Selected bacterial groups:
Actinomycetes 4.6 X 1010 7 X J09
Amrnonifiers 5 X 1011 4 X 109
Denitrifiers l.3 X 1011 I X lOS
Gas-producing anaerobes 3.9 X HY' 3X 107
Cellulolytic aerobes 7X HY' 1X lOS
Fungi I X 109 1X lOS
Protozoa 2 X lo<' 1 X !09
Algae 5 X Hf 2.5 X 107
Earthworms n.db 0 1- 1

" Viable cell counts are per kg of soil dry weight.

b n.d. , not determined.

and not to mass, bacteria which represent the smallest microorganisms are
the most active. Fungi play a critical role in the degradation of natural
polymers (e.g., lignin and cellulose); however, they are less active and
metabolically versatile than bacteria ; they are dealt with in Chapters 7
(Oberwinkler) and 9 (R ead) of this volume. Algae are obligate photolrophs,
and their activity is thus restricted to the soil surface or aquatic systems
(Steinberg and Geller, Chap. 3); the same applies to phototrophic bacteria.
Microorganisms are ubiquitous and cosmopolitan , and 1 know of no
distributional barriers. They are easily transported over long distances by
wind, water, or animals (Paul and Clark 1989). Transport of bacterial cel.ls,
their spores, or dormant stages might occur iJldependently or in association
with dust panicles or aerosols. Transocean transport of dust bas been docu-
mented, and microorganisms are recoverable from snowflakes faJLing at high
altitudes even after long intervals of precipitation. Microorgan isms can
travel from one continent to another in ocean currents or with migratory
birds. Bacteria possess numerous mechanisms to withstand and survive
h armful conditions, e.g., through the formation of endo- or exospores, as is
known for Bacilli, Clostridia, methanotropic bacteria , Streptomycetes, and
others.
An important consequence of the considerably high microbial cell counts
in soil, ease of microbial distribution, their metabolic flexibility and abi.lity
to resist detrimental conditions in natural environments is th at microbial
species from almost any taxonomic unit may be found in a gram of normal
garden soil, irrespective of the location on Earth from whence it was
collected.
Funciional Groups of Microorganisms 71

Substrates
(reduced compounds)

---.._I Cell

I
- - E<1ergy - - - - material

Catabolism .J). ~ Ana.balosm l}

n <0-.. (biosynthesis) ~
{} "-;j c >~ %:---
Exoenzymes
(and other extracellular material)
C02
(OJ other compounds)

Fig. 4.2. A simplified view o f bacterial metabolism. The energy (ATP or me mbrane
potential) produced through catabolic reactjons is used for biosynthesis or cellular
material, transport of nutrientS. maintenance or a proton gradient across the cytoplasmic
membrane, and driving tlageU11

4.3 Metabolic Types of Bacteria

The activity of microorganisms in their natural habitat is often difficu.lt

to identify. T heir metabolism is devoted to generating energy througJ1
the catabolic oxidation of reduced compounds (Fig. 4.2), whicb in most
instances are organic but may also be inorganic substances or light (Table
4.2). T he energy captured is used for growth and proliferation (Fig.
4.2). Many bacteria excrete extracellular enzymes (exoenzymes) into the
environment (e.g. , cellulases, proteases, nucleases, glucosidases) for the
depolymerization of natural polymers (Fig. 4.2), because the materials they
digest are generally too large for consumption in a single microbial celL
Animals (chemoorganoheterotrophs) and p.lants (photolithoautotrophs)
are restricted to an aerobic, respiratory, or p hototrophic type of metabolism;
they represent single metabolic types exclusively (Table 4.2). Their survival
is linked to the availability of light, oxygen, and/or organic material. In con-
trast, bacteria may act as chemoorganoheterotrophs, chemolithoautotrophs,
photolithoautotrophs, and photoorganoheterotrophs (Table 4.2). ln addi-
tion, bacteria may be aerobic or anaerobic (Table 4.2, Fig. 4.3) . Under
anaerobic conditions, two functional groups of ba.c teria are active, bacteria
with a fermentative metabolism or bacteria ca.pable of utilizing alternative
elect ron acceptors (Fig. 4.3). Suitable electron acceptors for anaerobic
respiration are oxidized organic (e.g., fumarate) or inorganic compounds
(e.g. , N0 3 - , N0 2 - , N20 , SO/- , sol -, S0 , C02 , Fe3 + , and other metal
ions), which are thereby reduced (Table 4.2, Fig. 4.3). Phototrophic bacteria
Low energy content
Hs-
Sulfur resporation:
- 28
Sullur·reducing bacteria
so
Succinate

- 86 Fumarate respiration;
V•brio sucdnogenes
Fumarate

Acelate

- 95 Carbonate respiration;
Acetogenlc bacteria
co••
Fe1 •

- 114 Iron-respiration;
Iron redY<:ong bacteria
Fe3 •

CH.

- 13t Carbonate respiration;

Mothanogenlc bacteria
co.
HS

- 152 Sulfate respiration:

Suttate·reducing bacteria
so.•

No. -

- 163 Dissimilatory nitrate respiration;

EschBrichia con

- 398 Denitrification of n~rite;

Denitrltylng bacteria

- 475
Aetotlk: respiration:
Most mlcrOO<ganisms

- 561
Denitrification ot nitrate;
Denltrilylng bacteria

Hg. 4.3. Ranking of electron acceptors utilized by bacteria in aerobic or anaerobic

respiration with respect to Gibbs· free ene rgies given in I:.J (mol of electron acceptor)- '.
(After Thauer et al. 1977. Frunzke and Meyer 1990)
Functional Groups of Microorganisms 73

are capable of usi ng H 2S and some other reduced compounds instead of

water as electron donors to perform an anaerobic type of photosy nthesis
(Table 4.2). U becomes obviotL~ that microbial life is not restricted to the
availability of light, oxygen, or organic compounds. ln addition , a large
num ber of bacteria are facultative, i.e. , they contain combinations of tJte
above metabolic types and features. Many microbiologists feel the metabolic
types and acti vities of bacteria are of much greater significance for the
understanding of ecosystem function than their taxonomic affi liation.
Bacteria in ecology are, therefore, more properl y addressed as fu nctionaJ
(physiological) groups rather than as taxonomic units. FunctionaJ groups of
bacteria involved in the biogeochemical cycles of selected elements will be
discussed below.
Winogradsky (Brock and Schlegel 1989; Zavarzin L989; and the lite rature
cited therein) distinguished between autochthonous (indigenous) micro-
organisms which grow slowly in soil contai ning no easily oxidizable substrate
and allochthonous (zymogenous, nonindigenous) m icroorgani~ms whjch
show bursts of activity when fresh res.idues are added lo the soil. This
al ready points to tl1e concept of K- and r-selection, which is of great
importance even in microorganisms. Microorganisms adapted to Jjfe under
conditions of constant energy availabi.lity at low concentrations are designa ted·
K-strategists or K-selected. They usually have high affinities (Km) for their
growth substrates but proliferate only slowly. On the otJ1er hand, r-strategists
or r-selected microorganisms are adapted to flushes of substrates at high
concentrations. They prolifera te rapidly at high Y111' " ' but their substra.te
affinity is generally low. A llochthonous microorganisms frequently suffer
from substrate stress, whereas autochthonous ones are stable since they are
adapted to substrate concentrations which are low and below thar of the Km
of the allochthonous microAora. The autochthono us microfJora is native and
permanent to a specific environment. A llochthonous microorganisms are
intrude rs or tra nsient, so they are transported to an environment or persist
there in a dormant (inactive) state.

4.4 Tbc Role of Microorganisms in t.be Decomposition of Organic Material

As a reslllt of plant primary production (Fig. 4.1) , litter, crop residues,

and root material are produced. These materials are mainly composed of
polymeric organic compounds (Fig. 4.4). Plants contain 5- 30% lignin, 15-·
60% cellulose, 10-30% hemicellulose, and 2-15% protein (Paul and Clark
1989). Many of th e naturaJ polymers are recalcitn mt or decompose slowly
(e.g., lignin , celluJose, hernicelluJose, pectin) . Only a few are easily degrad-
able (e.g., starch). Natural polymers frequently occur in association with
other polymers of different types. An example is the ljgnin-plus-cellulose
complex whicll is the normal substrate for hurnificaiion processes that occur

''" 'f '" ',_•••

Functional G ro ups of Microorganisms 75

acti vity ( Fig. 4 .2). Some exoenzymes cleave the side chains (e.g. , me thoxyl
groups); they only " polish" the polyme rs a nd do not a ttack their principal
structure . These reactions ofte n require a n additional ene rgy-yielding sub-
strate because they a re co-oxidative. Other exoenzymes catalyze a break-
down of polymers to smaller units, oligo-, di-, or monomers (Fig. 4.4) .
The latte r are ingested by the microorganisms a11d decomposed rapidl y via
ordinary metabolic pathways to yield e nergy (Fig. 4.2), C0 2 , CH.t, minerals.
and /or other degradation products (Fig. 4.4). A pro portion of the polyme rs
in nat ure is tra nsformed to humus and othe r recalcitra nt compollnds rathe r
th<m mine ralized insta ntaneously. Besides this mi ne ralization of organic
matte r, microorga nisms are also involved in soil-forming processes. For a
full treatment of all aspects of the microbial degrada tion of natural p roducts
incllldi ng sta rch, pectins, cellulose, hemicelluloses, lignin, aromatic com-
po unds, lipids, proteins, deoxyribonucleic acids and ribonucleic acids refer
to Winkelmann (1992).
Jn some instances, the micro bial exoenzyme activity is considera bly
facilitated by transferring polymer degradation into distinct reaction areas
providing optimized conditions, e.g. , into the gastrointe.stinal tract of
animals or insects. Exan1 ples of gastrointestinal microecology are the inter-
actions of the lactjc-acid-fermenting bacteria Streptococcus bovis and
Megaspfwera elsdeni i in tl1e n unen of starch-fed cattle (Russell and Allen
1984), adapta tions of bacteria in sheep rumen fluid in response to changes
in dietary oxala te a nd nitrate (Allison and Reddy 1984) , and microbial
ni trogen metabolism in the ceca (blind gut) of birds (Mortensen 1984).

4.4.1 Cellulose

Cellulose accounts for 50% of the dry weight of the photosyntJ1etic biomass
and is the most abundant of all naturally occurri ng structural polysaccharides.
It is the final product of about one-third of all the C0 2 fixed by plants. As a
cell wall develops, the cellulose network can be e ncrusted with lignin ,
producing a lignin-cellulose complex that makes the wall rigid , Limits
wa ter tra nsfe r across the waH , and reduces the susceptibility of the wall to
microbial attack (Reddy 1978; Crawford 1981 ; Lin ki ns e t al. 1984).
Cellulose is a n energy-rich molecule but too bulky to be taken djrectly
into m icrobial cells (Linki ns e t al. 1984). To make the ene rgy in cellulose
available , microorganisms excrete exoenzymes tha t hydrolyze it, converting
it into soluble carbohydrates tbat can pass thro ugh a micro bial cell me m-
bra ne . Once inside the cell, the monome ric carbohyd rates are metabolized
via ordinary metabolic patbways (Fig. 4.4).
T he exoenzymes involved in celllllose hydrolysis are collectively known
as cellulases and comprise two functional groups, exocellulases and e ndo-
celllllases (Linkins e t al. 1984) . Exocellulases will cleave glycosyl bonds near
the nonreducing e nds of cellulose molecules or " cellulose fragme nts,"
prod uced by e ndoceUulases. Endocellulases catalyze the random cleavage of
76 0 . Meyer

inte rnal glycosyl bonds of cellulose. The disaccharide cello biose resul ting
fro m cellulose degradation is byd rolyz.ed by cello biase (anothe r enzyme) to
glucose. G enerally, cellulose hydrolysis is limited by e ndocellulase activity;
the degree of limitation de pends o n the specific environment, e.g., tem-
perate forest soils versus A rctic tundra (Linkins et al. 1984). Cellulose
hydroysis i11 tundra so ils is regulate d by temperature, substrate q ua lity, and
pe rhaps the presence of certain soluble soil o rganics. E ndocellulase activity
is especially susceptible to te mperatures below 5 °C.
A mo ng the bacte r ia capable of producing cellulases are Streptomyces,
Celtulomonas, Pseudomonas, Chromobacterium , Bacillus, Clostridium ,
a nd Cytophaga (Reiche nbach and Dwor kin 1986; PauJ and C Lark 1989).
Fungi involved in cellu.lose degradation a re Trichoderma, Chaetomium , and
Penicillium.
Soil is considered to be the mai n habitat of bacteria of the genus
Cellulomonas, an d the use of Cellulomonas spp. for the productio n of
protein from wood products, their ro l.e in the decompositio n o f so lid co mpost
material, and their cellulase complex ha ve been studied (Keddie and Jones
1986). For a description of the ha bitats, isolation, e nrichment, cultivation,
a nd ide nt ification of Cellulomonas, refer to Keddie and .Jones (1986).

4.4.2 Lignin

Lignin is the most abunda nt and widely distributed renewable SOLLrce of

aroma tic nucleus on earth (Reddy 1984). Lignin constitutes 25% of the dry
weigh t of tbe estimated 100 billion metric tons of photosynthetic biomass
produced annuall y i~n the biosphere a nd is second only to ceUulose. How-
ever, Ligni n contains 50% more carbo n than ceUul.ose and othe r plant
polysaccharides and is, therefo re, rela tively mo re abunda nt as a source of
reduced carbon and solar e ne rgy tha n its weight wo uld indicate. Ligni n
biodegradation is of u tmost impo rtance in the earth's carbon cycle (Fig. 4.1)
no t o nly because of its great abundance but also because of its recalcitrance.
The biodegradati ve recalcitrance of Lignin is ascribed to its high mo lecular
weight, three-di me nsio na l structure , and high content of stable che mical
bo nds (Martin e t aJ. 1980; Zeikus et al. 1982; Oche r a nd Roch 1983).
W hereas the sugar aud polysaccha ride fractions in t he biomass are
degrad ed relatively rapidly by the soil microfio ra , the lignin fraction is
metabolized rathe r slowly (Martin ei al. 1980). Humus is also degraded
s lo wly, witJ1 a n estimated half-life io different soils of 76- 326 years (H aider
et al. 1977) .
T he functional gro up of Lignin-me tabolizi ng microorga nisms comprises
diJfere ut gene ra of bacte ria (e.g, Pseudomonas , Bacillus, Streptomyces,
Arthrobacter, Aerom onas , Xanthom onas , Flavobacterium) and fungi. T he
process seems to be the do main of the white-rot fungi , including severa l
hundred spec.i es of basidio mycetes and a few species o f ascomycetes; t he
78 0 . Meyer

Tbe peptidolytic clostridia fem1ent proteins or am ino acids to acetate,

fatty acids, ammonia, C02 , H 2 , a nd some produce exotoxins. Examples
a re C. botulinum, C. histolyticum , C. :.porogenes, C. telani, and C.
tetanomorphum. Some clostridia (e.g. , C. sporogenes) ferment only pairs of
amino acids. One amino acid serves as a n electron do nor a nd is oxidized
(e.g., aJ1mine, histidi ne , isoleucine, le ucine, valine), while another serves as
an electro n acceptor and is reduced (e.g., arginine, glycine , hydroxyproline,
proline, tryptophane). This type of coupled decomposition is kno wn as tl1e
S tickland reaction.
The saccharolytic clostridia ferment carbohydrates (e.g. , cellulose,
starch , pectin, sugars) to acetate, lactate , succinate, propionate, butyrate,
isobutyrate, isovalerate, acetone, ethanol, isop ropanol, butanol, C02 and
H 2 . C. pasteurianum is a free-living , anaerobic, N2-fixing bacterium . C.
acidurici ferments purines (e.g. , uric acid) to aceta te, ammo nia, an d C0 2 ,
and C. kluyveri conve rts e thanol to fatty acids . For a full treatment of bacilli
and clostridia, refer to Norris et al. (1986), Krieg (1986), Gotts chalk ct al.
(1986), and Claus (1986).

4.4 .4 .Pectin

Wood contains 1- 5% pectin , indicating that ii is a minor compo nent. of

the plant biomass (Cote 1977). Because of the covalent linkages between
pectin and bemicelluloses in natural p!ant tissue, pectin degradation always
implies to a certain extent hemicellulose degradation as well. The methoxyl
groups of natural pectin a re cleaved by pectin esterases, and the remaining
polygalacturooate (pectate) backbo ne is depolyme rized by a hydrolase or a
lyase which releases saturated or unsaturated ougomeric o r mo no me ric
galacturooic acid residues (Schink 1984) . Hydrolases and lyases with a
specificity for the esterified pectin polym er are also known . Depending o n
the preferred substrate ( methoxylated or nonme tlloxylated pectat.es, long-
or short-chain polymers) and the action pattern (random, terminal, or
pe nulti mate bonds attacked) , different e nzyme classes exist (Schiuk 1984).
So fa r, tl1ere is no consistent rule o n the occurrence of the various enzym e
types in tl1e different organisms; ratller, all classes of enzymes have been
fou nd in higher plants, fungi, and aerobic atJd facuJtatively or o bligately
anae robic bacteria .
The microbial a ttack o n pectin or polygalacturo nic acid-ricb acidjc
polysaccharides generally represents the initiating step in the maturation and
rotting of plant material, e.g., tissue, fruits, legumes, potato, roots , aod
tubers.
The functional group of pectinolytic microorganisms apparently comprises
few species, some of which are pathoge ns and ofte n a re specific for their
targets of attack . Potato tubers and carrot-s are preferentially rotted by mem-
bers of the genus Erwinia, which belongs to the famil y E ntero bacteriaceae
Functional Groups of Microurg-dnisms 79

(Perombe lon and Kelman 1980; Starr l986a,b). E xamples of indi vidual
species are E . carotovora (acting on carrots) and E. chrysamhem ium (acting
o n chrysanthe mums). For de tailed d escriptions of the genus Erwinia , its
habitats, isola tio n, identificatio n, and the ty pes of plant diseases the dif·
fere nt species cause, refer to Starr ( 1986a,b) and Bre nner (1986). In the
absence of o xygen, pectin hydrolysis is a lso brought abo ut by saccharo lytic
clostridia which have already been discussed in rela tio n to pro te in degrada-
tion. For a discussion of pecti:n d egr adatio n in the we twood syndrome ,
anoxic lake sedime nts, and extreme environme nts and the fate of pectin
me thyl residues, see Schin k (1984) .

4.5 Tbe Role or Mic.r oorganisms in the Biogeochemical Cycle of Nitrogen

Ino rga nic and o rganic nitrogen compo unds in nature are subject to a
microbial cycle of oxidation a nd reductio n (Fig. 4.5). The key inte rme diates
of t he biogeochemical cycle of nitrogen are a mmo nia, nitrate, and dinitrogen.
Again , the microorgan isms invo lved in the cyding of nitrogen compounds
are referred to as functio na l gro ups rathe r than taxonomic units. T he func-
tionaJ gro ups of microorganisms invo lved in the mjcrobia l cycle of nitroge n
(Fig. 4.5) are the nitrifying bacte ria (they conve rt ammonia to ni tric acid
in a two-step rea'-1 ion) , tl1e de nitrifying microorga nisms (they use n.itrate,
nitri1e , o r N2 0 as e lectron acceptors for anaerobic respiratio n, forming N 2) ,
nitroge n-fixing bacteria (they reduce N 2 to ammo nia which is assimilated) ,
nitrate and nitrite ammonifie rs (they usc nitrate o r nitrite as an e lectron
sink, fo rming ammonia), ammo n.ium-assimilati ng microorganisms (the
assimilation of ammonium into amino acids has to be acco mplished by all
microorganisms), a nd deaminating microorganisms (tJ1ey cleave ammonia
from amino acids , pe ptides, and proteins).

4.5. 1 Nit rificatio n

NitriJication (i.e ., the conversio n of ammonia to nitrate) is initiated by rwo

d iffe re nt functional groups ot: bacte ria, the Rmmo nium oxidize rs which con-
vert ammonia to nitrite using an 0 2 -dependent a mmo nium moooo xygenase,
a nd t he nitrite oxidizers which oxidize nitrite to ttitrate using a molybde num-
conta ining ni trite oxido re ductase. Bo th physio logical groups contain gram -
negative bacte ria with an obl.igal'e requireme nt fo r oxyge n. With one
exceptio n, the y are o bligate chc molitho autotrophs rhat ma ke use of the
ene rgy rel.eased fiom the two o xidation re actio ns. The nitrify ing bacteria
assimilate carbo n d ioxi de into tl1e cell material via the ri bulosebisphosphate
cycle .
80 0. Meyer

NtttificatkHl
(ae:obic)

(Ammonium (Nil.ri.l e oxkla!..an)

ox~)

Assimlfatlon
(aerobic c. anoe<Obic)

Nlti09GI\ 1\xa!l()ll
taerotHc 01
il,aet"OOC)

OonMiiealion
(an-00.:)

Fig. 4.5. Functional groups of microorganisms iu tbe biogeochemical cycle or nitrogen.

Open arrows refer to seq uences occurring within sii1gle organ.isms, small arrows refer to
intermediates

Nitrifying bacteria are ubiqujtous, and natural enrichments are found at

sites of ammonia accumulation such as manure or the brick walls in the
cellars of old buildings. Although nitr ifying bacteria are cbernolit bo-
autotrophs, their growth is not inh ibited by organic compounds. They
inhabit soils, compost piles, sewage disposal systems, fresh water and
marine habitats, and most other aerobic environments in which organic
compounds are being mineralized (Watson et al. 1986). For an extensive
description of t.he habitats, isolation, maintenance, identification , and other
microbiological properties and a full list· of references, refer to Watson et aJ.
(1986), Bock et al. (1989), and Prosser (1989). Nitrification in natural
environments is nearly exclusively carried out by the chemolithoautotrophic
nitrifying bacteria (Alexander 1977; Watson et al. 1986; Rheinhei.mer et aJ.
1988; Prosser 1989). ln nature, the growth rate of nitrifying bacteria is
controlled by substrate concentration, temperature, pH, and oxygen tension
(Watson et al. 1986). Most strains of nitrifying bacteria grow optimally at
substrate concentrations of 1-25mM, a pH between 7.5 and 8, and a
temperature of 25-30°C. Although nitrification is a very frequent micro-

• '''' I I·" ~•
82 0. Meyer

Depending on the environmental conditions, nitrification can prevent

nitrogen loss (if ammonia volatillzation is a major process) or lead to
nitrogen loss by the process of denitrification (the microbial reduction
of N03 - or N0.2 - to gaseous N20 or N2 ) , chemodenitrification (the
nonenzymatic loss of nitrogen through the spontaneous disproportionation
of nitrous acid to nitric acid and NO ; NO reacts with 0 2 to form N02 , which
in the presence of H 20 is transfonned to nitrous and nitric acid), and
leachi.ng of the highly water-soluble nitrate anion (Bock et aL 1989).
Nitri.fiers also occur as endolithic bacteria inhabiting the upper centimeters
of the rock walls of old buildings (Cologne cathedral, etc.), where they
produce nitric acid which attacks the building material, e.g. , dolomite
(Bock et al. l 989). Nitrosovibrio apparently is the most abundant ammonia
oxidizer at these sites (Bock et al . 1989).
The functional group of ammonia-oxidizi ng bacteria has been categorized
into the genera Nitrosomonos. Nitrosovibrio , Nitrosococcus, Nilrosospira,
and Nitrosolobus (the nitrosobacteria); the nitrite-oxidizing bacteria (the
nitrobacteria) comprise the genera Nitrooac t.er, Nitrococcus , and Nitrospira
(Watson et al. 1986).

4.5.2 Denitrification

In contrast to the nitrifying bacteria , which are strict aerobes, the denitrify-
ing bacteria have a facu ltative metabolism, i.e., they utilize nitrate and other
nitrogen oxides in place of 0 2 as terminal electron acceptors in a respiratory
type of metabolism; however, 0 2 is preferred over nitrate, if present.
Denitrification refers to tl1e dissimilatory reduction of one or both of the
ionic nitrogen oxides (nitrate, N03 -, and nitrite, N02 - ) to tJ1e gaseous
oxides (1titric oxide, NO, and nitrous oxides, N2 0), wltich may themselves
be fu rther reduced to di nitrogen (N 2} . The gaseous nitrogen specie.s are the
mai.n products of these reductive processes (Fig. 4.5). Denitrificatio n is a
major mechanism of loss of fertilizer nitrogen , resulting in a decreased
ef1iciency of fertilizer u.se. It is also important i.n the removal of nitrogen
from high-nitrogen waste materials such as animal residue.<; and an im-
portant process contributing N20 to the atmosphere, where it is involved in
stratospheric reactions which result in the depl.etion of ozone (Knowles
1982; Kaplan l984).
The functional group of denitrifying microorganisms comprises a large
number of bacteria from different taxonomi.c units. They also differ con-
siderably with respect to their substrate (electron-donor) speci.ficities.
Most denitrifyi ng bacteria are heterotrophs. The genus Pseudomonas
includes the most commonly isolated de nit.rifying bacteria from both soils
and aquatic sediments (Knowles 1982). The biochemistry and molecular
biology of denitrification have been extensively studied iu P. stutzeri and P.
perfectomarin.us (Kroneck and Zumft 1990 and literature cited therein). T he

• '''' I I·" ~•
84 0. Meyer

temperatu re are much more favorable for denitrification than in growing

forests, indicates that denitrification can compensate for the increased
atmospheric nitrogen deposition only to a smaJJ extent. It appears that forest
soils are signillcant sources of N2 0, and the N20 emission rate in a tem-
perate oak-beech forest was estimated 20 kg N20-N ha- t year- • (Tietema
et al. 1991). The N 20 emission from temperate forest soils was estimated at
0.7- 1.5Tg N year- 1 (Schmidt et al. 1988), which seems to be the largest
individuaJ source of atmospheric N 20. It appears that the formation of N2 0
by forest soils is the result of the inhibition of the N 20 reductase activity in
the indigenous denitr:ifying mi<.:rotlora by low pH values caused by acid
atmospheric deposition (Schmitt and Meyer 1992). For recent treatments of
the role of denitrification in the forest nitrogen cycle, refer to Gundersen
(1991), Struwe and Kj0Uer (1991) , Henrich and Hasselwandter (1991) and
Ineson et aJ . (1991). For a discussion of the spatial distribution of denitrifica-
tion (and nitrification) in acid forest soils, see Lensi et aL (1991) and
WiUison and Anderson (1991).

4.5.3 N2 Fixation

The assimilation of nitrogen gas (N2) into ceil material as a source of

nitrogen is called nitrogen fixation . Approximately 2.55 X 108 metric tons of
N2 are fixed annually, and microbial N2 fixation is thought to acc.ount for
approximately 70% of the totaJ N2 fixed (see tbe discussion by Gordon
(1986) and the literature cited therein) . 1lte process C-Onverts N2 to N l~ +
(Fig. 4.5) which is not liberated but instantaneously integrated into amino
acids.
Within the N2-fixing bacteria, the reduction of N2 to ammonia is catalyzed
by nitrogenas.e , which is C-Omposed of a dinitrogenase and a dinitrogenase
reductase. The reductase delivers the reducing equivalents and energy
(ATP) required for the reduction of N2 to ammonia, which .is catalyzed by
dinitrogenase. The nitrogenase reaction has an enormous requirement for
ATP and .reduciug equivalents, and Nrfixation is, therefore, very costly
for the bacteria involved. Din:itrogenases harbor a metal-sulfur c.ofactor
C-Ontaining iron as the sole metal (Fe-co, Fe-nitrogenases), iron plus
vanadium (FcVa-co, V-nitrogena:ses) , or iron plus molybdenum (FeMo-co,
Mo-nitrogeuases ).
Since the actuaJ reduction of N2 involves the participation of these
cofactors, the process of N2 fixation in natural environments has the metal
•
requirements specified . Nitrogenases exhibit a broad substrate specificity,
e.g., besides N2 tbey can reduce several analogues of N2 , e .g., HCN , HN 3 ,
CH 3NC, CH3CCH (for a full list, see Burns and Hardy 1975) of which G.!H2
(acetylene gas, which is reduced to ethylene gas) is the most famous, having
been adopted for the " acetylene test" for nitrogenase. Both components of

0:0 :!•I!• ··-···

Functional Groups o f Microorganisms 85

nitrogenase are rapidly and irreversibly inactivated by ~ . For a review

of the nitrogen cycle, nitrogenase biochemistry, genetics, physiology, and
ecology refer to Leigh and Postgate (1985) and Postgate (1989).
N2 fixation is a property of only certain bacteria and cyanobacteria
(sometimes falsely termed blue-green algae), referring to a fairly restricted
functional group. It is also important to note that N2 fixatjon is the domain
of prokaryotes and that rugher organisms (eukaryote_c;) are not capable of
carrying out that process. The ability to fix N2 is found in representatives
of numerous families of bacteria but, within these families, is generally
restricted to only certain genera , certain species, or even certain strauls. The
uneven distribution of N2 fixation has been ascribed to specific requirements
for the expression of nitrogen activity (Gordon 1986).
N2 fixation occUis in aerobic as well as anaerobic bacteria, in
cyanobacteria , phototrophic and chemotrophic bacteria. The Nrfixing
fami lies of heterocystous cyanobacteria are Nostocaceae (Anabaena,
Nostoe, etc.), Scytonemataceae, Rivula.riaceae (Calothrix , Gloeotrichia) ,
and Stigonemataceae ( Fischerellfl , etc.) ; the nonheterocystous families
are Chroococcaceae (Synechococcus , etc.) , Oscillatoriaceae (Oscillatoria,
Plectonema, Pseudoanabena, etc.), Clastidiaceae, Chroococcidiaceae, and
Hyellaceae (Pleurocapsa, Xenococcus). Families of Nr fixing phototrophic
bacteria are the RhodospiriJlaceae (Rhodospirillum, Rhodopseudomonas,
Rhodomicrobium), Chromatiaceae ( Chromatium, Ecwthiorhodospira) ,
and Chlorobiaceae (Chlorobium). Examples of families of N2-fixing chemo-
trophs are Spirillaceae (Spirillium, etc.), Azotobacteraceae (Azotobacter,
Azomonas, Beijerinckia , Derxia), Rhizobiaceae (Rhizobium), Methylo-
monadaceae (Methylosinus , Methylomonas, Methylococcus, Merhylo-
bacterium), Enterobacteriaceae (Escherichia , Citrobacter, KlebsieUa,
Ertterobacter, Erwinia) , Bacillaceae (Bacillus, Clostridium , etc.), and the
Coryneforms (Corynebacterium , Frankia). For a fuiJ List of the N2 -fixing
prokaryotes, refer to Gordon (1986). The baci.lli are an exampl.e of free-
living aerobic and the Clostridia of free-living anaerobic N2 fixers. An
association of the Nr flxing bacteria with plants provides substrates and thus
increases tbe potential for N2 fixation . The symbiosis between Rhizobium
and leguminous plan ts (clover) fixes between 150 and 200 kg N2-hectare
per year, whereas N2 .fixation rates of the free-living bacteria amount to
only one-tenth of th at or less. Another symbiosis involving morphological
adaptation by a plant host is that between various nodulated nonlegumes
such as Alnus, Myrica, Purshia, and Ceanothus and their Nrfix:i ng
endosymbioots. Lichens represent another intimate association, the fungus
providing protection from environmental stress to the Nr fixjng cyano-
bacterium. In addition, there are associations of cyanobacteria and
plants, e.g. , between the water fern A zolla and the cyanobacterium
Arwbaena azolla. The most important Nr fixing bacteria are found iu the
family Azotobacteraceae (Becking 1986) and the genus Rhizobium (Vincent
1986).
86 0 . Meyer

4.6 The Role of Microorganisms in the Biogeochemkal Cycle of Sulfur

Sulfur occurs in natural environments in inorganic and organic forms. In

soils (except arid ones) . the inorganic fraction is typically small compared
with the organic. Inorganic sulfur exists primarily as sulfate (S0 42 - ) or
sulfide (S 2 - ), in gypsum, aluminum sulfate, or various metal sulfides which
predomi.nate io the metal ores at mining areas. Inorganic sulfur compounds,
e .g. , H 2S04 , are major constituents of acid rain. Under tidal-marsh and
saline-lake conditions, sulfur accumulates mainly as sulfides and polysuHides
of iron (Paul and Clark 1989). The total sulfur content of a tidal marsh is
3- 3S mgg- 1, of agricultural soil 0.025- 0.54 mgg- 1, and of forest soil 0. 162-
2.328 mg g- 1 (Paul and Clark 1989). Biological material contains organic
forms of sulfur. Examples are sulfur-containing amino acids (e.g. , cysteine,
cystine , methionine) , iron-sulfur proteins (e.g., nitrogenase, carbon
monoxide dehydrogenase, hydrogenase, pyruvate dehydrogenase), cofactors
and coenzymes (e.g., coenzyme A , lipoic acid , U1iamine, bioti n, molybdenum
cofactor, i.rou-molybdenurn cofactor); the sulfatophosphates (adenosine 5' -
sulfatophosphate , adenosin 3' -phosphate 5' -sulfatophosphatc) are engaged
in assimilatory a.nd dissimilatory sulfate reductions.
Sulfur is essential for ilie nutrition of all microorganisms. In addition,
specialized functional groups of bacteria make use of inorganic sulfur com-
pounds for dissimilation (generation of energy) and thereby establish the
biogeochemical cycle of sulfu r in nature (Fig. 4.6) . Reduced inorganic sulfur
(S 2 - , S0) is oxidized by aerobic bacteria (mainl y thiobaciUi) to yield sulfuric
acid . U nder anaerobic conditions, oxidized sulfur compounds (mainly sulfate,
S04 2- , and eleme ntal sulfur, S0) are reduced to hydrogen sulfide (H 2S) by
functional groups of dissimilatory sulfate- and sulfu r-reducing bacteria.

4.6.1 The Oxidation of Reduced Sulfur Compounds

In principle, any inorganic exergonic oxidation reaction might be expected

to be the basis of the energy-conserving metabolism of a chemolithotrophic
microorganism provided (i) the reaction can drive the synthesis of ATP or
build up a membrane potential and (i.i) the conditions during geological time
had been suitable for the evolution and selection of enzyme systems and
microorganisms using the reaction (see discussion by Kelly 1986). Reduced
inorga nic sulfur compounds contain sufficient energy to support the growth
of the members unified in t.he functional group of strictl y aerobic, sulfur-
oxidizing bacteria (the reaction enth<tlpies have been adopted from Ke!Jy
1986):
H2S + 0.50 2 ~ S0 + H20 (- 210k1)
S0 + :I .502 + 1-120 ---+ H4 S04 ( - 496 kJ)
Hs- + 20 2 ---+ sol - + H + ( - 71.6 kJ)
s. o 32- + 20 2 + H2o ---+ 2S042 - + 2H + (- 936 k:J) .
Functional Groups of Microorganisms 87

SulhcJe ancl elemental

SUlfur OXIC3I>On (aetOO<C)

Photouoprne t>actena
(aM eJob!C)

SO4 ~. SO 2· ~:r>te SUI!ate

.; reoucron ~IICI111()1'1
. ... ot>oc """

Sulfate reducrion Sulfur reduction

s~;-. -- - so_.--
-- . .. - .. . .
Oc:svtfuf .Cat ~n
L----
(anaerObJC}

Fig. 4.6. Functional groups of microorganisms in the biogeochemica l cycle of sulfur. For
deta ils, see Fig. 4.3

In the presence of air, reduce.d sulfur is oxidized through a variety of

intermediates by microbial (and chemical) pathways (Fig. 4.6). Oxidation
states range from +6 in SOl - to + 4, + 2, 0, and - 2 in H~ and its
derivatives. Oxidation of sulfur in soils generates acidity (H 2S04 ) , and
depending on the type of soiJ , this may have either a positive or negative
effect on the whole soil environment. Iu the bacterial oxidatio n of iron
sulfides, ferric iron is produced by the oxidation of ferrous minerals. Soluble
ferric iron acts as an electron accepto r for the chemical oxidation of sulfide
minerals. The role of the iron-oxidizing thiobacilli is then to reoxidiz.e
the reduced electron carrier, ferrous iron. The sulfuric acid increases the
solubility of the iron ions, thereby accelerating the rate of metal solubiliza-
tion (Dispirit.o and T uovinen 1984). The use of acidophilic thiobacilli and
other sulfur-oxidizing microorganisms in the mining industry (microbial
leaching) for improving the yield of various metals from sulfide ores, e.g. .
sulfides of Fe , Zn, Ni, Co, U , Cu, Sn (Dispirito and Tuovinen 1984) and the
desulfurization of coal (Dugan 1984) is well-known. As discussed by Riviere
and Schmidt ( 1986), the sulfur deposits that are mined tod ay are biogenic
and have been formed by sulfate reduction followed by an oxidation step
which may have involved colorless sulfur bacteria. Furthermore, sulfide

" •.• h• ....