Carbon Dioxide Populations and Communities

Carbon Dioxide, Populations, and Communities

Carbon Dioxide, Populations, and Communities

This is a volume in the PHYSIOLOGICAL ECOLOGY series Edited by Harold A. Mooney

Carbon Dioxide, Populations, and Cornrnunities Edited by

Christian Korner Botanisches lnstitut der Universitat Basel Basel, Switzerland

Fakhri A. Bazzaz Department of Organismic and Evolutionary Biology Harvard University Cambridge, Massachusetts

Academic Press San Diego

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This book is printed on acid-free paper. Copyright 9 1996 by ACADEMIC PRESS, INC. All Rights Reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopy, recording, or any information storage and retrieval system, without permission in writing from the publisher.

Academic Press, Inc. A Division of Harcourt Brace & Company 525 B Street, Suite 1900, San Diego, California 92101-4495

by Academic Press Limited 24-28 Oval Road, London NW1 7DX Library of Congress Cataloging-in-Publication Data Carbon dioxide, populations, and communities / edited by Christian KOrner, Fakhri A. Bazzaz. p. cm.-- (Physiology ecology series) Includes bibliographical references (p. ) and index. ISBN 0-12-420870-3 (alk. paper) 1. Plants, Effect of atmospheric carbon dioxide on. 2. Atmospheric carbon dioxide--Environmental aspects. 3. Plant communities. 4. Plant ecophysiology. I. KSrner, Christian. II. Bazzaz, F. A. (Fakhri) A.) III. Series: Physiological ecology. QK753.C3C38 1996 581.5'222--dc20 96-33959 CIP

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Contents

Contributors Preface xix

xiii

Part Population-Level

I Responses

I. II. III. IV.

Introduction 3 The Genetic Bases for Evolutionary Responses to Climate Change Thermal Sensitivity and Evolutionary Responses to Climate Change Summary 11 References 12

I. II. III. IV.

Introduction 13 Experimental Methods Results and Discussion Conclusions 20 References 21

References

30

15 17

4 7

I. Plant Responses to Environmental Change: Theory and Review of Previous Work 31 II. An Experiment to Test Genotypic Responses to Increased CO2 38 III. Results from the Experiment and Discussion 39 IV. Outlook 47 V. Summary 48 References 49

I. II. III. IV. V. VI.

Introduction 51 54 Genetic Variability in C O 2 Responses Effects of Elevated CO2 on the Selection Process 61 What Characters Will Be Selected? 68 Possible Effects of Evolutionary Changes on Ecosystem Processes Summary 74 References 75

Part I I Commtmity-Level

Responses

I. II. III. IV. V.

Introduction 85 Current Vegetation Changes in Western Europe 86 Plant Functional Types and Response to Elevated CO2 Feedbacks 89 Summary 91 References 91

I. II. III. IV. V.

Introduction 93 Methods 94 Results 96 Discussion 97 Summary 98 References 99

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73

I. II. III. IV.

Introduction 10l Responses at the Level of the Individual 102 Responses at the Level of the Plant Community Conclusions and Recommendations 118 References 119

I. II. III. IV. V.

Introduction 123 The Experimental Designs 124 Species Responses within Community Ecosystem Responses 127 Discussion and Conclusion 131 References 136

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126

Community Microcosms I. II. III. IV. V. VI.

Introduction 139 The Jasper Ridge CO2 Experiment Methods 142 Analysis 144 Results 145 Discussion 151 References 155

140

I. Introduction 159 II. Design of CO2 and Plant Diversity Treatments in Calcareous Grassland Communities 160 III. Response of Calcareous Grassland Communities to Manipulations of CO2 and Plant Diversity 164 IV. Discussion 166 V. Summary 173 References 174

I. II. III. IV.

Introduction 177 CO2 and Vegetation Change Conclusions 188 Summary 189 References 190

I. II. III. IV. V.

Introduction 197 Site Description and Methodology 198 The Response of Primary Producers 200 Other Trophic Levels 203 Conclusions 204 References 205

I. II. III. IV. V.

Introduction 209 Experimental Setup and Methods Results 216 Discussion 221 Summary 226 References 227

I. II. III. IV. V. VI.

Introduction 231 The Role of Fire in Plant Communities 232 CO2 Effects on Vegetation and Fire 235 Predicting High CO2 Effects on Future Fire Cycles Research Priorities 243 Summary 244 References 245

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211

241

Part I I I Interactions

Organismic

I. Introduction 253 II. The Symbiotic N z Fixation: A Highly Flexible Way to Assimilate Nitrogen 254 III. The Link between Plant Growth, Nitrogen Assimilation, and N 2 Fixation 255 IV. The Link between Elevated CO2 and N Availability in the Soil 255 V. The Response of Symbiotic N 2 Fixation to Elevated CO2 in the Field: A Response to Both Increased Legume N Demand and Increased Strength of the Ecosystem N Sink? 258 VI. Model and Conclusion 259 VII. Summary 260 References 261

I. II. III. IV.

Introduction 265 Responses of Symbiotic Fungi to a COz-Enriched Environment Community and Ecosystem Level Consequences 268 Summary 271 References 272

I. Introduction 273 II. Survey of Differential Species Responses within Species Mixtures Exposed to Elevated CO2 275 III. Conclusions 282 References 284

266

I. II. III. IV.

Introduction 287 Materials and Methods Results and Discussion Summary 297 References 298

I. II. III. IV. V. VI. VII. VIII.

288 289

Introduction 301 Theory 301 An Experimental Test 303 Temperature, Phenology, and Competition 311 Species Competitive Abilities 313 Competition and Internal Plant Nutrient Status 314 Longer Term Implications 314 Summary 315 References 316

I. Introduction 319 II. Shade Tolerance of Spruce Seedlings and Some Co-occurring Grasses at Ambient and Elevated CO2 Concentration in Air 320 III. Interaction between Spruce Seedlings and at Ambient and Elevated CO2 327 IV. Conclusions 329 References 330

I. II. III. IV. V.

Introduction 333 Developmental Patterns and Competitive Ability 334 Predicting the Effect of Elevated CO2 on Development 336 Effect of Developmental Patterns on CO2 Responsiveness 341 Summary 344 References 345

I. II. III. IV. V. VI.

Introduction 347 Direct Effects of CO2 349 Interactive Effects: CO2 and Resource Availability 353 Indirect Effects: CO2 and Climate 354 Tritrophic Interactions 355 Predicting Insect Outbreaks: The Functional Attribute Approach 356 VII. Conclusions and Recommendations 357 References 359

I. II. III. IV. V.

Introduction 363 Ruminant Digestion 364 Impact of Elevated CO2 on Forage Quality 366 Impact of Elevated CO2 on Cattle Production in Tallgrass Prairie Conclusions 369 References 370

Part IV Theory, Modeling, Concepts

I. II. III. IV. V. VI.

The Need for Functional Types 375 Methodological Aspects 376 Interspecific Variation 380 Differences between Species at Low N Levels Ecological Aspects 390 Summary 391 References 406

I. Introduction 413 II. Light Interception in Mixed Species Stands

389

414

367

xii

III. Effect of CO2 Elevation on the Canopy Development in Two Annuals 418 IV. Nitrogen Allocation and Optimal Leaf Area Index under Elevated CO2 420 V. Summary and Conclusion 426 References 428

I. II. III. IV. V.

Introduction 431 Extrapolation 432 Reductionism from Below 434 Two Approaches to Research on Elevated CO2 Prediction and Uncertainty 439 References 440

I. II. III. IV. V. VI. VII. VIII. IX.

Index

Introduction 443 Why Study Variance? 444 Genotypic Responses in Populations 445 Responses of Plant Communities 446 Plant-Plant Interactions 449 Plant-Microbe Interactions 451 Plant-Animal Interactions 451 Theory, Modeling, Concepts 452 Ecosystem and Global Consequences 453 References 455 457

436

Contributors

on

D. D. Aekerly (413), Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138 John A. Arnone III (101), Institute of Botany, University of Basel, CH-4056 Basel, Switzerland Lisa M. Auen (363), Department of Agronomy and Department of Animal Science and Industry, Kansas State University, Manhattan, Kansas 66506 F. A. Bazzaz (413, 443), Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138 A. Birrer (31), Institut for Umweltwissenschaften, Universit~it ZOrich, CH8057 Zfirich, Switzerland L. O. Bj6rn (197), Department of Plant Physiology, University of Lund, Lund S-22100, Sweden Herbert Blum (253, 287), Institute of Plant Sciences, Swiss Federal Institute of Technology, 8092 Zfirich, Switzerland T. V. Callaghan (197), Department of Animal and Plant Sciences, The Centre for Arctic Ecology, The University of Sheffield, Sheffield $10 5BR, United Kingdom Bruce D. Campbell (301,375), AgResearch, Grasslands Research Centre, Palmerston North, New Zealand Nona R. Chiariello (139) ,Jasper Ridge Biological Preserve, Stanford University, Stanford, California 94305 Robert C. Cochran (363), Department of Animal Science and Industry, Kansas State University, Manhattan, Kansas 66506 Peter S. Curtis (13), Department of Plant Biology, The Ohio State University, Columbus, Ohio 43210 Paolo De Angelis (209), Department of Forest Environment and Resources, University of Tuscia, 1-01100 Viterbo, Italy Shivcharn Dhillion 1 (123), Centre d'Ecologie Fonctionnelle et Evolutive, Centre de la Recherche Scientifique, F-34033 Montpellier, France Christopher B. Field (139, 443), Department of Plant Biology, Carnegie Institution of Washington, Stanford, California 94305 1 Present Address: Department of Biology and Nature Conservation, Agricultural University of Norway (NLH), .3ts N-1432, Norway.

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Beret Fischer (253), Institute of Plant Sciences, Swiss Federal Institute of Technology, 8092 ZOrich, Switzerland Marco Frehner (253), Institute of Plant Sciences, Swiss Federal Institute of Technology, 8092 Z/irich, Switzerland C. Gehrke (197), Department of Plant Ecology, University of Lund, Lund S-223 62, Sweden; and Abisko Naturvetenskapliga Station, Abisko S98107, Sweden Jan Gloser (319), Department of Plant Physiology, Faculty of Science, Masaryk University, 61137 Brno, Czech Republic J. P. Grime (85), NERC Unit of Comparative Plant Ecology, Department of Animal and Plant Sciences, The University of Sheffield, Sheffield $10 2TN, United Kingdom Jean-Louis Gtdllerm (123), Centre d'Ecologie Fonctionnelle et Evolutive, Centre de la Recherche Scientifique, F-34033 Montpellier, France D. Gwyrm-Jones (197), Department of Animal and Plant Sciences, The Centre for Arctic Ecology, The University of Sheffield, Sheffield S10 5BR, United Kingdom Alan L. Hart (301), AgResearch, Grasslands Research Centre, Palmerston North, New Zealand Ueli A. Hartwig (253, 287), Institute of Plant Sciences, Swiss Federal Institute of Technology, 8092 Z~rich, Switzerland Thomas Hebeisen (253, 287), Institute of Plant Sciences, Swiss Federal Institute of Technology, 8092 Z~rich, Switzerland George R. Hendrey (253, 287), Department of Applied Science, Brookhaven National Laboratory, Upton, Long Island, New York 11973 T. Hirose (413), Biological Institute, Faculty of Science, Tohoku University, Aoba, Sendai 980-77, Japan M. Jasiefiski (51), Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138 U. Johanson (197), Department of Plant Physiology, University of Lund, Lund S-22100, Sweden Hyrum B.Johnson (177), United States Department of Agriculture, Agricultural Research Service, Grassland, Soil & Water Research Laboratory, Temple, Texas 76502 T. Herin Jones (93), NERC Centre for Population Biology, Imperial College at Silwood Park, Ascot, Berks SL5 7PY, United Kingdom Susan Kalisz2 (13), Kellogg Biological Station, Michigan State University, Hickory Corners, Michigan 49060 Joel G. Kingsolver (3), Department of Zoology, University of Washington, Seattle, Washington 98195 Present Address: Department of Biological Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania 15260.

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Dawn Jenkins Klus (13), Kellogg Biological Station, Michigan State University, Hickory Corners, Michigan 49060 Ch. K6rner (159, 443), Institute of Botany, University of Basel, 4056 Basel, Switzerland Elena Kuzminsky (209), Department of Forest Environment and Resources, University of Tuscia, 1-01100 Viterbo, Italy C. Lavigne (31), Institut for Umweltwissenschaften, Universit~it Ziirich, CH8057 ZCtrich, Switzerland Sharon P. Lawler ~ (93), NERC Centre for Population Biology, Imperial College at Silwood Park, Ascot, Berks SL5 7PY, United Kingdom John H. Lawton (93), NERC Centre for Population Biology, Imperial College at Silwood Park, Ascot, Berks SL5 7PY, United Kingdom Paul W. Leadley (159), Botanical Institute, University of Basel, 4056 Basel, Switzerland J. A. Lee (197), Department of Animal and Plant Sciences, The University of Sheffield, Sheffield S10 2UQ, United Kingdom Richard L. Lindroth (347), Department of Entomology, University of Wisconsin, Madison, Wisconsin 53706 Andreas L/iseher (253, 287), Institute of Plant Sciences, Swiss Federal Institute of Technology, 8092 Ziirich, Switzerland Giorgio Matteueci (209), Department of Forest Environment and Resources, University of Tuscia, 1-01100 Viterbo, Italy Herman S. Mayeux (177), United States Department of Agriculture, Agricultural Research Service, Grassland, Soil & Water Research Laboratory, Temple, Texas 76502 Shahid Naeem 4 (93), NERC Centre for Population Biology, Imperial College at Silwood Park, Ascot, Berks SL5 7PY, United Kingdom Marie-Laure Navas 5 (123), Centre d'Ecologie Fonctionnelle et Evolutive, Centre de la Recherche Scientifique, F-34033 Montpellier, France Josef N6sberger (253, 287), Institute of Plant Sciences, Swiss Federal Institute of Technology, 8092 Z/irich, Switzerland Clenton E. Owensby (363), Department of Agronomy, Kansas State University, Manhattan, Kansas 66506 H. Wayne Polley (177), United States Department of Agriculture, Agricultural Research Service, Grassland, Soil & Water Research Laboratory, Temple, Texas 76502 3Present Address: Department of Entomology, Universityof California, Davis, Davis, California 95616. 4Present Address: Department of Ecology, Evolution, and Behavior, Universityof Minnesota, St. Paul, Minnesota 55108. 5Present Address: CEFE and Biologie et Pathologie V6g6tale, ENSA-M,F-34060 Montpellier, France.

• Hendrik Poorter (375), Department of Plant Ecology and Evolutionary Biology, Utrecht University, 3508TB Utrecht, The Netherlands Catherine Potvin (23), Department of Biology, McGill University, Montr6al, Qu6bec H3A 1B1, Canada E. G. Reekie (333), Biology Department, Acadia University, Wolfville, Nova Scotia BOP 1X0, Canada Heather L. Reynolds (273), W. K. Kellogg Biological Station, Michigan State University, Hickory Corners, Michigan 49060 Catherine R0umet (375), Centre d'Ecologie Fonctionelle et Evolutive, Centre National de la Recherche Scientifique-Centre Louis Emberger, 34033 Montpellier, France Jacques Roy (123), Centre d'Ecologie Fonctionnelle et Evolutive, Centre de la Recherche Scientifique, F-34033 Montpellier, France Rowan F. Sage (231), Department of Botany, University of Toronto, Toronto, Ontario M5S 3B2, Canada Ian R. Sanders (265), Institute of Botany, University of Basel, CH-4056 Basel, Switzerland Giuseppe E. Scaraseia-Mugnozza (209), Department of Forest Environment and Resources, University of Tuscia, 1-01100 Viterbo, Italy B. Schmid (31), Institut for Umweltwissenschaften, Universit~it Zfirich, CH8057 ZOrich, Switzerland M. Sonesson (197), Department of Plant Ecology, University of Lund, Lund S-223 62, Sweden; and Abisko Naturvetenskapliga Station, Abisko S-98107, Sweden S. C. Thomas (51), Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138 LindseyJ. Thompson (93), NERC Centre for Population Biology, Imperial College at Silwood Park, Ascot, Berks SL5 7PY, United Kingdom Charles R. Tisehler (177), United States Department of Agriculture, Agricultural Research Service, Grassland, Soil & Water Research Laboratory, Temple, Texas 76502 StephenJ. Tonsor 6 (13), Kellogg Biological Station, Michigan State University, Hickory Corners, Michigan 49060 Denise Tousignant 7 (23), Department of Biology, McGill University, Montr6al, Qu6bec H3A 1B1, Canada Chris Van Kessel (253), Department of Soil Science, University of Saskatchewan, Saskatoon, Saskatchewan S7N 0W0, Canada Present Address: Department of Biological Sciences, Universityof Pittsburgh, Pittsburgh, Pennsylvania 15260. 7 Present Address: Ministere des ressources naturelles, Peponiese St. Modeste, St-Modeste, Quebec J0L 3W0, Canada.

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Jacob Weiner 8 (431), Biological Laboratories, Harvard University, Cambridge, Massachusetts 02138 Richard M. Woodfin (93), NERC Centre for Population Biology, Imperial College at Silwood Park, Ascot, Berks SL5 7PY, United Kingdom SUvia Zanetti (253, 287), Institute of Plant Sciences, Swiss Federal Institute of Technology, 8092 ZCtrich, Switzerland

8 Present Address: Department of Biology, Swarthmore College, Swarthmore, Pennsylvania 19081.

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Preface

In many aspects of biological science, variance is considered a nuisance. Variance makes experimental design difficult, requires much replication and detailed statistical analysis, and may greatly increase the need for expensive research facilities beyond the reach of many investigators. The results of some critical experiments may be statistically insignificant because of low replication. Consequently, many researchers in plant sciences, including those investigating CO2, have attempted to eliminate variance by cloning plants or by working with a small set of individuals and assuming that they represent the species. On the other hand, some researchers consider assemblages of plants and treat whole plant communities as a single "big leaf." In many of these cases, these smooth results and their mean values eliminate variance among individuals in the populations, which is the material for natural selection and evolution. Variance in response among individuals and species may be the most important aspect to consider in predicting the vegetation response to the continued enrichment of the atmosphere with CO2. Because of the speed with which CO2 in the atmosphere is increasing (~1.8 ppm/year), there is little time for the evolution of a new set of genotypes specifically adapted to this new global level of CO2 in the atmosphere. Therefore, it is the current genetic structure of populations that will determine the response of plants to elevated levels of CO2, especially in long-lived woody or clonal plants. Research on the response of a variety of plant species over the past two decades has convincingly shown that species do differ in their response to CO2. These differences can be very large, even among co-occurring species of a community. It is also well established that genotypes within a population differ in their response to CO2 enrichment. Thus, in a changing CO2 environment there may be winner (positively responding) and loser (less responding) individuals or species. This differential response may be underway already. Furthermore, this differential response may determine the genetic structure of future populations, may change the dominance relationship in communities, and thus may alter the importance of some plant functional groups, which may have feedbacks on the functioning of ecosystems. It may also influence biological diversity of some ecosystems. We must remember, however, that under natural conditions, selection by one xix

factor may not be the case, as factors of the physical and the biological environment interact in a variety of ways and may collectively influence the direction and the strength of selection. For example, CO2 enrichment may increase the water-use efficiency of a species or a genotype, providing access to more soil moisture to its otherwise less efficient neighbor, which in turn may offer the preferred food for a butterfly that may be an important pollinator for a third species. Scientists concerned about the global increase in CO2 met in the hills of the SwissJura Mountains in August 1994 and discussed the topics in this volume. They emphasized the need for a better understanding of the differences among individuals and of interactions among themselves a n d with other organisms. They sought to identify critical questions in this research area. This meeting represents one of the major steps in the Global Change and Terrestrial Ecosystems (GCTE) research plan, and its outcome is intended to complement that of the preceding workshop on ecosystem response to elevated CO2, the results of which appeared last year in this series. We gratefully acknowledge the support of the Swiss National Science Foundation, the Swiss Academy of Sciences, the United States Electric Power Research Institute (EPRI), and the United States National Science Foundation. The Leuenberg Conference Center near Basel provided a charming environment for this workshop. CH. KORNER

F. A. BAZZAZ

I Population-Level Responses

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1 Physiological Sensitivity and Evolutionary Responses to Climate Change

The global changes in C O 2 and climate expected to occur during the coming decades are but one of many types of environmental changes resulting from human activities during the past century. The ecological and evolutionary consequences of pollution, pesticides, heavy metals, and other environmental insults during the past 40 years have been well documented. It is natural to ask whether and how the lessons we have learned from such studies may be used to anticipate the evolutionary consequences of future climate change for populations and species. In this chapter I will argue that the evolutionary consequences of climate change may differ importantly from those documented by field studies of pesticides and many other environmental toxins for a rather simple reason: pesticides represent an abrupt step-change in the environment, whereas climate change represents a progressive, directional alteration of environmental conditions. To illustrate this point, I will suggest and defend two conjectures about the evolutionary consequences of climate change: 1. The evolutionary responses of populations and species to climate change will involve polygenic, not monogenic, genetical responses. 2. Species whose individuals have broad physiological tolerances to climatic conditions will be less able to adapt evolutionarily to rapid and

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Copyright 9 1996 by Academic Press, Inc. All rights of reproduction in any form reserved.

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climate change than those species whose individuals have intermediate tolerances. For the sake of discussion, I will argue these points with greater confidence than is perhaps warranted. My goal, however, is to show how lessons learned from the evolution of pesticide resistance and from quantitative genetic models of physiological sensitivity may provide some useful guidelines for evolutionary studies of climate change.

Most discussions of the biological consequences of climate change have downplayed any potential role for evolution, arguing that the predicted rapid rate of climate change will preclude evolutionary responses: species will either adjust ecologically or become extinct. It is certainly true that the relatively long generation times and small effective population sizes of many trees and large vertebrates make evolutionary responses to future climate change, which may occur on time scales of one to several decades, ineffective. However, the long history of studies of the evolution of resistance to pesticides and heavy metals clearly demonstrates that evolutionary responses to environmental changes can be rapid indeed in species of interest to humans. It is more useful to ask in what cases rapid evolution is likely to be important. First, rapid evolution is most likely in populations with large population sizes (e.g., >105-106), with short generation times (e.g., <1 year), and with high intrinsic rates of increase (e.g., rm > 0.5/generation). Thus, evolutionary responses to climate change may be quite likely in pest species. Second, rapid evolution is more likely when migration and dispersal are geographically restricted. Thus, evolutionary adaptation to climate change may be of importance in nature reserves and on other habitat islands, where the diluting effects of gene flow are reduced and where range shifts into new areas may be constrained.! geographically. Studies of the evolution of insecticide resistance in insect pests provide some useful insights into the possible genetic bases for evolutionary responses to climate change. A key question is whether evolutionary adaptation to climate change is more likely to involve a few major gene loci of large effect (monogenic), or many gene loci each of small effect (polygenic). Although the genetic basis for insecticide resistance has been intensively studied since the 1950s (Crow, 1957), the early studies appeared to be conflicting. Only in the last decade has a clear pattern in this literature been suggested: most laboratory studies, in which artificial selection is used

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to select for resistance from an initially susceptible population, indicate a polygenic basis for resistance. Conversely, many field studies, in which resistant genotypes are sampled from a population that has experienced frequent heavy insecticide doses, indicate a monogenic basis for resistance (Roush and McKenzie, 1987). The example of diazinon resistance in sheep blowflies is instructive (McKenzie and Batterman, 1994). Diazinon was widely used in Australia to control sheep blowflies, which rapidly evolved resistance to this insecticide. Genetic studies showed that this resistance was the result of the same allelic substitution at a single locus in different populations; and this resistant genotype was maintained near fixation during two decades of routine application of diazinon in the field. Subsequently, four populations of resistant blowflies were established in the laboratory and subjected to artificial selection for further increases in resistance. Within eight generations, more highly resistant strains had been developed, and genetic analyses showed that the increased resistance was due to multiple loci on at least four chromosomes. Thus, while two decades of field selection resulted only in monogenic evolutionary changes, laboratory selection led quickly to polygenic responses (McKenzie and Batterman, 1994). What causes these differing evolutionary responses both in the laboratory and in the field? The best current explanation is that the evolutionary response may depend on the intensity of selection (Roush and McKenzie, 1987; McKenzie and Batterman, 1994). Consider a laboratory population undergoing artificial selection for increased resistance to an insecticide (Fig. 1, top). During artificial selection, the intensity of selection (i.e., the fraction of the population killed by selection) must be chosen such that surviving individuals form a population sufficiently large to avoid substantial inbreeding and subsequent drift. Typically the insecticide dosage is chosen to achieve a selection intensity less than 80-90%, even for relatively large laboratory populations (103-104). As a result, selection occurs within the range of existing genetic variation in resistance in the population, which is often the result of many loci. The situation in the field is quite different. Here frequent and heavy doses are traditionally used to eliminate the entire pest population, and selection in this case could exceed 99% or more (Fig. 1, bottom). Even in large pest populations, only the rare individual with a mutant allele of large effects on resistance would be likely to survive. Because these rare alleles would only appear initially in heterozygotes, such alleles would need to be partially or fully dominant to be expressed. Such resistant alleles frequently have deleterious pleiotropic effects in the absence of insecticides, hence their initial rarity. Thus the very high insecticide doses, and hence the high selection intensity, typical of the field situation may have selected for resistance caused by one or a few alleles of larger effect.

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Figure I (Top) The distribution on the left (BEFORE) represents the distribution ot susceptible phenotypes within a population of insects before selection. When an insecticide dosage (Selection intensity, dashed line) is applied, only those individuals with resistances greater than the applied dosage (to the right of the dashed line) will survive. After repeated generations of selection, the distribution of phenotypes in the population will shift to the right as a result of evolution (AFFER). These selective conditions, typical of artificial selection studies in the laboratory, may preferentially select for a polygenic response. (Bottom) The distribution on the left (BEFORE) represents the distribution of susceptible phenotypes within a population of insects before selection. When a high insecticide dosage (Selection intensity, dashed line) is applied, only those individuals possessing mutations with large effects on resistance to the insecticide will survive. After repeated generations of selection favoring rare mutants of large effect on insecticide resistance, the distribution of phenotypes in the population will shift far to the right as a result of evolution (AFTER). These selective conditions, typical of insecticide applications in the field, may preferentially select for a monogenic response. Adapted from McKenzie and Batterman (1994), Fig. 1. T a b a s h n i k (1995) a r g u e s t h a t this d i c h o t o m y b e t w e e n m o n o g e n i c field r e s i s t a n c e a n d p o l y g e n i c l a b o r a t o r y r e s i s t a n c e is t o o simplistic. H e s u g g e s t s t h a t t h e e v i d e n c e t h a t r e s i s t a n c e typically h a s a m o n o g e n i c basis in t h e field is e q u i v o c a l a n d t h a t s o m e o f t h e m o s t t h o r o u g h s t u d i e s o f r e s i s t a n c e d o n o t fit n e a t l y i n t o e i t h e r t h e m o n o g e n i c o r p o l y g e n i c e x t r e m e s . F o r o u r p u r p o s e s , h o w e v e r , t h e p o i n t is t h a t m o r e g r a d u a l s e l e c t i o n is m o r e likely to s e l e c t o n e x i s t i n g q u a n t i t a t i v e v a r i a t i o n in r e s i s t a n c e in a p o p u l a t i o n a n d t h a t t h e c o n d i t i o n s o f s e l e c t i o n c a n i n d e e d i n f l u e n c e t h e g e n e t i c basis of resistance.

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What might this suggest for evolutionary responses to climate change? One characteristic of global climate change is that it will not occur in an abrupt step, but as a gradual, directional increase in CO2 and temperature. To those organisms most likely to respond evolutionarily--those with relatively short generation times and large population sizes--such gradual changes are likely to generate selection intensifies per generation more similiar to laboratory artificial selection regimes than to the extremes seen in field insecticide applications. Thus we might predict that the evolutionary responses to climate changes will involve primarily polygenic, not monogenic, control. One implication of this suggestion is that experimental studies exploring evolutionary responses to climate change need to consider the type of environmental change and the selection intensity imposed on the study population. In particular, studies that utilize abrupt step-changes in CO2 or temperature may affect the type of genetic responsesmpolygenic or m o n o g e n i c - - t h a t occur, in ways that do not accurately reflect the rates of change predicted from global climate change (see Tousignant and Potvin, Chapter 3). Again, the key issue is whether or not the imposed environmental change falls within the range of the existing genetic variation in the population. The notion that step-changes and progressive directional changes in the environment may yield qualitatively different responses has not received much attention. To further explore the importance of these differences, I will briefly discuss some recent models that address the question how does the physiological tolerance of individuals in a population affect the population's evolutionary response to selection?

One useful way to characterize the effects of temperature or other physical factors on the performance or fitness of an individual organism is in terms of a which maps environmental conditions onto physiological or ecological performance (Fig. 2). (For convenience I will focus on temperature effects throughout this secdon, but the basic ideas should apply to most other physical factors.) Performance initially increases with temperature, reaches some "optimal" temperature for performance, then declines rapidly as it approaches upper lethal levels. Frequently one can characterize the performance curve in terms of three parameters: optimal temperature (Z), the temperature at which performance is maximum; performance breadth (~r), the breath or width of the performance curve; and the maximum performance (Rmax), the level of performance at

Rmllx

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Z ENVIRONMENTALTEMPERATURE Thermal performance curves illustrating the relationship between an individual's performance (assumed directly proportional to fitness) and the environmental temperature it experiences. For each individual, there is an optimal temperature (Z) at which performance is maximized (Rmax).Performance curves are given for two individuals with identical optimal temperature (Z) and maximal performance (Rmax),but that differ in thermal performance breadth (tr). Adapted from Huey and Kingsolver (1989).

the optimal t e m p e r a t u r e (Fig. 2). We shall assume that the measure of p e r f o r m a n c e chosen is directly related to fitness. O n e natural question is how do the values of these parameters affect the ecological and evolutionary response to climate change (e.g., climate warming) ? Suppose we consider two individuals with identical Z and Rmax, but that differ in p e r f o r m a n c e breadth t r m t h a t is, one is a thermal " specialist" (small tr), the other a thermal "generalist" (large tr) (Fig. 2). Suppose the environmental t e m p e r a t u r e 0 is initially the same as Z, but then 0 increases somewhat. Obviously the reduction in p e r f o r m a n c e (and hence the reduction in fitness) of the thermal generalist is less (Fig. 2). Similarly, a population of thermal generalists will suffer a smaller decline in m e a n fitness than a population of thermal specialists in the face of a small increase in environmental temperature. Clearly, thermal generalists are at an ecological advantage in the face of climate warming. But how does thermal p e r f o r m a n c e breadth affect the evolutionary response of a population to sustained, directional climate warming? We have recently e x a m i n e d this question (Huey and Kingsolver, 1993), modifying a quantitative genetic m o d e l developed by Lynch and Lande (1993) (see Fig. 3). The p e r f o r m a n c e curve identifies the optimal t e m p e r a t u r e (Z) and thermal p e r f o r m a n c e breadth (tr) of each individual (Fig. 2). Suppose that optimal t e m p e r a t u r e Z is now a polygenic trait with some constant phenotypic and genetic variation in the population, but that all individuals

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Diagram illustrating the effect of thermal performance breadth on a population's evolutionary response to climate warming. Here f(Z) is the frequency distribution of phenotypic trait Z, the optimal temperature for performance. In each panel, the solid line represents the change in environmental temperature (0), and the dashed line represents the change in the population mean value of Z with time. As time proceeds, a lag develops between the environmental optimum and the population mean phenotype. For populations with large thermal performance breadths (top), this lag will be greater than for populations with small performance breadths (bottom). From Huey and Kingsolver (1993), Fig. 5.

in the p o p u l a t i o n (with fixed, constant, effective p o p u l a t i o n size) have identical p e r f o r m a n c e b r e a d t h (t r) a n d m a x i m u m p e r f o r m a n c e (Rma~). Initially the e n v i r o n m e n t a l t e m p e r a t u r e 0 is at t h e m e a n o p t i m a l t e m p e r a ture Z o f the p o p u l a t i o n ; 0 t h e n increases at a c o n s t a n t m e a n rate, b u t with s o m e stochastic ( r a n d o m ) variation. Given this situation, t h e m e a n o p t i m a l t e m p e r a t u r e Z o f t h e p o p u l a t i o n will evolve toward increasingly h i g h e r values, b u t will lag b e h i n d the e n v i r o n m e n t a l t e m p e r a t u r e (Fig. 3). m

0 If the rate of climate warming is too rapid, the population's lag will become too great, its mean fitness will approach zero, and extinction will occur. Hence one can identify a critical rate of climate change above which population extinction will quickly occur (Fig. 3). Using this model, we can address how performance breadth affects the critical rate of climate change that a population can sustain. Consider the simplest case in which the genetic variation in optimal temperature Z in the population is constant with rime and independent of performance breadth. The model then predicts that the critical rate of climate change will initially increase with increasing performance breadth, quickly reach a maximal value, and then decline with increasing performance breadth (Fig. 4). Thus the model predicts that populations with intermediate performance breadths will be able to sustain the highest rates of climate c h a n g e - that populations of thermal generalists are more likely to become extinct in the face of rapid climate change. Stochastic variation in climate decreases the critical rate of change and increases the performance breadth at which the rate is maximal, but does not alter the qualitative result (Fig. 4). Interestingly, these results do not depend on the existence of tradeoffs between specialists and generalists (Huey and Kingsolver, 1993). What produces this apparently paradoxical result? The key once again is the importance of the intensity of selection. For a population of thermal

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3 Theoretical predictions of the critical rate of climate change (in ~ above which population extinction will occur, as a function of thermal performance breadth (in ~ and the amount of stochastic climatic variation. Parameter values are for the case in which genetic variance is independent of time and of performance breadth. Adapted from Huey and Kingsolver (1993), Fig. 8.

1.

11

specialists, the change in climate each generation substantially reduces the population's mean fitness, generating strong selection on the population. Given available genetic variation, this intense selection will result in a substantial evolutionary response to selection and will reduce the lag of the population behind the environment (Fig. 4). For a population of thermal generalists, however, the change in climate each generation has a smaller effect on the population's mean fitness, and thus generates weaker selection. Because of the smaller evolutionary response to this weaker selection, the lag of the population behind the environment may become large: if the lag becomes too great, extinction will occur. Thus thermal generalists may be at an ecological advantage, but at an evolutionary disadvantage, relative to populations of individuals with intermediate thermal breadths (see Huey and Kingsolver, 1993, for further details). This result is sensitive to assumptions about the determinants of the genetic variation in the population. For example, if genetic variation in optimal temperature results largely from a balance of mutation, selection, and drift, one might expect populations of thermal generalists to possess greater genetic variance in Z than populations of thermal specialists; in this case, thermal specialists no longer can sustain higher critical rates of climate change than generalists (Huey and Kingsolver, 1993). However, Burger and Lynch (1995) have recently extended these models to allow for dynamic evolutionary changes in population size and genetic variance over time in the population. Their simulations suggest that, even when genetic variance is determined by a mutation-selection-drift balance and varies over time, the mean time to extinction will be greatest for populations with intermediate performance breadths. These models, while clearly simplistic, highlight some of the complexities in predicting the evolutionary responses of populations to progressive climate change. I believe the main lesson from the models is this: the evolutionary responses of populations to climate change cannot be predicted solely based on ecological information, but must include some understanding of the genetics of physiological performance traits, about which we know very little. Is optimal temperature a polygenic trait? Do populations of intermediate performance breadth possess less genetic variation for performance traits than populations of generalists? Will specialists and generalists respond in different ways evolutionarily to abrupt step-changes versus progressive changes in climate? These questions have hardly been asked, much less answered, by physiological ecologists; but the answers may be key to predicting the evolutionary responses to climate change.

Evolutionary responses to climate change are most likely to be of importance in abundant, short-lived species such as pests and in populations

12

restricted to habitat islands including nature reserves. There are compelling, empirical, and theoretical reasons to believe that evolutionary responses to abrupt step-changes in the environment may differ qualitatively from responses to gradual, progressive changes, because of the consequences of selection intensity for evolutionary response. Studies of the genetic bases for pesticide resistance over the past 40 years suggest that the evolutionary responses to climate change will most likely involve polygenic responses. Quantitative genetic models suggest that the performance breadth of physiological traits will play an important and complex role in evolutionary adaptation to climate change and indicate that the determinants of genetic variation in physiological performance are key to understanding the evolutionary responses of populations to progressive climate change.

I thank Ray Huey and Bruce Tabashnik for useful discussion of the issues considered here, an anonymous reviewer for helpful comments on the earlier version, and Ray Huey for help with Fig. 2. Research was supported in part by NSF Grants BSR-890130 and IBN-9220748 to the author.

Burger, R., and Lynch, M. (1995). Evolution and extinction in a changing environment: A quantitative genetic analysis. 49, 151-163. Crow, J. F. (1957). Genetics of insect resistance to chemicals. 2, 227-246. Huey, R. B., and Kingsolver, J. G. (1989). Evolution of thermal sensitivity of ectotherm performance. 4, 131-135. Huey, R. B., and Kingsolver, J. G. (1993). Evolution of resistance to high temperature in ectotherms. 142, $21-$46. Lynch, M., and Lande, R. (1993). Evolution and extinction in response to environmental change. "Biotic Interactions and Global Change" (P. M. Kareiva, J. G. Kingsolver, and R. B. Huey, eds.), pp. 234-250. Sinauer, Sunderland, MA. McKenzie, J. A., and Batterman, P. (1994). The genetic, molecular and phenotypic consequences of selection for insecticide resistance. 9, 166-169. Roush, R. T., and McKenzie, J. A. (1987). Ecological genetics of insecticide and acaricide resistance. 32, 361-380. Tabashnik, B. E. (1995). Genetic basis of insecticide resistance: Dichotomy or continuum. 10, 164-165.

2 Intraspecific Variation in C02 Responses in Raphanus raphanistrum and Plantago lanceolaCa: Assessing the Potential for Evolutionary Change with Rising Atmospheric CO2

Elevated atmospheric C O 2 has well-documented effects on plant physiology and growth that may alter important ecosystem processes, particularly carbon storage and nutrient cycling (Mooney 1991). Differential sensitivity among species to elevated CO2 may also alter interspecific interactions (e.g., competition, symbiosis, herbivory), resulting in changes in community structure (Bazzaz, 1990). Predictions of the ecological consequences of elevated atmospheric CO2 have almost always been based on mean physiological and growth responses from a small, and often arbitrary, subsample of the species under consideration. Global change analyses have also generally assumed both a uniform response to CO2 across populations and CO2 response levels that are stable over time. However, mean responses estimated from a small number of individuals are probably not representative of the range of responses found among distinct populations of a species. The range of responses determines the evolutionary potential of a population within a community. This is a restatement ofFisher's (1930) fundamental theorem:

13

Copyright 9 1996 by Academic Press, Inc. All fights of reproduction in any form reserved.

14

In the CAM species for example, both populations and genotypes within populations differed significantly in the relative proportion of CO2 uptake in the daytime versus that at night (Kalisz and Teeri, 1986). When such differences in CO2 uptake result in differences in growth, survivorship, a n d / o r fecundity, the most fit genotypes will come to predominate in future generations. The result will be a shift in the mean response of the population as a result of natural selection. If a species' mean physiological or growth response to elevated CO2 evolves over time, either positively or negatively, then predictions regarding possible community and ecosystem level responses to rising CO2 may need to be revised. The first step in understanding how communities and ecosystems evolve under elevated COz requires characterization of the variation within populations that constitute the community. A primary requirement for COz to act as a selective agent is the presence of heritable variation in CO2 responses of fitness-related traits among individuals in a population. Work with other anthropogenic environmental perturbations such as heavy metal, ozone, and herbicide pollution has shown that rapid evolutionary responses are possible within natural populations given even low levels of genetic variation in tolerance to these stresses (Bradshaw, 1991). However, not all populations or species possess the requisite genetic variation. Clearly, where heritable variation is absent, no adaptive change is possible. The nature and magnitude of genetic variation in CO2 responses are poorly known at present. Variation among two cultivars in grain production at elevated CO2 was shown by Ziska and Teramura (1992), Wulff and Alexander (1985) found differences among four maternal families of in germination and early growth at twice ambient CO2, and Garbutt and Bazzaz (1984) documented population-level differences in reproduction at high COz in Fajer (1992), however, found no significant differences in the magnitude of growth or leaf secondary chemistry responses to elevated CO2 among five clones, whereas Curtis (1994) found significant variation in the magnitude of changes in lifetime reproduction due to elevated CO2 among five paternal families of Making accurate predictions of responses to selection generally requires accurate narrow-sense estimates of heritabilities (Falconer, 1981). The narrow-sense heritability requires in turn an estimate of the additive genetic variance within the population. Additive genetic variance estimates are most often based on the correlations between paternal half-sibs or between pollen parent and offspring correlations. Although these approaches give the best estimates of the additive genetic variances, accurate estimates require many hundreds or thousands of offspring. This endeavor is extremely expensive when artificial elevation of atmospheric CO2 is involved.

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15

Because so little is known about the genetic basis for phenotypic variation in response to elevated CO2, more conservative initial approaches are necessary. A lower cost, initial estimate of the potential for evolutionary change can be gained from an examination of the variance among maternal fullsib families or from a limited number of paternal half-sib families. After significant variation at one of these levels is established, a more complete genetic analysis can be conducted. To improve our understanding of the evolutionary potential in CO2 responses, we characterized 12 additional paternal families in maternal families and conducted a separate study of 18 (Klus unpublished). Here we integrate results from these studies, presenting evidence for intraspecific, family-level variation in physiological, growth, and reproductive responses to twice ambient CO2. In the experiments, the goal was to obtain a preliminary test for the presence of additive genetic variance for leaf area and number of flowers, traits known to influence fitness in the field. In the experiments, the goal differed. Under normal atmospheric conditions populations of P. have already been shown to have heritable variation for a broad variety of traits likely to be affected by CO2 level or to affect fitness (Tonsor and Goodnight, 1996; Teramura and Strain, 1979; Wolff and Van Delden, 1989). Therefore, the goal in the experiments was to gain a mechanistic understanding of the range of responses to elevated CO2 within two populations and to gain a preliminary estimate for evolutionary potential in mechanistically important traits.

Raphanus raphanistrum Two separate experiments were conducted, in 1992 and in 1993. Seeds for parental genotypes were obtained from the same location in Deer Isle, Maine, in the year preceding each study. For the 1992 study, 5 individuals from separate maternal plants were randomly selected to serve as pollen donors and 20 randomly selected individuals, also from separate maternal plants, served as pollen recipients. Each pollen donor (male parent) was crossed with 4 recipients (female parents) in a nested design (females within males), yielding 5 paternal families. For the 1993 experiment, 12 separate males were crossed with each of 3 separate females in a standard diallel breeding design, yielding 12 paternal families. With these designs, significant paternal effects are interpreted as evidence for additive genetic variance among paternal genotypes. Experiments were conducted at the University of Michigan Biological Station, Pellston, Michigan, in large, open-top field chambers. Half of the

16

chambers were maintained at approximately 700/zl liter -1 CO2 and the remainder at ambient CO2 (--350/zl liter -1 CO2). Seeds were planted in 2.5-liter pots filled with a mixture of locally derived sand and topsoil and thinned to one plant per pot after germination. All pots were watered daily as needed. In 1992 there were no nutrient amendments whereas in 1993 each pot received three 23-mg additions of NHaNO~ over a 3-week period. Germination occurred within 4 - 6 days followed by growth of a basal rosette, with bolting and flowering beginning --30 days after planting. Each flower was hand pollinated 1-2 days after opening. Days to bolting, total leaf area at bolting (measured nondestructively), total n u m b e r of flowers produced, and total seed set (1992 only) were recorded for each plant. In 1992, 32 replicates per paternal family were randomly divided among 4 chambers for a total of 160 pots per CO2 treatment (5 paternal families • 4 maternal families • 4 replicates per female • 2 chambers per CO2 treatment). In 1993, 36 replicates per paternal family were divided among 6 chambers for a total of 216 pots per CO2 treatment (12 paternal families • 3 maternal families • 2 replicates per female • 3 chambers per CO2 treatment). Data were analyzed with a fixed-effects model ANOVA where CO2 and father were main effects and mother was either fully crossed (1993) or nested within fathers (1992). Response of progeny from individual fathers was evaluated with separate two-way ANOVAs where CO2 and m o t h e r were main effects.

Plantago lanceolata Seeds were collected from 12 open-pollinated plants (= maternal families) in each of two populations in southern Michigan. The experiment was conducted at the Kellogg Biological Station, Hickory Corners, Michigan, in small, open-top field chambers using the design of Curtis and Teeri (1992). Half of the chambers were maintained at approximately 700/zl liter -1 CO2 and the remainder at ambient CO2. Seeds were germinated at the CO2 level in which they were to be grown. Six seedlings from each maternal family were divided among four chambers at each CO2 treatment. Seedlings were individually planted in 2.5-liter pots filled with a mixture of locally derived sand and topsoil and placed in the chambers in early June 1992. All pots were watered daily as needed but received no additional nutrients. After 3 weeks' growth, all chambers were covered with a neutral density shade cloth to alleviate symptoms of high light stress and remained so shaded throughout the experiment. Net COz assimilation was measured on intact, newly expanded leaves after ca. 100 days' growth. Measurements were made in the laboratory with an ADC LCA2 photosynthesis system under saturating light intensifies using the same CO2 level under which the plants were grown. Plants were harvested after 127 days' growth. Sample size for each family was <-6 and 6 of

17

2.

the 24 families were excluded from analysis because two or fewer individuals had germinated in a particular COz environment. Data were analyzed with a fixed-effects model ANOVA with CO2 and population as main effects and family nested within population. In this analysis, significant CO2 treatment effects indicate a consistent difference between CO2 levels across populations and families. Significant population and family level effects indicate that the populations and families respond differently in terms of assimilation, which can contribute to an evolutionary response to elevated CO2. Family level differences in this design include genetic and maternal environmental effects. Thus, they indicate only the potential for a narrow-sense heritability.

We found significant genetic variation in life history and reproductive characteristics among families in both years, but markedly different responses to CO2 in 1993 compared to 1992 (Fig. 1). In 1992 there was no effect of CO2 on leaf area at bolting but there was a strong positive COz effect on flower production (Fig. 1A, P < 0.001). This stimula-

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Paternal family Genotypic variation in life history and reproductive responses of grown at elevated (solid symbols) or ambient (open symbols) CO2. Experiments were conducted in two years, 1992 (A) and 1993 (B), using seeds derived from a c o m m o n parental population. Vertical bars indicated one SE, n - 6 (1992) or n = 8 (1993). *P < 0.06, **P < 0.01.

18

tion of reproduction was not experienced uniformly across genotypes, however, ranging from an 8% increase in family 4 (not significantly different from zero) to a 50% increase in family 5 (P < 0.01). In the 1993 experiment, growth at elevated CO2 resulted in significantly less leaf area at bolting (9% decrease overall, P < 0.01), but this effect again was unevenly distributed across families (Fig. 1B). Nine families showed no significant CO2 effect on leaf area while three families had significant reductions, with a maximum of 23% less leaf area at bolting in family 8 under elevated CO2. Unlike results from 1992, flower production showed a pattern similar to that of leaf area at bolting, with a significant decrease overall at high CO2 (P < 0.001) but with considerable variation among families in the magnitude of this response. Most families showed no significant CO2 effect on numbers of flowers while families 7 and 9 had 40 and 38% reductions, respectively. These results are consistent with previous work documenting heritable variation in fitness characters in (Mazer, 1987). They do not, however, provide a clear picture of how rising CO2 might act on those characters. In 1992, an exceptionally cool and cloudy summer in northern lower Michigan, elevated CO2 increased reproductive output and led to a change in rank order of seed production among five genotypes (Curtis 1994). The weather in 1993 was considerably warmer and sunnier than that in 1992, and while leaf area growth prior to bolting reflected the improved growth conditions, flower production was equivalent to (ambient CO2, overall) or lower than (elevated CO2, overall) that recorded in 1992. Although CO2 effects on flower production varied across genotypes, we found no evidence in 1993 for changes in rank order of genotypes in ambient compared to elevated CO2. also exhibited among family variation in responses to elevated CO2 (Fig. 2). The average stimulation of photosynthesis at elevated CO2 was 50% over ambient, which is comparable to that reported for other herbaceous species (Drake and Leadley, 1991). It is important to note that this average results from 11 families that show no significant stimulation and 8 families that show up to 75% greater assimilation at elevated levels compared to ambient CO2 levels. This is the first time that intraspecific variation in this response has been described. Plant size, as measured by whole-plant biomass at the end of the growing season, also varied significantly among these families. Fifteen families showed small or nonsignificant CO2 effects, two families showed significant positive responses, and one family showed a strong negative response. Plant size is well correlated with reproductive output under field conditions (Tonsor and Goodnight, 1996). These size differences among families are therefore likely to affect plant fitness. Klus (unpublished data) found that some families acclimated photosynthetically

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Genotypic variation in photosynthetic and growth responses of grown at elevated (solid symbols) and ambient (open symbols) CO2.Assimilation was measured in September after 100 days' growth, and plants were harvested after 127 days' growth. Seeds were collected from plants growing in either a lakeshore population (families 2-15) or a field population (families 31-44). Vertical bars indicated one SE, n = 3-6. *1 = P < 0.1, *P < 0.05, **P < 0.01.

resulting in indistinguishable assimilation rates u n d e r to elevated CO2, a m b i e n t a n d elevated CO2 by the e n d of the season, w h e r e a s o t h e r families showed n o sign of such acclimation. T h e s e differences in the p h o t o s y n t h e t i c r e s p o n s e to CO2 could h e l p explain differences in g r o w t h r e s p o n s e to CO2 a m o n g families. With biomass as well as with assimilation, the average r e s p o n s e of the species was positive, b u t this average r e s u l t e d f r o m a mix o f families, s o m e of which r e s p o n d e d negatively, s o m e n o t at all, a n d s o m e positively. has b e e n shown to r e s p o n d rapidly to b o t h n a t u r a l a n d artificial selection o n a r a n g e of ecologically i m p o r t a n t c h a r a c t e r s (Wu a n d Antonovics, 1976; Wolff a n d Van D e l d e n , 1989). T h u s for o u r p o p u l a t i o n s of P. the a m o n g family variation could serve as the basis for the evolution of i n c r e a s e d c a r b o n gain in h i g h CO2 e n v i r o n m e n t s . P r e d i c t i o n s of the of evolution u n d e r i n c r e a s e d a t m o s p h e r i c c a r b o n gain r e q u i r e m o r e d e t a i l e d quantitative g e n e t i c studies.

Clearly, shifts in the proportional representation of these or families within their respective populations would change our perceptions of the species' performance with a community. The extent to which families responding to elevated CO2 will increase in abundance in natural communities depends on two factors. The first factor is the extent to which family level differences in assimilation, allocation, and growth reflect genetic or maternal environmental components. Tonsor and Goodnight (1996) found that maternal family-based heritability estimates of assimilation rate under ambient CO2 conditions in approximately double the significant narrow-sense estimates for this species, but they saw no maternal effects on biomass. This means that there was both a nuclear genetic and a maternal component to the inheritance of assimilation rate, while size was affected only by nuclear genes. In Tonsor and Goodnight's study of nine traits, only those traits associated with physiology and leaf anatomy showed significant maternal effects on family means, suggesting an important maternal genetic role via cytoplasmic inheritance for those traits. If the significant maternal family variance we found in P. has the same genetic basis as was seen in Tonsor and Goodnight's study, both assimilation rate and biomass can be expected to evolve under elevated CO2. The second factor influencing the extent to which responding families will increase in abundance in natural communities is the degree to which the variation measured is maintained under field conditions. This degree is influenced by genotype-environment interactions, where competition is a part of the normal field environment. We have little basis for judgment here, and the only solution is field studies that combine measures of community-level and population genetic-level changes.

Our data demonstrate substantial among family intraspecific variation in response to elevated CO2. This variation is a necessary precondition to any evolutionary response to rising CO2 and could lead to large shifts in average population-level responses under elevated CO2 conditions. Evolutionary changes within populations could thus alter both ecosystem-level processes such as carbon storage and community-level interactions among species. It is important, therefore, to understand the magnitude and distribution of this variation as we refine our predictions of the ecological consequences of global climate change. We remain a long way from accurately predicting rates of evolutionary change within a community context. Although this chapter documents the best studies to date of the evolutionary potential of herbaceous plants under elevated CO2, much larger and more detailed studies of evolvability under

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21

field c o n d i t i o n s are necessary. A clearer u n d e r s t a n d i n g o f the physiological, allocational, a n d life-historical causal m e c h a n i s m s for intraspecific variation in r e s p o n s e to elevated CO2 are n e e d e d . T h e s e can c o n t r i b u t e to a m o r e effective use o f f u n d s d e v o t e d to the necessarily large-scale studies o f evolvability u n d e r elevated CO2. O n c e the m o s t a p p r o p r i a t e traits for study have b e e n clearly identified, c o m p a r i s o n s o f g e n o t y p e s using b o t h quantitative genetics a n d its r e c e n t hybrid with m o l e c u l a r genetics, quantitative t r a i t locus (QTL) identification, can be u s e d to describe the g e n e t i c a r c h i t e c t u r e u n d e r l y i n g this variation. U n d e r s t a n d i n g the g e n e t i c a r c h i t e c t u r e is a crucial step in assessing the evolvability o f the traits. Studies that i n c l u d e s i m u l t a n e o u s m e a s u r e s o f the c h a n g i n g g e n e t i c c o m p o s i t i o n o f species a n d the relative a b u n d a n c e s o f species within the c o m m u n i t y are especially i m p o r t a n t in p r e d i c t i n g w i t h i n - c o m m u n i t y adaptation versus successional c o m m u n i t y r e p l a c e m e n t as r e s p o n s e s to c h a n g e s in a t m o s p h e r i c chemistry. T h e i n t e g r a t i o n o f physiological, allocational, a n d g e n e t i c studies c o n d u c t e d in n a t u r a l p l a n t c o m m u n i t i e s c o u l d contribute substantially b o t h to o u r ability to p r e d i c t whole-ecosystem c a r b o n storage a n d to the i n t e g r a t i o n o f subdisciplines within the field o f ecology. I n t e g r a t e d studies o f species- a n d community-level r e s p o n s e s to elevated CO2 r e p r e s e n t b o t h a f o r m i d a b l e c h a l l e n g e a n d an exciting o p p o r t u n i t y for the unification o f ecology.

We thank Jon Ervin, Pam Woodruff, Nina Consolatti, Andrea Case, and Katherine Syverson for their assistance in the field and Allison Snow and Jim Teeri for critical scientific and material assistance. This research was supported with funds from the Ohio State University, an NSF predoctoral fellowship to D.J.K., NSF Grant CIR-9113598 to the Kellogg Biological Station, Michigan State University, the University of Michigan Biological Station, and the University of Michigan Project for the Integrated Study of Global Change.

Bazzaz, F. A. (1990). The response of natural ecosystems to the rising global C O 2 levels. 21, 167-196. Bradshaw, A. D. (1991). Genostasis and the limits to evolution. B 333, 289-305. Curtis, P. S., and Teeri, J. A. (1992). Seasonal responses of leaf gas exchange to elevated carbon dioxide in 22, 1320-1325. Curtis, P. S., Snow, A. A., and Miller, A. S. (1994). Genotype-specific effects of elevated CO2 on fecundity in wild radish 97, 100-105. Drake, B. G., and Leadley, P. W. (1991). Canopy photosynthesis of crops and native plant communities exposed to long-term elevated COs. 14, 853-860.

22 Fajer, E. D., Bowers, M. D., and Bazzaz, F. A. (1992). The effect of nutrients and enriched CO2 environments on production of carbon-based allelochemicals in A test of the carbon/nutrient balance hypothesis. 140, 707-723. Falconer, D. S. (1981). "Introduction to Quantitative Genetic Analysis." Longman, New York. Fisher, R. A. (1930). "The Genetical Theory of Natural Selection." Clarendon, Oxford. Garbutt, D., and Bazzaz, F. A. (1984). The effects of elevated CO2 on plants. III. Flower, fruit and seed production and abortion. 98, 433-446. Kalisz, S., and Teeri, J. A. (1986). Population-level variation in photosynthetic metabolism and growth in 67, 20-26. Klus, D.J., Kalisz, S., Tonsor, S.J., Curtis, P. S., and Teeri, J. A. Intraspecific variable responses to elevated atmospheric CO2: Resource partitioning in above- and below-ground tissues in L., unpublished. Mazer, S.J. (1987). The quantitative genetics of life history and ftness components in L. (Brassicaceae): Ecological and evolutionary consequences of seed-weight variation. 130, 891-914. Mooney, H. A., Drake, B. G., Luxmoore, R. J., Oechel, W. C., and Pitelka, L. F. (1991). Predicting ecosystem responses to elevated CO2 concentrations. 41, 96-104. Teramura, A. H., and Strain, B. R. (1979). Localized populational differences in the photosynthetic response to temperature and irradiance in 57, 25592563. Tonsor, S. J., and Goodnight, C.J. (1996). Testing the effect of mating structure on the partitioning of phenotypic variance in in press. Wolff, K., and Van Delden, W. (1989). Genetic analysis of ecologically relevant morphological variability in Response and correlated response to bidirectional 62, 153-160. selection for leaf angle. Wu, L., and Antonovics, J. (1976). Experimental ecological genetics in II. Lead tolerance in and from a roadside. 57, 205-208. Wulff, R. D., and Alexander, H. M. (1985). Intraspecific variation in the response to COs enrichment in seeds and seedlings of 66, 458-460. Ziska, L. H., and Teramura, A. H. (1992). Intraspecific variation in the response of rice (Oryza to increased COz- photosynthetic, biomass and reproductive characteristics. 84, 269-276.

3 Selective Responses to Global Change: Experimental Results on Brassicajuncea (L.) Czern.

The climate change forecasted for the next century is predicted to occur at an unprecedented rate (Huntley, 1991). Projections are an increase of ---4~ in global mean temperature over some 50 years. The rates of plant migration necessary to track such changes in climate are higher than the maximum rates of migration estimated from the Quarternary climate change (Huntley, 1991). Therefore, it is unlikely that plants will successfully migrate in response to global change, hence the threat of massive extinction. Holt (1990) and Bradshaw and McNeilly (1991) suggested that evolutionary changes resulting in genotypes adapted to the new climatic environment might prevent the extinction of some species. Bradshaw and McNeilly (1991) also suggested that, in the absence of genetic changes, adaptive plasticity could provide an alternative strategy. Yet the potential for evolutionary responses to global change has received little attention to date. The experiment discussed in this chapter was designed to assess the evolutionary consequences of global change. We selected a wild mustard species, (L.) Czern., over 7 generations, for growth under conditions simulating global change. Throughout this chapter we refer to the long-term growth environments as Selection treatments. Specifically, we want to quantify the relative importance of genetic and plastic responses to Selection. was chosen as a model species because it is self-incompatible, which prevents excessive inbreeding (Williams and Hill, 1986), and it has a short life cycle, which, under our experimental conditions, lasted 50 days. Copyright 9 1996 by Academic Press, Inc. All rights of reproduction in any form reserved.

Two replicate lines of 70 plants were selected u n d e r conditions simulating either the present atmosphere ( " C o n t r o l " treatment) or, by gradually increasing CO2 and temperature, global change ("Predicted" treatment). In the Control treament, conditions were maintained at the initial temperature (22~176 and CO2 conditions ( 3 7 0 / x l . liter -1) during the 7 generations of Selection. In contrast, conditions in the Predicted treatment changed gradually from one generation to the next (Table I). During Selection, daily m e a n temperature increased by 3.6~ while CO2 approximately doubled. Degree-days were used to model the desired changes in temperature over time, by combining increased mean temperatures and more frequent heat stress. This design accommodates the prediction of an increase in length and frequency of heat waves with the greenhouse effect (Mearns 1984). To " m i m i c " Natural Selection, we selected for high fecundity in both treatments. After the plants were harvested and the siliques dried, the 18 most productive plants within each selection line, based on total silique mass, were selected and their seeds used to sow the next generation. Consequently, plants from the Control and Predicted treaments were subjected to identical fecundity selection and inbreeding. Overall, inbreeding ranged between 2.3 and 3.9% and the possible significance of inbreeding and inbreeding depression for our results is discussed elsewhere (Potvin and Tousignant, 1996). The choice of total silique biomass as a fitness estimate was validated by calculating genetic correlations a m o n g fitness-related traits at the start of Selection, based on Rose and Charlesworth (1981). There were positive genetic correlations between, on one hand, total silique mass and, on the other hand, total seed n u m b e r and total seed mass (ranging from 0.812 to 0.995). To identify evolutionary responses after Selection, we carried out a reciprocal transplant experiment. Plants selected u n d e r Predicted conditions

Generation number

CO2 level (/xl 9liter-1)

0 1 2 3 4 5 6 7

370 410 450 490 530 570 610 650

Day/night temp. (~ 22.0/16.0 22.0/16.0 22.4/16.4 22.8/16.8 23.2/17.2 23.6/17.6 24.0/18.0 24.4/18.4

No. of days of heat stress (32~176

Daily mean temp.

0 2 3 4 5 6 7 8

20.0 20.4 21.0 21.6 22.1 22.6 23.1 23.6

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were grown in both Control and Predicted conditions and vice versa. The chambers were p r o g r a m m e d to either one of the conditions prevailing at the 7th generation. This approach has been used in the field and in artificial selection experiments to test for genetic adaptation (Jain and Bradshaw, 1966; Maxon Smith, 1977; Agren and Schemske, 1993). The underlying assumption is that a plant adapted to its environment will perform better in that environment than in a new one. In other words, given genetic adaptation, home transplants should do better than foreign ones. At first harvest we examined growth during the prereproductive life stage. The analysis of variance (ANOVA) indicated a significant main effect of Selection and a significant Selection by Environment interaction (Table II). Overall, the vegetative biomass was higher for plants selected in the Predicted regime. examination of the results indicated that the vegetative biomass of plants of selected and grown in the Predicted environment was significantly higher than that of plants grown under any other (Fig. 1A). At the end of the reproductive phase, vegetative biomass was significantly lower in the Predicted plants and the adaptive response was lost (Fig. 1B). The response of silique biomass to the Predicted growth conditions was highly significant but their was no effect of the Selection treatment. Overall, silique biomass was 3.45 g under Control conditions and 0.95 g under Predicted ones. Direct exposure of Control plants to Predicted conditions (CP/CC) reduced silique biomass from 3.2 to 1.0 g (Fig. 1C). Silique biomass of the Predicted plants likewise was reduced by growth in the Predicted environment with no sign of genetic adaptation. The analysis of the reciprocal transplant answered our first main question. Vegetative biomass responded to the stimulated global change mainly through genetic changes. Between 15 and 18% of the total variation in vegetative biomass was due to the effect of Selection. Furthermore, in the prereproductive growth period, these genetic changes were adaptive. Conversely, the response of silique biomass was plastic and maladaptive. The reproductive output of an annual plant without a seed bank such as provides a direct estimate of fitness (Primack and Kang, 1989). Consequently, the second part of this chapter will further examine the responses of silique biomass to the gradual changes in environment imposed in the Predicted treatment. Despite a fecundity selection, silique biomass decreased significantly under both treatments during the 7 generations of Selection (Fig. 2). This reduction in silique biomass was not accompanied by a reduction in vegetative biomass. The decrease in total silique biomass was significantly faster for the Predicted selection lines, overall -0.443 g 9 generation -1, than for the Control lines, overall -0.334 g 9 generation -1 (Table III). A closer look at the data suggests that whereas silique biomass decreased continuously in the Predicted environment, it

26

6

6

I

-r-

I

-T-

I

(A) Vegetative biomass of at the prereproductive (Day 21) and (B) late reproductive (Day 49) harvests, and (C) pod biomass at maturity (Day 49). Vegetative biomass was the mass of stems, leaves, and roots. Plants of both selection lines were pooled and sample size is indicated in parentheses. Significant differences among groups using Tukey's HSD, P < 0.05, are indicated by different letters. Differences in sample sizes were due to postgermination mortality. CC: "Control" lines grown under "Control" conditions; CP: "Control" lines grown under "Predicted" conditions; PP: "Predicted" lines grown under "Predicted" conditions; PC: "Predicted" lines grown under "Control" conditions. (Modified from Potvin and Tousignant, 1996.)

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0 0

(A) Mean pod biomass of over seven generations of selection in the "Control" or "Predicted" conditions and (B) mean divergence of the "Predicted" lines from the average value of "Control" ones. Data were not available for the first generation. In (A) each value represents the mean of 70 plants. CI: "Control" line 1; C2: "Control" line 2; PI: "Predicted" line 1; P2: "Predicted" line 2.

stabilized at g e n e r a t i o n s 3 - 4 for the C o n t r o l e n v i r o n m e n t . This e x p o n e n t i a l d e c r e a s e in silique biomass can be best c a p t u r e d using n o n l i n e a r r a t h e r t h a n linear regression, as shown by the h i g h e s t r 2 values (Table III). T h e e x p o n e n t i a l e q u a t i o n p r e d i c t e d asymptotic r e p r o d u c t i v e biomass of 2.02 a n d 2.08 g for the two C o n t r o l selection lines. T h e r e was n o clear a m e l i o r a t i o n in curve fitting w h e t h e r linear or nonlinear r e g r e s s i o n was u s e d to analyze the silique biomass of P r e d i c t e d plants. F r o m the o b s e r v e d c h a n g e in silique biomass t h r o u g h time, we p r e d i c t e d the o u t c o m e of Selection in the P r e d i c t e d e n v i r o n m e n t . For b o t h selection lines, we u s e d linear r e g r e s s i o n to p r e d i c t the cumulative selection differential, AS, r e d u c i n g slique biomass to zero. S is d e f i n e d for e a c h g e n e r a t i o n as the d i f f e r e n c e existing b e t w e e n the m e a n p a r e n t a l value for a trait a n d the m e a n r e s p o n s e of the offsprings for that trait (Falconer, 1989). A s e c o n d series of r e g r e s s i o n was u s e d to p r e d i c t the n u m b e r of g e n e r a t i o n s n e e d e d to r e a c h such AS value. T h e cumulative selection differential r e q u i r e d to r e d u c e re-

28

Sources (A) Treat. Env. Line(Treat.) Treat.XEnv. Env. XLi(Tre.)

Sums of squares

0.726 0.241 0.161 0.884 0.169

1 1 2 1 2

9.26 3.07 1.04 11.28 1.08

0.0032 0.08 0.36 0.0012 0.35

8.360 1.226 0.176 0.673 0.240

1 1 2 1 2

13.44 1.97 0.14 1.08 0.19

0.0005 0.17 0.87 0.30 0.83

0.389 114.1 0.498 0.647 2.316

1 1 2 1 2

0.83 243.3 0.53 1.38 2.47

0.37 0.0001 0.60 0.24 0.09

(8) Treat. Env. Line(Treat.) Treat. XEnv. Env. •

(c) Treat. Env. Line(Treat.) Treat. XEnv. Env. XLi(Tre.)

productive growth to zero was 8.7 and 9.4 for the two selection lines. Assuming a constant rate of increase in ASthrough time, complete reproductive failure would occur in the Predicted environment within 9.8-10.1 generations. Therefore, the Predicted environment would lead to local extinction of B. with an additional 3 generations of Selection.

Selection lines "Current" 1 "Current" 2 "Predicted" 1 "Predicted" 2

L i n e a r regression

N o n l i n e a r regression

3.74-0.311 g e n r~ = 0.721 a 3.883-0.334 gen r~ = 0.626 a 4.093-0.434 gen r~ = 0.813 b 4.281-0.446 gen r~ = 0.882 b

2.045 + e x p ( - 0 . 3 2 9 * g e n ) r2 -- 0.933 2.084 + e x p ( - 0 . 3 3 7 * g e n ) r~ = 0.907 1.696 + e x p ( - 0 . 3 0 6 * g e n ) r~ --- 0.847 1.81 + e x p ( - 0 . 2 9 2 * g e n ) r~ = 0.866

For the linear regressions, slopes followed by a different letter are statistically different with P < 0.05. a

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was apparently unable to adjust to the simulated global change either plastically or evolutionarily. Could the model of Kingsolver (Chapter 1) explain this absence of evolutionary response? In our experiment, the CO2 concentrations increased by 40 /~1 9 liter -1 between two successive generations, while the mean daily temperature rose by 0.4-0.6~ The environmental changes were clearly well within the natural variation in CO2 and in temperature encountered by The maximum high temperature, 32/26~ was also within the temperature range encountered in the field (Polowick and Sawhney, 1988). Our experimental situation might thus have been analogous to that of the "thermal generalists" (see Kingsolver, Chapter 1). Each generation was sown with seeds from 18 mothers, which represents 25% of the original population. Kingsolver's model suggests that this intensity of selection might not have been strong enough to sustain the rate of changes in environmental conditions. A lag between the population tolerance and the environmental conditions was thus created. As this lag increased, we observed a decrease in silique biomass, hence fitness, that could lead to the future extinction of the population. The evolutionary model of Kingsolver thus provides an appropriate theoretical framework to examine our experimental results. In conclusion, we would like to examine our results in a broader evolutionary perspective. We wish to make three main claims: first, the directional and gradual changes in the environment did exert a selective pressure on Second, evolutionary responses to such gradual change in CO2 concentration and climate are possible and were evidenced by the genetic changes in vegetative biomass. Finally, the magnitude and direction of those changes will clearly be trait-specific. Vegetative biomass responded mainly by genetic changes whereas silique biomass showed only plastic responses. We believe that our understanding of the evolutionary consequences of global change cannot be predicted from an abrupt change in environmental conditions. Our experimental results support the idea that ecological information is not sufficient to predict the evolutionary responses to climate change (see Kingsolver, Chapter 1). More specifically, for B. any inferences of the evolutionary consequences of global change drawn from the response of vegetative biomass alone would have been misleading. A better understanding of the evolutionary consequences of global change might come from the analysis of the heritabilities and genetic correlation structure of fitness-related traits.

During the 18 months of Selection, we had continuous support from M. Romer and C. Cooney from the McGill Phytotron. We thank M. Beaudet and D. Cantin for their assistance during

seemingly endless seed counting and weighing. Discussions with Drs. S. Arnold, Y. Carri/~re, and M. Johnson helped to clarify the evolutionary aspects of this work R. G. Shaw has been most helpful in disentangling problems in the quantitative genetic approach. This research was funded by a "Nouveaux chercheurs" research grant, Fonds FCAR, Quebec, to C.P.D.T. acknowledges a NSERC postgraduate fellowship.

Agren, J., and Schemske, D. W. (1993). The cost of defense against herbivores: An experimental study of trichome production in 141, 338-350. Bradshaw, A. D., and McNeilly, T. (1991). Evolutionary response to global climatic change. 67 (Suppl. 1), 5-14. Falconer, D. S. (1989). "Introduction to Quantitative Genetics." Wiley, New York. Holt, R. D. (1990). The microevolutionary consequences of climate change. 5, 311-315. Huntley, B. (1991). How plants respond to climatic change: Migration rates, individualism, and the consequences for plant communities. 67(Suppl. 1), 15-22. Jain, S. K., and Bradshaw, A. D. (1966). Evolutionary divergence among adjacent plant populations. 21, 407-441. Maxon Smith, J. W. (1977). Selection for response to CO2-enrichment in glasshouse lettuce. 17, 15-22. Mearns L. O., Katz R. W., and Schneider S. H. (1984). Extreme high-temperature events: Changes in their probabilities with changes in mean temperature. 23, 1601-1613. Polowick, P. L., and Sawhney, V. K. (1988). High temperature induced male and female sterility in Canola. L.). 62, 83-86. Potvin, C., and Tousignant, D. Evolutionary consequences of simulated global change: Genetic adaptation or adaptive phenotypic plasticity. in press. Primack, R., and Kang, H. (1989). Measuring fitness and natural selection in wild plant populations. 20, 367-396. Rose, M. R., and Charlesworth, B. (1981). Genetics of life history in I. Sib analysis of adult females. 97, 173-186. Williams P. H., and Hill, C. B. (1986). Rapid-cycling populations of 232, 13851389.

Genetic Variation in the Response of Plant Populations to Elevated in a NutrientPoor, Calcareous Grassland

Results from models and experiments on the effects of rising C O 2 differ in that the models often predict large effects on ecosystems (Woodward, 1992; World Conservation Monitoring Centre, 1992), whereas only small effects at the ecosystem level have been observed in experiments (e.g., Billings 1984; Grulke 1990; Ktrner and Arnone, 1992, but see Curtis 1989). In particular, though expected from the response of single species grown under high CO2, shifts in species composition within a community are rare and appear to be highly dependent on characteristics of the ecosystem considered, such as the availability of nutrients and light and the intensity of competition (Bazzaz, 1990). In a study of a natural tallgrass prairie, Owensby (1993) found essentially no change in the species composition and basal cover of the major warm-season dominants in response to CO2 treatments over a 3-year period. The time scale of the experiments might, however, often be too short for shifts in species composition to be observed (cf. Milchunas and Lauenroth, 1995). Ktrner and Arnone (1992), for example, found no significant response of the total biomass of an artificial ecosystem to elevated CO2 but pointed out that the slight observed biomass increase under elevated CO2 and the harmful levels of starch in leaves might alter the dominance relationships in this community in the long term. 31

Copyright 9 1996 by Academic Press, Inc. All rights of reproduction in any form reserved.

32

We suggest that both in models and in experiments there are implicit misconceptions about the nature of ecosystems because they are thought to contain assemblages of species or of individuals of species that have only mean properties. Variation within species is assumed to be negligible, interactions among species are rarely taken into account, and evolution is not allowed. A general feature of hierarchically organized systems is that lower level processes express more variation than higher level processes, because constraints are more stringent at the higher level (e.g., total biomass versus component-species biomass in an ecosystem; see O'Neill 1986; Odum, 1989). However, even though the lower level dynamics in an ecosystem such as individual and population processes might not greatly influence p h e n o m e n a observed at the ecosystem level in the short term, they cannot be neglected to understand the mechanisms that could lead to ecosystem-level modifications in the longer term. In this chapter, we shall focus on the dynamics of genetic variation within species and discuss its consequences for predicting the response of an ecosystem to an increase in CO2. Our aim is to demonstrate that lower level dynamics must be considered if CO2 research is to yield reliable predictions.

A. Genetic Variation and Plasticity Variation in natural populations is caused by several factors, including plastic response to variations in environmental conditions, genetic differences among individuals, and developmental noise. Phenotypic plasticity is environmentally induced phenotypic change that occurs within an organism's lifetime (Bradshaw, 1965; Stearns, 1989). Evidence suggests much of this environmentally induced variation is selectively advantageous (see, e.g., Marshall 1986) so that plasticity as a trait itself could be sensitive to selection (de Jong, 1990a,b). Moreover, genetic variation for plasticity in fitness-related traits has been observed in many plants (e.g., Scheiner and Goodnight, 1984; Silander, 1985; Schmid and Weiner, 1993; Stratton, 1994; Cheplick, 1995). Because of their open organization and their inability to move when conditions change, plants are thought to adjust to a change in their environm e n t largely by phenotypic plasticity, whereas mobile animals usually respond by behavior (e.g., migration) (Schmid, 1992). To illustrate the importance of understanding genetic variation, phenotypic plasticity, and genetic variation in phenotypic plasticity within a species to predict the effect of increasing CO2, it is convenient to start with a theoretical example. The range and mean value of conditions under which an individual can grow vary among species and even within species among genotypes. Two parameters can describe the fitness response or tolerance curve (Lynch and Gabriel, 1987) of a genotype to a given environmental factor: (1) the value of the environmental factor at which the fitness reaches the maximum

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for the genotype and (2) the range of values of this factor over which the genotype has positive fitness, i.e., over which it can grow, survive, and reproduce. T h e first p a r a m e t e r may be called the " n i c h e position" a n d the second one the " n i c h e width" of the genotype (Roughgarden, 1974). A genotype (or species) with a wide niche is called a "generalist," whereas a genotype (or species) with a narrow niche is called a "specialist." For an individual genotype the phenotypic expression of a quantitative character across an environmental factor is called a " r e a c t i o n n o r m " (Woltereck, 1909). It can be r e p r e s e n t e d by a functional response of the genotype to the environmental factor (de Jong, 1995). Now consider a set of genotypes with the same niche positions but different niche widths across an e n v i r o n m e n t a l gradient (Fig. 1). U n d e r the assumption that the fitness response (shown in a g r a p h of the niche) is related to the response of some resource-use character such as rooting d e p t h (shown in a reaction n o r m ) in each genotype, the generalist genotypes in the set are expected to have a m o r e plastic response in the resource-use character than the specialist genotypes. T h a t is, character values for the resource-use character, but not for fitness, should differ m o r e a m o n g contrasting environments in the generalists than in the specialists. Figure 1 presents the reaction n o r m s of different genotypes and the resulting fitness responses across an arbitrary e n v i r o n m e n t a l gradient. An ideally plastic genotype would maintain a high fitness in every e n v i r o n m e n t by adjusting the resource-use character along an optimal reaction n o r m (see also Schmid, 1992). However, genetic, physiological, and mechanical constraints likely exist, possibly in the form of trade-offs between traits, which restrict plasticity. Consequently, reaction n o r m s will usually diverge from the line of ideal plasticity and therefore the fitness response of any genotype will be limited to a certain range of e n v i r o n m e n t a l values beyond

Reactionnorms for a hypothetical resource-use character across an arbitrary environmental gradient and resulting niche responses or tolerance curves of three genotypes with similar niche position but different niche width. The ideally plastic reaction norm is indicated by the thin, dashed line with slope 1 in the left graph; the genotype with the steepest reaction norm is almost ideally plastic; and the one with the horizontal reaction norm is not plastic at all.

34 which conditions become too extreme for growth, survival, and reproduction. Returning to the generalist-specialist comparison, the generalist genotypes are assumed to have higher fitness than the specialist genotypes over most environmental conditions except those that are optimal for the specialist. This is because the ability to perform a broader variety of tasks through plasticity in resource-use characters may be possible only at the cost of reduced maximum performance. The view of a cost of plasticity has, however, been challenged by results from some experiments in which individuals that performed better in an "optimal" environment also performed better in other environments (Huey and Hertz, 1984). We shall assume for the purpose of the demonstration that all the genotypes have the same fitness under optimal conditions, and different assumptions would not change the conclusions drawn from this example. Let us now consider how a generalist and a specialist genotype will respond in a short-term experiment during which replicate individuals of the genotypes are grown at either ambient or elevated COp. Assuming that plants are adapted to the COp concentration they experience today or did some decades earlier, i.e., that their niche positions are fixed, and given, by definition, that generalist genotypes exhibit steeper reaction norms in traits that relate to CO2 uptake, these generalist genotypes should perform better under high COp than specialist genotypes.

B. Response at the Species Level As with genotypes, a generalist species has a broad fitness response and a specialist species has a narrow fitness response across an environmental gradient, such as some resource axis (Roughgarden, 1974). Specialist species always consist of a small n u m b e r of specialist genotypes with a similar niche position. Generalist species, however, may be either polymorphic and consist of specialist genotypes differing in niche position or monomorphic and consist of generalist genotypes with similar niche positions, or generalist species may represent some intermediate condition (Fig. 2). To stress the relevance of studying genetic variation in the response to increasing CO2, we shall now compare the results expected from shortterm experiments (in which plants are grown under elevated CO2) and the long-term evolution of specialist and generalist species differing in genetic variation a n d / o r plasticity. For this purpose it is convenient to characterize a species by the variation among its constituent genotypes in niche position and niche width. Six possible combinations are described in Fig. 3. For each of them, we present first the plasticity of the genotypes in a resource-use character (here related to CO2 uptake) and the distribution of niche positions (optimal COp concentration), then the performance of the species in a short-term experiment in which it is grown in monoculture under ambient and elevated COp, and, finally, its expected perfor-

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Environmental gradient Figure 2 Performance of two hypothetical generalist species (a, b) and one hypothetical specialist species (c) along an arbitrary environment gradient. Thick lines indicate the niches of the species; thin lines indicate niches of genotypes. The generalist species (a) is composed of a few similar generalist genotypes, generalist species (b) is composed of specialist genotypes with different niche positions, and the specialist species (c) is composed of a few similar specialist genotypes.

mance if it were allowed to evolve over a longer time period with continuously increasing CO2 concentrations. The continuous increase shall be slow enough for shifts in the frequency distribution of genotypes to keep pace, and the shifts shall come about only by selection and recombination without the appearance of new favorable mutations. The six species depicted in Fig. 3 represent the following cases: (A) low genetic variation for optimum CO2, no plasticity, no genetic variation in plasticity; (B) low genetic variation for optimum C 0 2 , high plasticity, no genetic variation in plasticity; (C) no genetic variation for optimum CO2, some genotypes with high plasticity, genetic variation in plasticity; (D) high genetic variation for optimum CO2, no plasticity, no genetic variation in plasticity; (E) high genetic variation for optimum CO2, intermediate plasticity, no genetic variation in plasticity; and (F) high genetic variation for optimum CO2, some genotypes with high plasticity, genetic variation in plasticity. If selection-recombination cycles are not allowed in the short term, the genetic composition of a population cannot change and only species containing generalist genotypes with high plasticity in CO2-resource use will be able to adjust to the new conditions and maintain a high performance (Fig. 3B and, to a lesser extent, Fig. 3E). This will be the case in shortterm experiments with suddenly increased CO2. With a slow and continuous increase in CO2, however, it is the species containing different specialist genotypes, i.e., the species with a large genetic variation within populations in CO2-resource use, that will maintain a high performance by an evolutionary adjustment of its mean response (Figs. 3 D - F ) . Obviously, many simplifications must be made in the theoretical example. In reality, there are other niche dimensions or characters in addition to C O 2 o r CO2-optimum for growth/reproduction, respectively, that will be

36

Reaction norms for a hypothetical COz-use character of six species differing in genetic variation and plasticity and their expected performance in ambient CO2 (amb.), in elevated CO2 in a short-term experiment (high ST), and in elevated CO2 if the increase is slow enough for evolution to happen (high LT). The numbers at the top of the bars in the

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modified with future climatic change, and interactions among the different characters might prove important. In particular, the existence of genetic variation in response to CO2 might not be relevant if it is negatively correlated with other traits (e.g., if there were a negative correlation between optimum temperature and optimum CO2 concentration for photosynthesis). Interactions among species also are to be taken into consideration. CO2 might, for example, change the relationship between higher plants and mycorrhiza (see Sanders, Chapter 17). Three predictions can, however, be derived from the theoretical example. First, the best "phytometers" for bioindication in global change should be specialists with low plasticity and low genetic variation in resource-use characters (Fig. 3A). Because of this low plasticity and low genetic variation, specialist species should indeed be the first ones to be outcompeted when environmental conditions change. An interesting problem that remains to be investigated is whether a specialist with respect to one environmental factor is also a specialist with respect to other environmental factors. In the first case it would be possible to use indicator species for nutrient-poor grasslands such as (described below) also to detect changes in atmospheric composition. Second, in short-term experiments on the effect of CO2on plants, generalist species consisting of similar generalist genotypes, i.e., with high plasticity (Fig. 3B), should do better than generalist species consisting of different specialist genotypes (Fig. 3D) because the first can adjust faster to the new conditions than the second. Consequently, it is impossible to predict the effect of elevated CO2 on the species composition of a community from short-term experiments, unless it is known whether the differences in the specific responses are due to phenotypic plasticity or genetic variation. Third, if the conditions change slowly enough for the genetically variable species to evolve, we may in the long term expect a plastic species to be outcompeted by the better adapted genotypes of a genetically variable species. Under this scenario, environmental change will inevitably lead to a reduction in genetic and species diversity in an ecosystem. These points stress the necessity to consider the dynamics of the genetic composition of the species in order to predict the effect of environmental changes in communities of species (Billington and Pelham, 1991; Bradshaw and McNeilly, 1991).

right set of graphs give the ranking of the species if their performance is compared under the same conditions (i.e., amb., high ST, or high LT). As in Fig. 1, the dashed line represents an ideally plastic genotype. The left mark on the x-axis represents the ambient level of CO2 and the right mark represents an elevated level of CO2.The width of the shaded area visualizes the amount of genetic variation for optimum CO2 in the species; see text for interpretation.

38

Therefore the questions we wished to address experimentally were the following: 1. How do generalists and specialists phenotypically respond to elevated CO2? 2. Is there genetic variation within species in the response to elevated CO2? 3. What proportion of the variation in phenotypic characters has genetic causes (heritability) ? In the following sections we present results obtained for a model pair of a specialist and a generalist species. (specialist) and (generalist) are two closely related grassland perennials. Known genotypes of these two species were grown in a CO2 field experiment in a nutrient-poor, calcareous grassland south of Basel, Switzerland (see Leadley and K6rner, Chapter 11).

In a research program a field experiment was set up to investigate the effects of varying plant diversity on ecosystem responses to elevated CO2 (K6rner, 1995; Leadley and K6rner, Chapter 11; see also Weber and Schmid, 1995). The aim was to provide ecologists of different expertise with properly replicated and maintained installations in which the influence of elevated CO2, competition, and three biodiversity treatments on plant growth and ecosystem processes could be tested. As a compromise between the conflicting demands of realism and precision (see Levins, 1968), the experiment was carried out under natural field conditions using species and homogenized soil from the site but with controlled plantings in three biodiversity treatments (5-, 12-, 31-species plots). The ambient and elevated CO2 treatments were applied using screen-aided CO2 enrichment (SACE, see K6rner 1995; Leadley and K6rner, Chapter 11). A number of test plants were grown in a competition-free microenvironment in tubes within the planted plots. For as many species as possible, defined genetic material was propagated in the glasshouse and similar-sized seedlings or cuttings were transplanted to the field plots according to a predefined random arrangement. The species according to our a priori information from the floristic literature (e.g., Hess 1972; Landolt, 1977) represent an ideal generalist-specialist pair, and this classification could be supported in nutrient-gradient experiments with added competition (Birrer and Schmid, unpublished data). occurs over a broad range of environ-

39

4.

ments from nutrient rich to relatively nutrient poor, from dry to wet, from grassland to disturbed sites, and even to road margins within forests; P. is restricted to nutrient-poor, dry grasslands and has received legal status as indicator species for this community type in Switzerland. Twenty-eight genotypes of each species were collected at random from selected patches at the field site. To assess genetic variation and treatment-by-genotype interactions, each genotype was grown in competition-flee tubes and in all the treatment combinations that contained transplanted communities (3 diversity levels • 2 CO2 levels; Table I). Measurements of fitness-related characters were taken at the start of the experiment in the spring and repeated in 2-3 months. The analysis presented was carried out on the second set of measurements.

A. Species Responses No main effects of C O 2 o n the investigated characters could be detected (for n u m b e r of leaves and cumulative leaf length see Table II). The performance of the plants as indicated by the measured characters declined with increasing biodiversity from 5-species plots to 12-species plots to 31-species plots. However, because each of these three biodiversity levels was represented by a particular (replicated) mixture, this effect could have been due to the presence of a particular strong competitor in the m e d i u m and an even stronger one in the high diversity plots (see Naeem 1994). Indeed, one certain effect of high diversity is the increased chance of always having a particular species with high performance "at h a n d " in any particular environment. Large microgeographic variation was reflected in highly significant plot effects (Table II). This indicated the importance of using proper replication at the plot level because the effects of CO2 and biodiversity had to be compared with the variation among plots to obtain. significance tests (see Hurlbert, 1984).

CO 2

level

Ambient Elevated (---600 ppm)

Diversity treatment

Competitionfree tubes

5 species

12 species

31 species

12 plots 12 plots

4 plots 4 plots

4 plots 4 plots

4 plots 4 plots

40

Table II Results from Analyses of Variance of the Measured Quantitative Characters a N u m b e r of leaves (In) Source of variation

SS c

Cumulative leaf length (In)

pd

SS

P

(A) Without competition Block CO2 Plot Species CO2 • species

1 1 21 1 1

Block CO2 Biodiversity CO2 • biodiv. Plot Species CO~ • species Biodiversity • species CO2 • biodiv. • species

1 1 2 2 17 1 1 2 2

3.838 0.040 7.261 9.862 0.957

<0.001 >0.1 <0.001 <0.001 <0.05

1 1 21 1 1

3.724 0.078 19.352 15.218 0.587

<0.1 >0.1 <0.001 <0.001 >0.1

(B) With competition 28.907 <0.001 1.616 >0.1 1.595 >0.1 1.872 >0.1 9.372 <0.001 7.092 <0.001 0.005 >0.1 0.442 >0.1 1.229 <0.05

1 1 2 2 17 1 1 2 2

18.972 1.510 10.753 8.638 8.705 60.605 0.138 0.094 1.982

<0.001 >0.1 <0.01 <0.05 <0.05 <0.001 >0.1 >0.1 <0.1

Only the treatment and species effects are shown, the analysis of genetic variation within species is presented in Table 3. o degrees of freedom. cSS, sum of squares. dp, error probability. a

In contrast to the absence of main effects of CO2 there were significant interactions between this factor and biodiversity (cumulative leaf length), and among these two factors and species (number of leaves) (Table IIB). Thus, whereas the different levels of biodiversity could not be distinguished at ambient CO2, they had a differential effect on cumulative leaf length, presumably a good indicator of plant fitness, under elevated CO2: it was highest in the low-biodiversity treatment at elevated CO2 and lowest in the high-biodiversity treatment at elevated CO2 (Fig. 4A). The result demonstrates that the effect of diversity under elevated CO2 cannot be predicted from studying the effect at ambient CO2. The CO2-by-biodiversity interaction possibly reflected increased competition due to a positive response to elevated CO2 of some other species in the medium-biodiversity and even more so in the high-biodiversity treatments. Again it may be argued that in a larger set of species there is a greater probability that one species benefits more than proportionately from increasing CO2 concentrations but, again, this would neither be trivial nor would it invalidate the cautionary statement concerning predictions about biodiversity effects under elevated CO2. It

4. Variation in the Response of Plant Populations

41

-

~

loo

.~ ~_, g E~

4oo

~-"--~-'~-....~

\ \ \

P. grandiflora ~,.

Z

|

\ \

Cumulative leaf length (a) and leaf number (b) of the two Prunella species grown without competition or with competition at different levels of biodiversity and in ambient and elevated C02. Bar in lower left of upper graph in both (a) and (b) indicates one standard error of differences among means.

could also be argued that competition was greater under high diversity because there is reduced opportunity for escape by plasdc niche shifts. Prunella vulgaris responded negadvely to elevated C02 whereas P. grandiflora was not affected. Thus, the generalist species surprisingly was at

42

disadvantage compared with the specialist species at elevated CO2 in the competition-free tubes (significant 2-way interaction CO2-byspecies for number of leaves in Table IIA), as well as in medium- and highbiodiversity plots (significant 3-way interaction CO2-by-biodiversity-byspecies for number of leaves in Table IIB; see Fig. 4B). This is evidence against a high plasticity with regard to CO2 in and indicates either that this species is a generalist because of high genetic variability or that, with regard to CO2 as resource axis, the generalist-specialist distinction does not hold for the two species.

B. Genotypic Responses Significant differences among genotypes in a given environment or in response to environmental changes indicate the existence of genetic variation (broad-sense heritability). The amount of this genetic variation is the most important characteristic of a species in predicting its evolutionary potential for adaptation to environmental change because the expected shift in the mean of a character is directly proportional to its heritability (Bradshaw, 1984). We estimated the broad-sense heritabilities (H 2) of the investigated quantitative characters under ambient CO2, under elevated CO2, and over both levels pooled for plants growing both in the competition-free tubes (Table IliA) and in the diversity treatments (Table IIIB). The estimates for ambient and elevated CO2 were calculated from mixed-model analyses of variance as the quotient of the variance component due to differences among genotypes (s2) and the sum of this component and the residual variance (s2es) within plots (Falconer, 1989): 2 H(1,2)

=

s~ + S~Res

The pooled heritability was calculated as the quotient of the variance component due to differences among genotypes (s2) and the sum of this component, the component for the genotype-by-CO2 interaction (sZxco2), and the residual variance (S2Res)within plots: H~ / =

s~ s~ + s G2x C O

2

+ S2R~s"

A significant genotype-by-CO2 interaction indicates that there is heritability in the response tO elevated CO2 and that the slopes of the responses of the genotypes (reaction norms) are significantly nonparallel. An estimate of the heritability of this response to CO2, i.e., of the heritability of plasticity, can be obtained in an analogous way (see Scheiner and Lyman, 1989):

43

(ml))

(m2))

(m3))

(m4))

(0.05) b (0.11) (0.00)

(A) Without competition Ramet length (ln) Number of leaves (In) Cumulative leaf length (ln)

0.58 (0.40) (0.28)

0.52 (0.15) (0.28)

0.51 0.25 0.31

Ramet length (ln) Number of leaves (ln) Cumulative leaf length (ln)

0.57 (0.00) (0.00)

0.51 (0.25) (0.37)

(0.10) (0.00) (0.00)

0.45 (0.17) (0.27)

(B) With competition Ramet length (ln) Number of leaves (ln) Cumulative leaf length (ln)

0.38

0.31

0.33

(0.00)

(0.09)

(o.oo)

o.11

(o.oo)

0.26

0.14

0.20

(0.00)

Ramet length (ln) Number of leaves (ln) Cumulative leaf length (ln)

(0.00) (0.00) (0.09)

0.17 (0.05) 0.28

(0.04) (0.06) 0.15

(0.04) (0.00) (0.01)

a The response-heritability was calculated using the mean square of the CO2-by-genotype interaction from an analysis of variance. bValues in parentheses are not significant (P > 0.05).

S2XCO2 H~4) = -

s~ + s 2G•

2 + SLs

Significant genotype-by-CO2 interactions may occur in the following general cases (Fig. 5): (a) if a p p a r e n t genetic variation in a new e n v i r o n m e n t (elevated CO2) is increased c o m p a r e d to the present one (ambient CO2), (b) if a p p a r e n t genetic variation in a new e n v i r o n m e n t is decreased compared to the present one, or (c) if levels of variation in a new and the present e n v i r o n m e n t are similar but the rankings of the genotypes differ between environments. Case (a) might be expected if the new e n v i r o n m e n t (in this case elevated CO2) had never before been experienced and therefore stabilizing or directional selection could not have r e d u c e d heritability whereas it did so in the present e n v i r o n m e n t (Falconer, 1989). The opposite case (b) seems unlikely, because it would imply that the population is more precisely p r e a d a p t e d to the new e n v i r o n m e n t than to its present. Case (c) would be expected if some of the genotypes were better p r e a d a p t e d to the new e n v i r o n m e n t whereas other genotypes were better adapted to the

44

Three types of significant variations in slopes of reaction norms. Type (a) would be expected if selection had reduced apparent genetic variation in the present environment (but obviously not in the new one; for further explanation see text). The diagrams are drawn without main effects of C02, that is, the average slopes are not significantly different from zero.

present environment. This has often been observed in reciprocal transplant experiments involving two environments and has been referred to as a home-versus-away effect (Schmid, 1992). With regard to the two CO2 environments, however, this explanation can be ruled out because no genotype could already have experienced the elevated CO2 environment. Therefore, a crossing of reaction norms must be taken as an expression of unselected genetic variation. In the present study, some of the observed variation in morphological characters of the two species clearly had genetic causes. The highest heritabilities were found in the generalist and the lowest in the specialist (see Table III). This suggests a higher genetic variation in P. and is consistent with the view that this generalist, with wide character distributions, consists of many specialist genotypes, each with a narrower distribution than the entire species, and not of a few plastic genotypes. This also indicates a strong potential for the evolution of this generalist species with increasing CO2 and therefore agrees with the findings of others (Parsons, 1992) that u n d e r a global-change scenario, generalists, in this case should replace specialists, i.e., in the longer term. This long-term prediction is in contrast to the short-term advantage of observed here. The reaction norms of individual genotypes of the three species across the two CO2 treatments appear to represent a r a n d o m scatter of lines when plotted (Fig. 6). In particular, there was no consistent response to increased CO2 and no evidence for larger apparent genetic variation in the new than in the present environment (see Table III), as would have been expected if stabilizing or directional selection had reduced the heritability in the present environment (see discussion of Fig. 5). However, the reaction

4.

Reaction norms of replicated genotypes of (a) and (b) grown in competition-free tubes. The means of the lines are significantly different among each other in and the slopes of the lines are significantly different among each other in that is, this species expresses significant genetic variation in the response to CO2 (see also Table 3). Bars indicate standard errors of differences among means.

n o r m s of the genotypes did significantly differ in slope for r a m e t length in (see Table IIIA and Fig. 6). These differences in slopes, which c o r r e s p o n d to type (c) in Fig. 5, must be i n t e r p r e t e d as significant genetic variation in the response to increased CO2, but presumably with little adaptive value in the past. Nevertheless, because the genetic variation occurs in characters that potentially affect plant fitness, it can be expected that, everything else not considered, with the rising CO2 the genotypes " p r e a d a p t e d " to high CO2 will b e c o m e d o m i n a n t over and eventually replace the genotypes best a d a p t e d to the past and present atmospheric conditions. T h e r e d u c e d slope-heritabilities u n d e r competition (see Table IIIB) indicate, however, that the genetic variation that is a p p a r e n t without competition may be masked in the natural vegetation (see Bazzaz and Sultan, 1986).

C. Consequences for Predicting the Response of Ecosystems O u r results are consistent with results from a small n u m b e r of cases r e p o r t e d in the literature that also have shown that within single populations

46 of plant species variation in the response to elevated CO2 can be significant. Garbutt and Bazzaz (1984) found variation in the response to elevated CO2 among four populations of with regard to flowering dynamics, total number of flowers, final biomass, and total number of flowers per unit dry mass. At the genotypic level, the increase in the number of flowers and seeds under elevated CO2 was found to be genotype dependent in (Curtis 1994). Wulff and Alexander (1985) reported significant differences in growth and germination among progenies of five maternal lines of grown at ambient and doubled CO2 concentrations. Polley and co-workers (1995) found differential modifications of water-use efficiency among wheat cultivars induced by elevated CO2. The fact that some genotypes show a positive, some others a neutral, and yet others a negative response to increased CO2 has several important implications for research on the effect of rising CO2 and global change. Results from any study working with replicates of a single or a few genotypes per species may not be extrapolated to predict community-level responses, not even at the local scale of a single field site, because depending on the sampled genotypes the response of each studied species may vary from positive to negative! Two possible solutions to evaluating a species response are short-term experiments in which the reaction norm of a representative n u m b e r of genotypes is measured separately (this study) and long-term experiments which allow changes in the genetic composition of the species to be observed. Because of the existence of genetic variation in response to elevated CO2, anticipated global change to a large extent may be absorbed by evolution within species rather than lead to substitutions of species. Indeed, when the response lines of the two species are compared (Fig. 6), there is much overlap between the two species. It is known that for many species most genetic variation exists within populations, with small but significant components added among populations, races, etc. (Baur and Schmid, 1996). However, we lack information on whether this progression of decreasing size of variance components is continued at the abovespecies level, and we do not know how quantitative genetic variation is partitioned into components among and within functional groups of species (cf. comparative approach of Bell, 1989). Therefore, we cannot predict at which level the greatest changes will occur in response to rising CO2. Another implication of these results is that characters measured on individual plants and genotypes are more sensitive indicators of possible environmental impacts on ecosystems than characters measured at higher levels of organization because the response of a higher level is the result of many lower level responses that may differ in direction. Quite generally, the fact that studying single genotypes can be useful for indication of environmental change does not mean that such studies can also be useful for prediction.

4.

47

Osenberg (1994) have recently shown that in environmental monitoring, individual-based parameters perform better than chemical, physical, or population-based parameters.

It is becoming increasingly clear that genetic variation within species may play an important role in the response of plant communities and ecosystems to global change. This genetic variation makes it possible for species to evolve, that is, to adjust to environmental change by shifting their mean characteristics. Indirect evidence for the possibility of withinspecies evolution has been obtained by Dippery (1995) with Plants grown under very low CO2 were unable to set seed because of bud abortion. Although the CO2 concentration used in the experiment was one of the lowest that this species might have experienced, this suggests that it is now composed of genotypes that have become adapted to present levels of CO2 Further examples of genetic variation or evolution in response to increasing CO2 are presented (see Curtis Chapter 2; Kingsolver, Chapter 1; and Tousignant and Potvin, Chapter 3). The possibility of evolutionary changes in the characteristics of species under the selective pressure of increasing CO2 should therefore be considered in models that try to predict effects of global change on ecosystems. This will be necessary in particular when considering organisms with short generation times. Several questions remain to be answered before such evolution can correctly be predicted. First, as shown by the variable responses of different genotypes to elevated CO2, the expression of genetic variation can vary across environments. This cautions against premature conclusions, because the responses could be modified by other genotype-by-environment interactions, e.g., different weather conditions, competition, and pathogens. A second caveat is that negative genetic correlations can exist among characters. For example, the significant heritability of leaf number would be irrelevant if it were correlated with "compensatory" genetic variation in leaf size, resulting in zero heritability at the level of whole-plant fitness. This calls for further analyses of a large set of characters and the study of their correlations to better understand which traits are relevant to estimate individual fitness. In particular, the longer-term survival of the planted genotypes in the different experimental treatments needs to be assessed. Finally, in order to predict the effect of an increase of CO2 concentration on the evolution of a given species, the intensity of the selection pressure exerted by this increase will have to be compared with the effects of other evolutionary forces, whether selective (effect of increasing temperature, UV radiation, nitrogen depositions, frequency of extreme events) or not

48 ( r a n d o m genetic drift, for example), and take into account the existence of potential constraints such as photosynthetic pathways (C~, C4, CAM).

We propose that the response of ecosystems to global change, in particular increasing CO2, will d e p e n d mainly on the extent to which plant species adjust to new conditions by plasticity or evolutionary change, which d e p e n d s on genetic variation. We show that the possibility of extrapolating results of short-term experiments to long-term prediction d e p e n d s on the relative i m p o r t a n c e of these two processes. Moreover, if genetic variation exists within species in the response to elevated CO2, it will not be possible to predict evolutionary changes from heritability estimates m a d e u n d e r present atmospheric conditions. In a field e x p e r i m e n t we grew genotypes of two closely related grassland perennials without competition and with competition at three levels of biodiversity u n d e r a m b i e n t and elevated levels of CO2. T h e generalist P. genetically more variable but not more plastic than the specialist and was at a relative disadvantage u n d e r elevated CO2. Thus, the hypothesis that specialists should be replaced by generalists when the e n v i r o n m e n t changes was not supported in the short term in this exemplary case study. Long-term predictions about the response to environmental change will, however, be difficult according to our result because showed significant genetic variation in its response to increased CO2, indicating that its long-term response cannot be predicted from heritability estimates m a d e u n d e r present conditions. F u r t h e r m o r e , an effect of biodiversity on the growth of the two species was only visible at elevated CO2, indicating that biodiversity may b e c o m e more i m p o r t a n t as the envir o n m e n t changes. T h e existence of large genetic variation within populations in ecologically relevant characters demonstrates that species cannot be considered as constants in ecosystem studies and global change models. Characters m e a s u r e d at the level of the individual may therefore be more promising indicators of ecosystem change than higher level characters.

We thank C. K6rner, P. Leadley, I. Sanders, T Steinger, and their many co-workersfor excellent collaboration in this experiment. We also thank F. A. Bazzaz, C. K6rner, D. Matthies, A. McLellan, D. Prati, T. Steinger, and an anonymous referee for critical comments on the manuscript. This research was supported by the SwissPriority Programme (SPP) Environment of the Swiss National Science Foundation (Grant 5001-035229 to B. Schmid and B. Baur and by the Swiss Federal Office for Education and Science (Grant 93.0271 to B. Schmid and C. K6rner).

4.

49

Baur, B., and Schmid, B. (1996). Spatial and temporal patterns of genetic diversity within species. "Biodiversity: A Biology of Numbers and Difference" (K. J. Gaston, ed.). Blackwell Sci., Oxford, in press. Bazzaz, F. A. (1990). The response of natural ecosystems to the rising global CO2 levels. 21, 167-196. Bazzaz, F. A., and Sultan, S. E. (1986). Ecological variation and the maintenance of plant diversity. "Differentiation Patterns in Higher Plants" (K. Urbanska, ed.), pp. 69-93. Academic Press, London. Bell, G. (1989). A comparative method. 133. 553-571. Billings, W. D., Peterson, K. M., Luken, J. O., and Mortensen D. A. (1984). Interaction of increasing atmospheric carbon dioxide and soil nitrogen on the carbon balance of tundra microcosms. 65, 26-29. Billington, H. L., and Pelham, J. (1991). Genetic variation in the date of budburst in Scottish birch populations: Implications for climate change. 5, 403-409. Bradshaw, A. D. (1965). Evolutionary significance of phenotypic plasticity in plants. 13, 115-155. Bradshaw, A. D. (1984). The importance of evolutionary ideas in ecology--and vice versa. "Evolutionary Ecology" (B. Shorrocks, ed.), pp. 1-25. Blackwell Sci., Oxford. Bradshaw, A. D., and McNeilly, T. (1991). Evolutionary response to global climatic change. 67 (Suppl. 1), 5-14. Cheplick, G. P. (1995). Genotypic variation and plasticity of clonal growth in relation to nutrient availability in 83, 459-468. Curtis, P. S., Drake, B. G., Leadley, P. W., Arp, W. J., and Whigham, D. F. (1989). Growth and senescence in plant communities exposed to elevated CO2 concentrations on an estuarine marsh. 78, 20-26. Curtis, P. S., Snow, A. A., and Miller, A. S. (1994). Genotype specific effects of elevated CO2 on fecundity in wild radish 97, 100-105. deJong, G. (1990a). Genotype by environment interaction and the genetic covariance between environments: Multilocus genetics. 81, 171-177. de Jong, G. (1990b). Quantitative genetics of reaction norms. J. 3, 447-468. de Jong, G. (1995). Phenotypic plasticity as a product of selection in a variable environment. 145, 493-512. Dippery, J. K., Tissue, D. T., Thomas, R. B., and Strain, B. R. (1995). Effects of low and elevated CO2 on C3 and C4 annuals. I. Growth and biomass allocation. 101, 13-20. Falconer, D. S. (1989). "Introduction to Quantitative Genetics," 3rd ed. Longman, New York. Garbutt, K., and Bazzaz, F. A. (1984). The effects of elevated COz on plants. 98, 433-446. Grulke, N. E., Riechers, G. H., Oechel, W. C., and Laeger, C. (1990). Carbon balance in tussok tundra under ambient and elevated atmospheric CO2. 83, 485-494. Hess, H. E., Landolt, E., and Hirzel, H. (1972). "Flora der Schweiz," Vol. 3. Birkh~iuser Verlag, Basel. Huey, R. B., and Hertz, P. E. (1984). Is a jack-of-all-temperatures a master of none? 38, 441-444. Hurlbert, S. H. (1984). Pseudoreplication and the design of ecological field experiments. 54, 187-211. K6rner, C. (1995). Biodiversity and CO2: Global change is under way. 4, 234-243. K6rner, C., and Arnone, J. A. (1992). Responses to elevated carbon dioxide in artificial tropical ecosystems. 257, 1672-1675.

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Landolt, E. (1977). Okologische Zeigerwerte zur Schweizer Flora. 64, 1-208. Levins, R. (1968). "Evolution in Changing Environments." Princeton Univ. Press, Princeton, NJ. Lynch, M., and Gabriel, W. (1987). Environmental tolerance. 129, 283-303. Marshall, D. L., Levin, D. A., and Fowler, N. L. (1986). Plasticity in yield components in response to stress in and (Leguminosae). 127, 508-521. Milchunas, D. G., and Lauenroth, W. K. (1995). Inertia in plant community structure: State changes after cessation of nutrient-enrichment stress. 5, 452-458. Naeem, S., Thompson, L., Lawler, S. P., Lawton, J. H., and Woodfin, R. M. (1994). Declining biodiversity can alter the performance of ecosystems. 368, 734-737. Odum, E. P. (1989). "Ecology and Our Endangered Life-Support Systems." Sinauer, Sunderland, MA. O'Neill, R. V., DeAngelis, D. L., Waide, J. B., and Allen, T. F. H. (1986). "A Hierarchical Concept of Ecosystems." Princeton Univ. Press, Princeton, NJ. Osenberg, C. W., Schmitt, R.J., Holbrook, S. J., Abu-Saba, K. E., and Flegal, A. R. (1994). Detection of environmental impacts: Natural variability, effect size, and power analysis. 4, 16-30. Owensby, C. E., Coyne, P. I., Ham, J. M., Auen, L. M., and Knapp, A. K. (1993). Biomass production in a tallgrass prairie ecosystem exposed to ambient and elevated CO2. 2, 55-70. Parsons, P. A. (1992). Biodiversity and climatic change. "Conservation of Biodiversity for Sustainable Development" (O. T. Sandlund, K. Hindar, and A. D. H. Brown, eds.), pp. 155-167. Scandinavian Univ. Press, Oslo. Polley, H. W., Johnson, H. B., and Mayeux, H. S. (1995). Nitrogen and water requirements of C3 plants grown glacial to present carbon dioxide concentrations. 9, 86-96. Roughgarden,J. (1974). Niche width: Biogeographic patterns among lizard populations. 108, 429-442. Scheiner, S. M., and Goodnight, C.J. (1984). The comparison of phenotypic plasticity and genetic variation in populations of the grass 38, 845-855. Scheiner, S. M., and Lyman, F. (1989). The genetics of phenotypic plasticity. I. Heritability. 2, 95-107. Schmid, B. (1992). Phenotypic variation in plants. 6, 45-60. Schmid, B., and Weiner, J. (1993). Plastic relationships between reproductive and vegetative mass in 47, 61-74. Silander, J. A. (1985). The genetic basis of the ecological amplitude of II. Variance and correlations analysis. 39, 1034-1052. 39, Stearns, S. C. (1989). The evolutionary significance of phenotypic plasticity. 436-445. Stratton, D. A. (1994). Genotype-by-environment interactions for fitness of show fine-scale selective heterogeneity. 48, 1607-1618. Weber, M., and Schmid, B. (1995). Reductionism, holism, and integrated approaches in biodiversity research. 20, 49-60. Woltereck, R. (1909). Weitere experimentelle Untersuchungen •ber Artver~inderung, speziell ftber das Wesen quantitativer Artunterschiede bei Daphniden. 19, 110-192. Woodward, F. I. (1992). A review of the effects of climate on vegetation: Ranges, competition, and composition. "Global Warming and Biological Diversity" (R. L. Peters, and T. E. Lovejoy, eds.), pp. 105-123. Yale Univ. Press, New Haven, CT. World Conservation Monitoring Centre (1992). "Global Diversity: Status of the Earth's Living Resources." Chapman & Hall, London. Wulff, R. D., and Alexander H. M. (1985). Intraspecific variation in the response to CO2 enrichment in seeds and seedlings of 66, 485-460.

5 Genetic Variability and the Nature of Micro evolutionary Responses to Elevated CO2

There are four important questions one might pose regarding natural selection and increasing atmospheric CO2. First, is there genetic variability within plant populations on which rising CO2 might act? Second, how will rising CO2 affect the component processes of natural selection (namely, the expression of phenotypic variation in fitness, the degree to which this variation is heritable, and genetic covariance of other traits with fitness)? Third, what phenotypic traits will be favored under elevated CO2 conditions? And fourth, how will evolutionary changes affect plant community composition and ecosystem processes? Empirical studies addressing potential evolutionary implications of rising CO2 have primarily addressed the first question (Strain and Cure, 1985; Wulff and Alexander, 1985; Curtis 1994); the third and fourth questions have received some cursory attention in recent reviews (McLauglin and Norby, 1991; Roose, 1991; Strain, 1991; but see Geber and Dawson, 1993). This chapter addresses primarily the second question (which has received very little attention) and focuses on the direct effects of CO2 rather than indirect effects mediated by climate change. Our thesis is that an understanding of the impact of elevated CO2 on the component processes of selection is of central importance in predicting which traits are likely to be affected, and how selection of these traits may ultimately affect population, community, and ecosystemlevel processes. 51

Copyright 9 1996 by Academic Press, Inc. All rights of reproduction in any form reserved.

52

In examining the implications of rising CO2 to natural selection, a useful comparison may be made to the relatively well-studied case of heavy metal tolerance (Antonovics 1971; Baker, 1987; Shaw, 1991). Drawing on this work, Bradshaw and McNeilly (1991) present a simple conceptual model of the effects of global change on selection processes. This model has a fixed selection criterion: individuals displaying phenotypes above this threshold survive and reproduce, whereas other individuals do not (Fig. 1: Model 1). Bradshaw and McNeilly's primary intent in presenting this model is to point out the importance of genetic variation in determining the potential future success of a species under profound environmental change. A more genetically variable population will generally have a greater proportion of individuals falling above the selection criterion cutoff, and would thus be expected to be more successful under altered conditions. Selection for metal tolerance generally involves a direct and nearly typological response (tolerant versus intolerant genotypes). In contrast, selec-

Three possible modes of directional selection under anthropogenic environmental change.

5.

53

tion pressures under elevated C O 2 a r e likely to be indirect and nontypological. Selection under elevated CO2 is likely to be indirect in that the immediate effect on most genotypes in most species is enhanced vegetative growth mediated by higher carbon uptake (cf. Bowes, 1991). However, at the population level such overall growth enhancements are likely to enhance local competitive interactions (see also Bazzaz and McConnaughay, 1992). This would result in a greater importance of resources other than CO2 in limiting plant growth. Selection pressures under this scenario would thus be highly contingent on local-neighborhood conditions and local supply rates of other plant resources. These considerations suggest some alternative conceptual approaches to the "mode of selection" problem, such as those illustrated as Models 2 and 3 in Fig. 1. To include the importance of resource competition, one might assume that some constant proportion of individuals displaying the highest fitnesses in a given population successfully reproduce (Fig. 1: Model 2). Alternatively, to incorporate the idea that enhanced density dependence would be local, one might assume that a constant number of the most "fit" individuals successfully reproduce in subpopulations of varying size (Fig. 1: Model 3). Wallace (1968) originally used the terms "hard" versus "soft" selection to distinguish between Models 1 and 2, respectively. These terms have since been co-opted, and are now frequently used to refer to preversus postdispersal selection in multiple-deme models (e.g., Wade, 1985; Holsinger and Pacala, 1990). Model 3 corresponds in important respects to the idea of "sieve selection," used to describe selection under conditions of strong local density dependence (Antonovics 1973 cited in Antonovics, 1978; see also Wilson and Levin, 1986). One might assume that because selective pressures under elevated CO2 are indirect, they would also tend to be weak. On the other hand, selection for heavy-metal tolerance has been celebrated as a microevolutionary model in part because selection pressures are often very strong. In this regard it is useful to examine previous work on selection against metal tolerance in noncontaminated areas. In many respects selection against tolerance may provide a closer parallel to selection under elevated CO2, because selection is dependent more on differential growth and reproduction than on survivorship, and the intensity of selection is highly density dependent (Cook 1972; Hickey and McNeilly, 1975; see also Namkoong 1993). Under high-density a n d / o r high-productivity situations, metal-tolerant genotypes are at a strong disadvantage. These genotypes can generally persist only under conditions of low competitive pressure. Observations of the incidence of metal tolerance along environmental gradients also suggest that density-dependent selection against metal tolerance may be quite strong (McNeilly, 1968; MacNair 1993). Along similar lines, Davies and Snaydon (1976) compared selection pressures on grass species

54

in the Park Grass Experiment, involving long-term fertilizer and liming treatments in plots maintained over more than 50 years. In general, greater coefficients of selection were found under conditions of higher overall plant growth. In summary, although not directly addressing the case of CO2, previous studies clearly indicate that indirect selection pressures mediated by competitive interactions can be very strong in natural plant populations. We have argued that the mode of selection under elevated CO2 will generally differ from selection for heavy metal tolerance and similar forms of anthropogenic change involving typological, noncontingent responses. Two other important general properties of a selective regime are its directionality and its spatial extent. With regard to the latter, selection for metal tolerance is generally local in scale, with a high probability of introduction of new genetic information from plants outside of the affected area (e.g., McNeilly, 1968; MacNair 1993). In contrast, selection under elevated CO2 is truly global in scale, affecting all extant plant populations. With the exception of "temporal migration" from seed banks, there will be no introduction of nonselected genetic material as plants evolve under rising CO2. Like selection for metal tolerance, elevated CO2 is likely to primarily result in directional selection, as opposed to stabilizing or disruptive selection. The global ambient CO2 concentration averaged over an annual interval is monotonically increasing (Houghton 1992). This progressive, gradual nature of CO2 increase does contrast markedly with selection for metal tolerance. Models of evolutionary responses to rising CO2 will thus need to consider genetic variation in responses across a range of CO2 levels. Additionally, there is a well-documented correlation between seasonal variation in CO2 and average CO2 concentrations, especially at high latitudes (e.g., Tans 1990). The selective regime under rising CO2 could thus involve some increase in variance associated with an increase in the mean. However, the amplitude of this variation is small relative to overall rise in CO2 levels. Moreover, winter peaks in CO2 are unlikely to be of importance since most plants are photosynthetically dormant during this period (thus driving the seasonal oscillations in atmospheric CO2). Higher winter peaks in CO2 may, however, be of some selective consequence in species showing pronounced photosynthetic activity during this period, such as winter annuals or winter-photosynthesizing conifers.

A. Conceptual and Mensurational Issues Natural selection is contingent on heritable variation. This raises the question of how we can best detect and measure genetic variability in C02

5.

55

responsiveness. In answering this question, it is first important to note that "CO2 responsiveness" at the whole plant level is not a trait expressed by an individual, but is rather an aspect of a plant's " n o r m of reaction" (i.e., the expression ofa phenotype across environmental states) (Schmalhausen, 1949). A second important point is that we are principally concerned with genetic variability in fitness-related traits, such as lifetime reproductive output. Much existing work on whole-plant responses to elevated CO2 focuses on vegetative aspects of plant growth and development, and thus may not be of direct relevance. Genetic variability in CO2 response may be detected rather simply as an interaction term in analysis of variance (e.g., Curtis 1994). However, such interactions are generally scale dependent, and also do not serve to measure the degree of genetic variability. Heritability coefficients quantify the proportion of variation in phenotypes that may be accounted for by genetic variation (Falconer, 1989): "narrow-sense" heritabilities measure the additive genetic c o m p o n e n t of variance, whereas "broad-sense" heritabilities measure the total variance accounted for by all genetic effects (i.e., additive, epistatic, and dominance components). It is sometimes of interest to quantify heritabilities for traits that summarize responses across environments. For this purpose clonal propagules or siblings may be grown in each environment, and heritabilities are calculated for the relative or absolute differences in mean performance across environments. Although this approach has been c o m m o n in studies of herbicide and metal tolerance, such measures are compromised by problems of both interpretation and analysis. For example, heritability values for metal resistance measured in this way commonly reflect variability in control populations rather than in experimental populations (MacNair, 1991). It is important to stress that for most purposes the heritability of responsiveness per se is not of direct interest. Rather, we wish to know the heritability of each trait in each environmental state, and the genetic covariances between traits measured in these different states (Falconer, 1952; Via and Lande, 1985; Via, 1987; see also Roose, 1991). Plant growth responses to elevated CO2 have most often been quantified in terms of response ratios, the conventional measure being the ratio of whole-plant biomass at 700/350 ppm CO2 (cf. Kimball, 1983; Cure and Acock, 1986; Poorter, 1993; Ceulemans and Mousseau, 1994). Similar data have been reported for intraspecific variation (Wulff and Alexander, 1985; Curtis 1994). From a comparative perspective, a fundamental problem with this measure is that it will generally vary through plant ontogeny. This ontogenetic variation arises inevitably from the sigmoidal nature of plant growth. To understand why this is so, consider two plants, one at ambient and one at elevated CO2, and both showing logistic growth. The biomass ratio (/3) as a function of time (t) would be:

56

where the constants Khi and/~o are asymptotic biomass values at elevated and ambient CO2, respectively, rhi and ~io are the corresponding initial relative growth rate parameters, and No is initial biomass. If rhi -- ~io then /3 will remain constant through ontogeny, being determined primarily by the ratio of/<,i to / ~io, the function will always be " h u m p e d " in form, displaying a local maxima at an intermediate value of t. Physiologically, enhanced carbon gain at elevated CO2 is directly linked to early growth rate, providing a strong expectation that rhi > ~io.Therefore, we can generally anticipate that differences in plant size (either relative or absolute) between CO2 levels will increase early in plant ontogeny. In contrast, the physiological basis for predicting effects on asymptotic maximal size is much less clear. Thus, as growth approaches an asymptote under both environmental conditions, the ratio may often decrease and approach a constant value. In order for the "response ratio" to remain constant throughout plant ontogeny, plant growth would have to be linear, which it is not (Causton and Venus, 1981). More generally, these patterns indicate that no single summary statistic, such as a response ratio, can adequately summarize effects of CO2 on plant "growth." Plant growth curves generally must be specified by at least two parameters (cf. Causton and Venus, 1981). It therefore follows that growth responses must also be quantified by at least two parameters, such as those describing effects on early exponential growth, and effects on asymptotic size. Empirical studies that have conducted detailed growth analyses under varying CO2 levels have generally found such " h u m p e d " patterns of response through ontogeny (e.g., Rogers 1984; Tolley and Strain, 1984; Bazzaz 1989; Coleman and Bazzaz, 1992; Tremmel and Patterson, 1994; Walters 1993; see also Fig. 2). Moreover, these analyses indicate that peak size differences are reached at different times for different species. Therefore, no single time frame during development can be used for comparison. Any effort to understand variation within or among species in CO2 growth responses should take these basic ontogenetic patterns into account. Most experiments on CO2 growth responses report only final harvest measurements, however. Also, the majority of studies focus overwhelmingly on early growth. For example, the median growth interval of studies reviewed by Poorter (1993) is 43 days. From a microevolutionary standpoint, some researchers have argued that growth trajectories should generally be treated as "infinite-dimensional" characters, in which the phenotype of an individual is treated as a function (of arbitrary form) rather than as a finite set of measurements (Kirkpatrick and Lofsvold, 1989, 1992). The variance-covariance matrix of a trait mea-

57

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Growth curves (left panels) and response ratios (right panels) for three genotypes of u n d e r a m b i e n t a n d elevated CO2 conditions. In the first set of panels, o p e n symbols indicate plants at a m b i e n t CO2 (350 p p m ) , closed symbols plants at elevated CO2 (700 p p m ) .

sured at several points in time yields eigenvalues and eigenfunctions, and their magnitude and shape, respectively, indicate which evolutionary modifications in growth trajectories are more or less likely. For several reasons, this general approach is well suited to describing and modeling genetic variation in plant growth responses to CO2. In particular, a growth equation (such as the logistic) need not be assumed a priori, and the evolutionary response of the entire growth trajectory can be modeled (cf. Kirkpatrick 1990). Moreover, the infinite-dimensional formalism can be similarly extended to treat the evolution of norms of reaction (Gomulkiewicz and Kirkpatrick, 1992), such as response to CO2 levels treated as a continuous function. Models of this sort yield insights into evolutionary dynamics of traits (see below for an example of such an analysis) and would also be of particular use in projecting evolutionary changes under conditions of

58

gradually increasing C O 2. The primary disadvantage of this approach is the need for very large data sets to parameterize models (i.e., data on the continuous growth of plants of known ancestry at a range of CO2 levels). It should also be emphasized that current models of the evolution of growth trajectories have not incorporated density- or frequency-dependent processes. Although reproductive responses are of primary importance from an evolutionary perspective, the vast majority of existing comparative data on whole-plant responses to CO2 focus on vegetative growth. Reproductive output is often closely correlated with vegetative biomass and other measures of plant size in herbaceous plants (e.g., Samson and Werk, 1986; Weiner, 1988; Kawano 1989; Hartnett, 1990). However, there are a variety of experimental results suggesting effects of elevated CO2 on reproduction that are disdnct from vegetative growth enhancement (see, e.g., Ziska and Teramura, 1992; Enoch and Honour, 1993; Ackerly and Bazzaz, 1995; Bazzaz 1995a). Reekie (1994) provide evidence that long-day plants generally display accelerated reproduction at elevated CO2, whereas short-day plants exhibit delayed reproduction. Either accelerated or delayed reproduction may result in altered patterns of reproductive allometry under elevated CO2. There may also be changes in seed quality under elevated CO2 (Garbutt and Bazzaz, 1984; Farnsworth and Bazzaz, 1995). Further work on these issues is called for, particularly multiplegeneration experiments. However, it is clear that differential vegetative growth may not be a safe basis by which to infer evolutionarily relevant variation in responses to elevated CO2. In summary, studies of C O 2 effects on plant growth have generally taken what is inherently a multidimensional problem, and reduced it to a single dimension (i.e., the "response ratio"). Future work aimed at understanding either intra- or interspecific variation in CO2 effects on plant growth should account for the variation of effects through plant ontogeny, and also across the range of CO2 levels to be encountered by plant populations. Additionally, there is evidence that reproductive responses to elevated CO2 may often diverge from vegetative responses. Attempts to understand the evolutionary implications of rising CO2 should therefore directly examine proximate fitness measures such as lifetime reproductive output. B. Empirical Data on Variation within and among Species The preceding discussion points to the general importance of growth analyses and reproductive data in studies of evolutionary responses to CO2. In what follows, we will make extensive use of data from a recent experiment characterizing norms of reaction of Medic. genotypes to CO2 and conspecific density. Detailed methods and results of the study will be presented in full elsewhere (S. C. Thomas, M. Jasiefiski, and F. A.

5.

59

Bazzaz, manuscript in preparation; see also Bazzaz 1995). In brief, the study incorporated a fully crossed design using 8 genotypes grown individually in 2-liter pots and in dense, monospecific stands, under elevated (700 ppm) and ambient (350 ppm) CO2 conditions. The experiment was conducted in a controlled-environment facility at Harvard University, and each CO2 level was represented by three spatially interspersed blocks. Each block had 4 replicate individual and 12 replicate high-density plants for each genotype. Available soil volumes and nutrient input levels were matched to those of eastern Massachusetts. The genotypes were selfed progeny of cloned plants that had previously been systematically sampled from a natural population. Growth analyses were based on allometric estimates of biomass derived from destructive harvests of plants grown under similar conditions. The importance of growth analysis in understanding genetic variation in whole-plant responses to CO2 is well illustrated by the data shown in Fig. 2. (Note that each point represents an average of 24-36 replicate plants.) Genotype A shows a pronounced early growth enhancement and a positive, though smaller, enhancement in final size. The biomass response ratio thus declines from near 2 to 1.2. In contrast, genotype C shows a very strong early growth enhancement, but considerably smaller final biomass at elevated than at ambient CO2 levels. The biomass response ratio thus declines from near 3 to less than 0.6. (Losses in estimated biomass late in ontogeny reflect leaf drop during fruit development in this species .) The general " h u m p e d " pattern of response shown in these three genotypes was seen in all genotypes at both density conditions. Given the range of variation in biomass response ratios seen within a single species, much of the variation in CO2 responses reported among species could actually represent intraspecific variation that is either genetic or ontogenetic in nature. This point is dramatically illustrated by the range of variation in CO2 response found among genotypes sampled from an Illinois old field (Fig. 3). The overall distribution of growth enhancement ratios, pooling all genotypes and sequential measurements, is statistically indistinguishable (G test: P > 0.05) from the distribution of response ratios across 155 species reported by Poorter (1993). In order to partition variation in CO2 responses into within and between species components, the minimal data requirement would be growth analyses of genotypes within some sample of plant species. Ideally, such data should also encompass a range of environments for each species, so as to allow an evaluation of the relative importance of"environmental" variation in CO2 responsiveness. Unfortunately, no such data set yet exists. Existing data do give some indication that genetic variation in CO2 responsiveness is actually large, relative to variation among species. Table I lists the conventional "response ratios" for genotypes in four studies investigating genetic

60

F i g u r e 3 Distributions of CO2 growth " e n h a n c e m e n t ratios" (biomass at 700 p p m / b i o m a s s at 350 ppm) for 8 genotypes of pooling 7 weekly measurements and 2 density treatments (top), and 155 plant species compiled by Poorter (1993) (bottom). The 2 distributions do not differ significantly (G test for homogeneity: P > 0.050).

variation in CO2 responses in annual plants. Table II gives the result of a mixed model analysis of variance that partitions variance in response ratio within and among species, and among environmental states. For each

Species

Env.

Genotypes

Range of response

Reference

2 nutr. 2 nutr. 1 only

4 6 5

0.47-2.37 0.25-1.37 0.93-1.39

Wulff and Alexander, 1985 Fajer 1992 Curtis 1994

2 dens.

8

0.30-1.40

Thomas manuscript in preparation

a Responses are calculated as the ratio of plant performance at 700/350 ppm for the most proximate fitness characteristic measured. The ranges reported are pooled across environments in studies for which measurements were made under different environmental treatments.

61

5.

Effect

d.f.

SS

MS

F

P

Species Environment Genotype Error Total

2 1 16 21 40

0.120788 0.377143 3.80075 2.31536 6.83487

0.060394 0.377143 0.237547 0.110255

0.25424 3.4206 2.1545

0.7786 0.0785 0.0502

For this analysis environmental treatments were classified as "good" (high nutrient or low density) vs "poor" (low nutrient or high density).

species the most proximate fitness measure was used (i.e., either final total reproductive or vegetative biomass). Also, in three of the four studies multiple environmental states were measured. For the purposes of the analysis, these were scored as "favorable" (high nutrients or low density) or "unfavorable" (low nutrients or high density). This preliminary analysis suggests that intraspecific variation exceeds interspecific variation: 56% of total variance in response ratio is explained by genotype, approximately 6% is explained by environmental state, and less than 2% is explained by species. The genotype term approaches significance at the P < 0.05 level, while the environment term is also marginally significant. Existing data thus suggest that intraspecific variation in responses to elevated CO2 is very substantial, perhaps even greater in magnitude to interspecific variation. However, we emphasize that this preliminary analysis does not take into account the important issue of ontogenetic changes in growth enhancement. Additionally, models that incorporate CO2 effects in the context of local resource competition would be necessary to rigorously evaluate the relative importance of genetic change versus change in species composition under rising CO2.

A. A Quantitative Genetic Framework Quantitative genetic models represent a potentially powerful tool for understanding the evolutionary dynamics under global change (e.g., Lynch and Lande, 1993). A central assumption of these models is that phenotypic traits of interest are determined by many genes of small effect (MitchellOlds and Rutledge, 1986; Falconer, 1989). However, there are important cases of evolutionary responses to anthropogenic disturbance in which

62

single locus changes have very large effects (such as copper tolerance in (MacNair, 1977, 1991). It is within the range of possibility that single genes could also have large effects on CO2 responses. For example, Musgrave (1986) examined CO2 responses in pea hybrids differing in the presence vs. absence of the cyanide-resistant respiratory pathway. Presence of the pathway was associated with a very low growth response to CO2, the explanation offered being that carbohydrate production was respired in hybrids possessing the pathway. Many metric traits display a right-skewed distribution of gene effects, with some degree of "major gene" influence as well as many genes of small effect (Hill and Caballero, 1992). It seems likely that CO2 responses would have a similar distribution of gene effects; however, studies addressing the genetic basis of CO2 responses in natural plant populations are entirely lacking. In the simplest quantitative genetic models of selection, the rate of change in fitness is a product of the heritability of fitness, and the relative variation in fitness [Eq. (2a)]. The response of some trait correlated with fitness may be estimated by substituting the product of fitness heritability and the covariance of the trait with fitness in this expression [Eq. (2b)]. The "Chicago school" multivariate quantitative genetic models of selection essentially extend this expression to predict selection on a set of traits, incorporating a genetic variance-covariance matrix in the place of the heritability term (Lande, 1979, 1982; Arnold and Wade, 1984) h2 h2

(2a)

2 2.

(2b)

Here R or R' is the selection rate on fitness or on a correlated trait, respectively; h2 is narrow sense heritability, V~ is variance in fitness, W is mean absolute fitness before selection, and ~ is the covariance of a given 2 is simply the square of the trait with fitness. Note that the term coefficient ofvariance of fitness (cf. Thomas and Bazzaz, 1993). The product h2 2 is sometimes called the "opportunity for selection" (denoted I), and has been used as a measure ofevolvability (Crow, 1958; Houle, 1992). Elevated CO2 may potentially affect the selection process by systematically altering some or all of the variables in these expressions, namely, the relative variance in fimess within local populations, the heritability of fitness-related traits, and the genetic covariance of particular traits of interest with fitness. In the subsequent sections, these parameters are addressed in turn.

B. Phenotypic Variability Rising C O 2 may affect the selection process simply by altering the degree of phenotypic variability in fitness related traits. One mechanism by which this could occur is the acceleration of size differences due to enhanced

63

5.

overall growth. In the exponential phase of plant growth, small differences in growth rates among individuals result in exponential increases in size differences. Over time an even-aged set of plants that displays a normal distribution of seedling sizes will show increasing relative variation (Koyama and Kira, 1956; Uchmafiski, 1985). The addidon of any resource is expected to accelerate this process. By this reasoning, one would expect greater phenotypic variability in size in plant populations under elevated CO2. However, the sigmoidal nature of plant growth modifies this expectation. Plants grown at higher resource states may reach asymptotic sizes earlier, which could potentially result in decreased variability in asymptotic size or reproductive output under high resource conditions. A second mechanism by which elevated CO2 could influence phenotypic variability in plant size and reproductive output is by accelerating competitive interactions for other plant resources. In general, size variability increases through stand ontogeny in even-aged plant monocultures (e.g., Thomas and Weiner, 1989), and monocultures growing at higher densities display greater variability in plant size (Weiner and Thomas, 1986). Addition of nutrients and other resources often results in greater variation in size and reproductive output (Weiner, 1985; Rice, 1990). Elevated CO2 might similarly result in increased size variability. Morse and Bazzaz (1994) specifically addressed this issue in experiments with stands of two annual plants. Their results provide some evidence that elevated CO2 may accelerate size hierarchy formation and self-thinning. However, from an evolutionary perspective, it is of greatest interest to examine variability in reproductive output, rather than in size. Table III

C.V. of final total seed mass

Opportunity for selection (I)

Broad-sense heritability (H 2)

Response to selection (R)

350 p p m

0.557

Individually grown 0.31

0.052 ,

0.016

700 p p m

0.400

0.16

0.236

0.038

350 p p m

1.442

H i g h density 2.08

0.050

0.104

700 p p m

1.752

3.07

0.104

0.320

Statistical significance of differences were tested using a boot-strapping approach (cf. Thomas and Bazzaz, 1993), with 2000 iterations for each test. * Indicates pairwise comparison is significant at P > 0.05. Based on Bazzaz 1995. a

64

3,1.

presents data from the experiment. The data are consistent with the hypothesis that enhanced competition results in higher variability in fitness under elevated CO2: a significant difference in the coefficient of variation of final seed mass was found at high density, though not for individually grown plants. Not all species show such a pronounced response, however (S. C. Thomas, M. Jasiefiski, and F. A. Bazzaz, unpublished data).

C. Heritability The heritability of fimess-related traits is expected to be close to zero, as selection will operate to remove genetic variance for such traits (Fisher, 1930). Nonzero heritabilities may commonly be maintained by negative genetic correlations among a set of fitness-related traits. However, if traits are expressed in an evolutionarily novel environment in which selection has had no opportunity to act, then heritabilities may be much higher even in the absence of "trade-offs" among fitness components (e.g., Service and Rose, 1985). This raises the central issue of whether or to what degree elevated atmospheric CO2 (i.e., in the 350-700 ppm range) constitutes an evolutionarily novel environment. From a very long-term paleoecological perspective, CO2 levels were considerably higher in the geological past (B6ger, 1980; Spicer and Corfield, 1992). However, the past 160,000 years have been a period of relatively low atmospheric CO2 levels (Barnola 1987). Life spans of terrestrial plants vary in general from less than 1 year to several hundred years (Harper and White, 1974). Because the majority of plant species are iteroparous, generation times are generally much shorter. If changes in CO2 concentrations have directly or indirectly resulted in even modest selective effects (e.g., selection coefficients of order 0.00010.01), then there has almost certainly been sufficient time for preindustrial low CO2 levels to have eroded genetic variance related to earlier evolutionary processes driven by high CO2. The idea that rising CO2 constitutes an evolutionarily novel environment also depends on the nature of the selective regime generated. As noted above, the selective impact of rising CO2 may generally be expressed indirectly, particularly by exacerbating competitive interactions for other resources (as well as through the indirect effects of CO2-forced climatic change). In a review that briefly addresses this issue, Roose (1991) suggests that "these secondary effects of increased CO2 do not create novel environments, but rather environments which already occur elsewhere" (p. 122). There are several strong arguments against this view. First, almost any "novel" selective pressure is novel only locally, not globally. To take the paradigmatic example, mining activities expose heavy-metal-rich soils of a sort that generally already occur elsewhere; yet this does not alter the fact that local populations colonizing mine-spoils may have high genetic variance in fitness components due to a lack of previous heavy-metal expo-

5.

65

sure. Second, competitive regimes generated by altered C O 2 levels may indeed be qualitatively novel. For example, if plant monocultures are able to sustain a higher leaf area index under elevated CO2, then this could generate a qualitatively novel light environment under the canopy of a given species. Along these lines, one study detected substantial effects of CO2 on red-far red ratios of light transmitted through a canopy (Arnone and K6rner, 1993). Rising CO2 could also act as a novel evolutionary environment through its effects on plant development. Two general classes of developmental effects may be of importance in this regard. First, CO2 has known biochemical interactions in plants that are not mediated by the carboxylase activity of rubisco. For example, CO2 is directly involved in the regulation of ethylene biosynthesis (e.g., Horton, 1985; Cheverry 1988). Also, CO2 binds to rubisco to create the active form of the enzyme, and also regulates the activity of rubisco activase (for a review see Bowes, 1991). Second, elevated CO2 may have important novel effects on plant development that arise from increased carbon accumulation. One notable example is changes in nonstructural carbohydrate chemistry. For example, wheat shows a qualitatively different pattern of fructan accumulation under elevated CO2, with large amounts synthesized very early in ontogeny (Smart 1994). Completely novel carbohydrates are synthesized by certain conifer species at elevated CO2 (H. Lee, personal communication). Such quantitative and qualitative changes in carbohydrate chemistry may have important and novel effects on plant morphogenesis. One possible example of such an effect is dramatic changes in leaf form seen in (Fig. 4). Under elevated CO2 plants produced exaggerated "sun-leaf" morphologies, with significant changes in leaf length and degree of dentition. An alternative perspective on fitness heritabilities under rising CO2 derives from studies of genotype-specific performance under varying competitive regimes. A variety of studies indicate that competition in plant populations is often asymmetric with respect to size: large individuals usurp resources at the expense of small individuals (Lomnicki, 1988; Weiner, 1990). This phenomenon has the potential to greatly amplify small differences in size among individuals in a population, particularly in even-aged stands. Differences in size early in plant ontogeny may generally be largely due to microenvironmental heterogeneity. The amplification of early size differences may therefore act to enhance environmental variation in plant performance. This reasoning leads to a prediction of lower heritabilities for size under conditions of enhanced competition, such as at high density (Thomas and Bazzaz, 1993). Higher resource levels would also be expected to result in earlier and more intense competitive interactions. By this reasoning, one might expect reduced heritabilities for fitness-related traits under elevated CO2.

66

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To summarize these arguments, there is strong reason to believe that increasing CO2 levels could act as an evolutionarily novel environment, perhaps most importantly through effects on plant developmental processes. This is expected to be associated with increased genetic variability in fitness-related traits at elevated CO2. However, accelerated competitive interactions may under some conditions act to increase the importance of small-scale environmental sources of variation in plant performance. This effect may act to reduce genetic variability in fitness-related traits at elevated CO2. Do trait heritabilities actually respond to elevated CO2? Data from the experiment indicate a consistent pattern of higher heritabilities at elevated CO2 than at ambient CO2 for final seed mass (Table III). This pattern is most pronounced for the individually grown plants, although high-density plants show a nonsignificant trend in this direction. Heritabilities at either CO2 level are also generally lower at high density. The overall pattern is consistent with the idea that accelerated competitive interactions may enhance the role of "environmental noise" in determining plant performance (cf. Thomas and Bazzaz, 1993). There is thus some evidence

5.

67

that both "evolutionary novelty" and "environmental noise" may play important roles in determining heritabilities of fitness-related traits under elevated CO2. D. Genetic Correlation Structure

Responses of a given trait to selection depend on the covariance of that trait with fitness. More generally, the response to selection of any set of phenotypic characteristics will depend on the overall genetic variancecovariance structure (Lande, 1982; Falconer, 1989). An ultimate task, however, is to establish a connection between quantitative-genetic estimates of variation and covariation of traits, developmental processes, and functional relationships of traits (Riska, 1989). Only then will we be able to provide mechanistic explanations of the evolution of suites of traits in novel environments (Chapin 1993). Such limitations notwithstanding, quantitative genetics of covariances among traits continues to be a basic framework for evolutionary considerations. The verdict is still out, however, as to the feasibility of using phenotypic correlations among traits in lieu of, more difficult to obtain, genetic correlations (Cheverud, 1988; Willis 1991; Roff, 1995). Although genetic variance-covariance structure is often treated as constant in quantitative genetic models, it is not fixed. There is a substantial literature that examines changes in genetic correlation structure with environmental conditions (e.g., Giesel 1982; Itoh and Yamada, 1990; Wilkinson 1990). (Although genetic covariances are directly used in calculating selection effects, comparative analyses are often conducted with genetic correlations.) In plants, changes in genetic correlation structure have been best documented with respect to changes in local density (Geber, 1990; Mazer and Schick, 1991; Thomas and Bazzaz, 1993; but see Shaw and Platenkamp, 1993; see also Young 1994). A body of theoretical work exists regarding expected changes in genetic variance-covariance structure under selection and drift (Crow and Kimura, 1970, pp. 236-239; Avery and Hill, 1977, 1979; Turelli, 1988). However, less attention has been given to possible effects of environmental changes, novel or otherwise. The statement has even been made that " . . . theory cannot predict whether the environmental changes that select for new phenotypes will change environmental or genetic covariances" (Turelli, 1988, p. 1344). One possible basis for prediction may, however, stem from observations that functionally or developmentally related traits generally show high (positive or negative) genetic correlations (e.g., Clark, 1987; Cowley and Atchley, 1990). One might predict in a novel environment of any sort that functionally related genetic correlation structure would tend to weaken. Similarly, environmental changes altering developmental processes could result in an overall lowering of absolute values of genetic

correlations. Another possibility is that changes in genetic variance in fitness could affect relationships between fitness correlates and other traits simply by altering overall phenotypic variance. Specifically, given some underlying genetic relationship, an increase in variance in one trait could result in increased genetic covariance with another trait. The sign of such covariance, however, is hard to predict, especially in traits whose phenotypic expression depends on the allocation of a single resource (van Noordwijk and deJong, 1986; de Jong and van Noordwijk, 1992). The empirical data on allow for a preliminary analysis of effects of elevated CO2 on genetic correlation structure (Fig. 5). In spite of the relatively small sample size (in terms of numbers of genotypes), both statistically significant genetic correlations and statistically significant differences between CO2 treatments are detected. At both ambient and elevated CO2 there are high positive genetic correlations between final size metrics: namely, height, leaf area, and biomass. Also in both treatments there is a high negative genetic correlation of these characteristics with seed size (mass). However, while at ambient CO2 initial relative growth rate shows a strong positive genetic correlation with final size characteristics, this correlation is very weak at elevated CO2. Genetic correlations of any of the traits examined to the most proximate fitness measure (final fruit mass) do not attain statistical significance (P < 0.05) for either COz level. However, there is a suggestive negative genetic correlation of final plant height with fruit mass that is considerably higher at elevated CO2. Overall, genetic correlations appear to be somewhat weaker under elevated CO2 conditions. These observations suggest surprisingly large effects of CO2 on genetic correlation structure; however, we emphasize that in this preliminary analysis we have not performed a conservative pooled test for the entire character matrix (cf. Shaw, 1991b). Long-term responses to selection may often be determined by fitness differentials, rather than genetic correlation structures, unless genetic correlations are very high (e.g., Via, 1987; Zeng, 1988). This point is of some interest from the perspective of evolutionary responses to a relatively sudden environmental change such as rising CO2. Although fitness maximization may prevail over the long term, it is likely that effects of genetic correlation structure will be especially pronounced over the first several generations of selection. This points to the importance of further studies aimed at elucidating genetic correlation structure and its consequences of evolution under rising CO2.

It has commonly been assumed that traits directly involved in physiologi cal responses to C02 may respond evolutionarily to rising C02. Thus, a priori

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69

Effects of elevated CO2 on genetic correlation structure in Data are for individually grown plants. Black bars indicate significant positive genetic correlations; white bars indicate significant negative correlations. Hatched bars indicate nonsignificant positive correlations; stippled bars indicate nonsignificant negative correlations. Genetic correlations were calculated as Pearson product-moment correlations between genotypic means. Bar width is proportional to the absolute value of the correlation.

predictions regarding expected evolutionary responses may be derived from considerations of optimal allocation patterns. For example, one might e x p e c t e v o l u t i o n a r y r e s p o n s e s involving c h a n g e s in n i t r o g e n a l l o c a t i o n f r o m r u b i s c o to e i t h e r d a r k cycle e n z y m e s i n v o l v e d in R U B P o r p h o s p h a t e

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regeneration (Bowes, 1991,1993; Stitt, 1991 ) or to light-harvesting molecules such as chlorophyll. However, there is presently a complete absence of studies addressing genetic correlations of such physiological traits with reproductive output under elevated CO2. Similarly, it is not clear that evolutionary responses ofstomatal density will match developmental responses of individual plants (see Beerling and Chaloner, 1993). Reported long-term trends in stomatal density (e.g., Woodward, 1987; Pefiuelas and Matamala, 1990) may or may not involve genetic change. It also cannot be assumed that either net photosynthesis orvegetative growth responses to CO2 will necessarily increase as plants evolve under rising CO2. For example, there is a negative genetic correlation offruit production with final plant height observed in the population under elevated CO2 (Fig. 5). The predicted short-term selective response would thus be for plants of smaller final stature. If rising CO2 levels generally act to exacerbate competitive interactions within and among plant species (Bazzaz and McConnaughay, 1992), one might expect CO2 to favor traits that are also favored under conditions of high density or high productivity. Such traits may include early germination, rapid early growth, delayed reproduction, and increased stem allocation, among others (e.g., Thomas and Bazzaz, 1993). A second a priori hypothesis is that selection under elevated CO2 will often involve amelioration of "nonadaptive" plastic responses. Consider, for example, species that show strong developmental effects, such as altered reproductive timing (cL Reekie 1994). Genots, pes that retain a flowering schedule more closely matched to their current seasonal pattern might be strongly favored under rising CO2. Similarly, forms of that do not develop exaggerated sun leaves under elevated CO2 (see Fig. 4) may be differentially favored. Future studies should be cognizant of possible indirect selective pressures brought about by enhanced competitive interactions and also by developmental effects of rising CO2. The potential for evolutionary change in plant traits can also be explored through an analysis of their covariance structure during ontogeny (Kirkpatrick 1994). In the case of per-plant leaf area measured in at six points in time, the eigenfunction associated with the dominant eigenvalue did not change sign in high-density populations, at either CO2 level (Fig. 6; M. Jasiefiski, S. C. Thomas, and F. A. Bazzaz, manuscript in preparation). This means that selection for an increase (or decrease) in leaf area at one age has the same effect at every point during ontogeny. A similar effect was found in the case of plants grown individually, although much smaller fraction of total variance in growth trajectories was concentrated in the first eigenvalue (i. e., 60% of variance, rather than over 90%, as in high-density plants). In the low-density plants, the second eigenfunctions changed signs (Fig. 6), indicating possible trade-offs in responses to selection for early versus late leaf area; e.g. selection for an increase in leaf area

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700 ppm CO2

350 ppm CO2

1st eigenfunction

High density

o.eoj

/

~

o.1o

0.05 ~

0.05

30

40

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60

70

80

30

40

50

60

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80

1st eigenfunction 0.15

0.15

0.10

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density

2nd eigenfunction 0.2

0.2

0.1

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0.0 ~ , J 3 0

-0.1[

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'

'

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-0.1 Time since germination (d)

Figure 6 Effectsof elevated CO2 and density on the covariance structure of leaf area during growth in Line thickness of the eigenfunction corresponds to the fraction of variance associated with its eigenvalue. In high-densityplants, second eigenvalues accounted for less than 5% of total variance and are not shown. From M. Jasiefiski, S. C. Thomas, and F. A. Bazzaz, manuscript in preparation. of young plants will lead to decreases in leaf area of older plants, and vice versa. Density of plants had a stronger direct effect than CO2 on the potential for evolutionary modifications in growth trajectories: selection on leaf area in plants grown without competition had m o r e possible outcomes than selection in high-density populations. This result points again to density as an i m p o r t a n t proxy for CO2 effects. A recent selection e x p e r i m e n t on (see Tousignant and Potvin, Chapter 3) provides virtually the only direct experimental evidence

regarding traits favored under rising C O 2. Following eight generations of truncation selection for reproductive output (under a regime of increasing CO2, temperature, and temperature variation), selected lines exhibited increased biomass, but reduced allocation (in both absolute and relative terms) to reproduction. One possible explanation for these results is that plants under elevated CO2 were effectively under a selective regime of increased aboveground competition. A variety of life history models predict increased size and decreased reproductive allocation under such conditions (e.g., Gadgil and Bossert, 1970). However, the inclusion of the temperature increases and heat shock episodes in the experimental design make these experimental results difficult to interpret unambiguously. Inbreeding effects could also have resulted in the observed reproductive declines. One earlier study attempted to select lettuce for high growth response to elevated CO2 (Maxon-Smith, 1977). No significant response was detected after eight generations of selection; however, the author suggests that the experiment may have been compromised by poor control of CO2 and temperature levels. Some intriguing physiological responses to selection under very low CO2 conditions have been documented in a series of experiments with doubled haploid lines of (Delgado and Medrano, 1991; Delgado, 1992a,b, 1993). Lines selected for survival at CO2 levels near the CO2 compensation point (60 ppm) were found to display increased vegetative growth under both field and laboratory conditions. However, this was not associated with either increased leaf-level photosynthesis or decreased photorespiration. Rather, selected lines showed increased rates of leaf production and lower respiration rates (Delgado 1992b, 1993). Additionally, leaves of selected lines possessed smaller mesophyll cells than did controls, which may have decreased mesophyll limitation of CO2 diffusion under low CO2 conditions. The implications of these findings to selection under high CO2 are not entirely clear. However, it is of some interest that screening of genotypes under low CO2 levels has previously been used as a strategy to select for high photosynthetic rates and growth potential in crop species (see also Cannell 1969; Menz 1969). One potentially important source of direct evidence regarding traits favored under rising CO2 is a comparison between populations of plants growing near naturally high CO2 environments with populations under ambient levels. Unfortunately, no systematic study of this nature has yet been attempted. However, one obscure and very early study addressing the ecology of crater plants on the island of Java contains some suggestive observations on possible effects (Von Faber, 1925, 1927). Von Faber's attention was initially drawn to CO2 vents by the presence of extremely green leaves of plants in the immediate vicinity of the vents. He later documented that these plants did in fact show exceptionally high chloro-

5.

phyll content. Von Faber also speculated that high C O 2 levels could compensate for very low light levels, facilitating the evolution of extreme shade plants in such environments (Schimper, 1935, p. 146). In summary, at present no strong a priori theory exists allowing for predictions of what traits will be favored under rising CO2. Two speculative hypotheses are advanced: first, selection may act largely through enhanced local competition, thus favoring suites of traits enhancing fitness under high density or high productivity environments; and second, in cases where CO2 has pronounced effects on plant developmental processes, selection may operate to ameliorate such effects. Definitive empirical studies aimed at identifying traits favored under rising CO2 are presently lacking. A variety of approaches, including selection experiments, quantitative genetic investigations, and comparative studies of populations exposed to naturally high CO2 levels are necessary to make progress in this area.

There are well-documented examples in which genetic change in populations can have profound impacts on ecosystem function. In the case of a heavily contaminated mine spoil, ecosystem properties such as carbon and nitrogen flux may be entirely contingent on patterns ofintraspecific genetic variability (Antonovics 1971; Shaw, 1991). If no tolerant genotypes were available to colonize heavily contaminated areas, then no carbon fixation by any autotrophic organism would exist. The evolutionary implications of a resource increase are, however, less clear at the ecosystem level. Some bounds on potential evolutionary effects on ecosystem function might be derived from selection experiments which monitor both ecosystem properties and genetic composition. The data from the experiment provides some preliminary data on this issue. Using quantitative genetic projections [Eq. (2)], we calculated a < 1% per generation increase in net primary productivity in either high or low density populations (Bazzaz 1995). This result was primarily due to a low correlation between reproductive and vegetative growth enhancement, in spite of relatively high values for the total response to selection. Since data regarding traits selectively favored under rising CO2 are very scant, predictions regarding consequences of evolutionary change to ecosystem processes are largely premature. However, such lack of information does not mean that evolutionary processes could not potentially play an important role in determining future trends in ecosystem function. For example, enhanced root turnover or root exudate production (for reviews see Stulen and den Hertog, 1993; Rogers 1994) may not result in

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enhanced plant performance. Physiological characteristics that provide the basis for these responses could thus be rapidly selected out of plant populations, depending on genetic variability and fitness consequences. If plants do indeed generally exhibit greatly enhanced levels of belowground carbon release under elevated COs, the evolutionary implications for soil microbes may be very large. In this case, short generation times could facilitate very rapid evolutionary responses, perhaps favoring the ability to rapidly utilize newly available fluxes of belowground carbon. It would be remarkable indeed if a doubling of the primary substrate for the world's most abundant enzyme did not have profound evolutionary implications for the world's autotrophic organisms. The few existing studies documenting genetic variation in plant responses to elevated COs have consistently found that not all genotypes respond positively (cf. Wulff and Alexander, 1985; Curtis 1994; Bazzaz 1995; Wayne and Bazzaz, 1995). In this regard, we may confidently predict, both on the basis of general theory and existing data, that selection under elevated COs will involve some loss of genetic variability in plant populations. This may or may not have long-term repercussions to community composition or ecosystem function. However, because COs-related selection affects all plant populations throughout the globe, such a threat to global genetic resources should be examined in earnest. Even considering massive anthropogenic changes in land use patterns and atmospheric pollutants, globally rising COs could well be the single most profound selective agent affecting our planet's autotrophic organisms.

Recent empirical work has documented substantial intraspecific genetic variation in plant growth responses to elevated CO2. thus raising the issue of selective responses to elevated CO2 in plant populations. In contrast to the well-studied case of selection for heavy-metal tolerance, selection under rising CO2 is likely to be density dependent and contingent on local availability of other plant resources. The component processes of natural selection, namely, the expression of phenotypic variation in fitness, the degree to which this variation is heritable, and genetic covariance of other traits with fitness, may each respond in predictable ways to rising COs conditions. Each of these parameters is examined, with specific reference to reaction norm experiment investigating the responses of genotypes of to population density and COs. Phenotypic variation within plant populations may be enhanced by elevated COs: for example, variation in size-related traits may increase due to accelerated divergence in growth a n d / o r accelerated competitive interactions. Heritabilities of fitness-related

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traits m a y o f t e n b e e x p e c t e d to b e h i g h e r , b e c a u s e e l e v a t e d C O 2 c o n s t i t u t e s a n o v e l e n v i r o n m e n t a l state n o t p r e s e n t in t h e r e c e n t selective h i s t o r i e s o f m o s t p l a n t species. G e n e t i c c o r r e l a t i o n s t r u c t u r e m a y also b e a l t e r e d , p e r h a p s d u e to a d i s r u p t i o n o f f u n c t i o n a l i n t e g r a t i o n o f p l a n t d e v e l o p m e n t . E x i s t i n g d a t a s u g g e s t t h a t r i s i n g CO2 levels will h a v e p r o f o u n d selective c o n s e q u e n c e s o n p l a n t p o p u l a t i o n s . H o w e v e r , t h e r e is very little d a t a availa b l e to s u g g e s t w h a t p h e n o t y p i c c h a r a c t e r i s t i c s will u l t i m a t e l y b e s e l e c t e d . T h e c o n s e q u e n c e s o f s u c h s e l e c t i o n o n c o m m u n i t y a n d e c o s y s t e m level p r o c e s s e s a r e also p r e s e n t l y u n c l e a r , a l t h o u g h s e l e c t i o n u n d e r r i s i n g CO2 will n e c e s s a r i l y r e s u l t in s o m e loss o f g e n e t i c v a r i a t i o n a m o n g p l a n t p o p u l a tions.

We thank F. A. Bazzaz for collaboration on the experiment reported here, and for inspiration and discussions of the ideas presented. This work was supported by a grant from the U.S. Department of Energy (DEFGO2 ER 60257).

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Mitchell-Olds, T., and Rutledge,J.J. (1986). Quantitative genetics in natural plant populations: A review of the theory. 127, 379-402. Morse, S. R., and Bazzaz, F. A. (1994). Elevated COz and temperature alter recruitment and size hierarchies in C3 and C4 annuals. 75, 966-975. Musgrave, M. E., Strain, B. R., and Siedow, J. N. (1986). Response of two pea hybrids to CO2 enrichment: A test of the energy overflow hypothesis for alternative respiration. 83, 8157-8161. Namkoong, G., Bishir, J., and Roberds, J. H. (1993). Evolutionary effects of density-dependent selection in plants. 62, 57-62. Noordwijk van, A.J., and de Jong, G. (1986). Acquisition and allocation of resources: Their influence on variation in life history tactics. 128, 137-142. Pefiuelas, J., and Matamala, R. (1990). Changes in N and S leaf content, stomatal density and specific leaf area of 14 plant species during the last three centuries of CO2 increase. 41, 1119-1124. Poorter, H. (1993). Interspecific variation in the growth response of plants to an elevated ambient CO2 concentration. 104/105, 77-97. Reekie, J. Y. C., Hicklenton, P. R., and Reekie, E. G. (1994). Effects of elevated CO2 on time 72, 533-538. of flowering in four short-day and four long-day species. Rice, K.J. (1990). Reproductive hierarchies in Effects of variation in plant density and rainfall distribution. 71, 1316-1323. Riska, B. (1989). Composite traits, selection response, and evolution. 43, 1172-1191. Roff, D. A. (1995). The estimation of genetic correlations from phenotypic correlations: A test of Cheverud's conjecture. 74, 481-490. Rogers, H. H., Cure, J. D., Thomas, J. F., and Smith, J. M. (1984). Influence of elevated CO2 24, 361-366. on growth of soybean plants. Rogers, H. H., Runion, G. B., and Krupa, S. V. (1994). Plant responses to atmospheric CO2 enrichment with emphasis on roots and the rhizosphere. 83, 155-189. Roose, M. L. (1991). Genetics of response to atmospheric pollutants. "Ecological Genetics and Air Pollution" (G. E. Taylor, L. F. Pitelka, and M. T. Clegg, eds.), pp. 111-126. Springer-Verlag, Berlin. Samson, D. A., and Werk, K. S. (1986). Size-dependent effects in the analysis of reproductive effort in plants. 127, 667-680. Schimper, A. F. W. (1935). "Pflanzengeographie auf physiologischer Grundlage," 3rd ed. Fischer, Jena. Schmalhausen, I. I. (1949). "Factors of Evolution: The Theory of Stabilizing Selection." Univ. Chicago Press, Chicago. Service, P. M., and Rose, M. R. (1985). Genetic covariation among life-history components: The effect of novel environments. 39, 943-945. Shaw, A.J., ed. (1991a). "Heavy Metal Tolerance in Plants: Evolutionary Aspects." CRC Press, Boca Raton, FL. Shaw, R. G. (1991b). The comparison of quantitative genetic parameters between populations. 45, 143-151. Shaw, R. G., and Platenkamp, G. A.J. (1993). Quantitative genetics of response to competitors in 47, 801-812. Smart, D. R., Chatterton, N. J., and Bugbee, B. (1994). The influence of elevated CO2 on nonstructural carbohydrate distribution and fructan accumulation in wheat canopies. 17, 435-442. Spicer, R. A., and Corfield, R. M. (1992). A review of terrestrial and marine climates in the Cretaceous with implications for modelling the 'Greenhouse Earth.' 129, 169-180.

Stitt, M. (1991). Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells. 14, 741-762.

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Strain, B. R. (1991). Possible genetic effects of continually increasing atmospheric CO2. "Ecological Genetics and Air Pollution" (G. E. Taylor, L. F. Pitelka, and M. T. Clegg, eds.), pp. 177-202. Springer-Verlag, Berlin. Strain, B. R., and Cure, J. D. (1985). "Direct Effects of Increasing Carbon Dioxide on Vegetation." United States Dept. of Energy, Carbon Dioxide Research Division, DOE/ER 0238, Office of Energy Research, Washington, DC. Stulen, I., and den Hertog, J. (1993). Root growth and functioning under atmospheric CO2 enrichment. 104/105, 99-115. Tans, P. P., Fung, I. Y., and Takahashi, T. (1990). Observational constraints on the global atmospheric CO2 budget. 247, 1431-1438. Thomas, S. C., and Bazzaz, F. A. (1993). The genetic component in plant size hierarchies: Norms of reaction to density in a species. 63, 231-249. Thomas, S. C., and Bazzaz, F. A. (1996). Elevated CO~ and leaf shape: Are dandelions getting toothier? 83, 106-111. Thomas, S. C., and Weiner, J. (1989). Growth, death and size distribution change in an population. 77, 524-536. Tolley, L. C., and Strain, B. R. (1984). Effects of CO2enrichment on growth of and seedlings under different irradiance levels. 14, 343-350. Tremmel, D. C., and Patterson, D. T. (1994). Effects of elevated CO~ and temperature on development in soybean and five weed. 74, 43-50. Turelli, M. (1988). Phenotypic evolution, constant covariances, and the maintenance of additive variance. 42, 1342-1347. Uchmafiski, J. (1985). Differentiation and frequency distributions of body weights in plants and animals. 310, 1-75. Via, S. (1987). Genetic constraints on the evolution of phenotypic plasticity. "Genetic Constraints on Adaptive Evolution" (V. Loeschcke, ed.), pp. 47-71. Springer-Verlag, Berlin. Via, S., and Lande, R. (1985). Genotype-environment interaction and the evolution of phenotypic plasticity. 39, 505-522. Von Faber, F. C. (1925). Untersuchungen fiber die Physiologie der javanischen SolfatarenPhflanzen. 18/19, 89. Von Faber, F. C. (1927). Die Kraterpflanzen Javas in physiologisch-tkologischer Beziehung. no. 1. Wade, M.J. (1985). Soft selection, hard selection, kin selection, and group selection. 125, 61-73. Wallace, B. (1968). Polymorphism, population size, and genetic load. "Population Biology and Evolution" (R. C. Lewontin, ed.), pp. 87-108. Columbia Univ. Press, New York. Walters, M. B., Kruger, E. L., and Reich, P. B. (1993). Growth, biomass distribution and CO2 exchange of northern hardwood seedlings in high and low light: Relationships with successional status and shade tolerance. 94, 7-16. Wayne, P. M., and Bazzaz, F. A. (1995). Seedling density modifies the growth response of yellow birch maternal families to elevated carbon dioxide. 1,315-324. Weiner, J. (1985). Size hierarchies in experimental populations of annual plants. 66, 743-752. Weiner, J. (1988). The influence of competition on plant reproduction. "Reproductive Ecology of Plants: Patterns and Strategies" (J. Lovett-Doust and L. Lovett-Doust, eds.), pp. 228-245. Oxford Univ. Press, New York. Weiner, J. (1990). Asymmetric competition in plant populations. 5, 360-364. Weiner, J., and Thomas, S. C. (1986). Size variability and competition in plant monocultures. 47, 211-222. Wilkinson, G. S., Fowler, K., and Partridge, L. (1990). Resistance of genetic correlation structure to directional selection in 44, 1990-2003.

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Willis, J. H., Coyne, J. A., and Kirkpatrick, M. (1991). Can one predict the evolution of quantitative characters without genetics? 45, 441-444. Wilson, J. B., and Levin, D. A. (1986). Some genetic consequences of skewed fecundity distributions in plants. 73, 113-121. Woodward, F. I. (1987). Stomatal numbers are sensitive to increases in COzfrom pre-industrial levels. 327, 617-618. Wulff, R. D., and Alexander, H. M. (1985). Intraspecific variation in the response to COz enrichment in seeds and seedlings of 66, 458-460. Young, H.J., Stanton, M. L., Ellstrand, N. C., and Clegg, J. M. (1994). Temporal and spatial variation in heritability and genetic correlations among floral traits in wild radish. 73, 298-308. Zeng, Z.-B. (1988). Long-term correlated response, interpopulation covariation, and interspecific allometry. 42, 363-374. Ziska, L. H., and Teramura, A. H. (1992). Intraspecific variation in the response of rice (Oryza to increased COzmPhotosynthetic, biomass and reproductive characteristics. 84, 269-276.

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II Community-Level Responses

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The Changing Vegetation of Europe: What Is tile Role of Elevated Carbon Dioxide?

Although there is no doubt that atmospheric carbon dioxide concentrations are rising rapidly (Keeling 1982) and will continue to do so (IPCC, 1992), there is considerable uncertainty with regard to the consequences for plant communities and ecosystems (Korner, 1993). The difficulties in predicting the impact of elevated CO2 first become evident in the laboratory or growth chamber and multiply as we move outdoors and begin to consider large-scale processes operating over extended periods of time. From laboratory studies we know that plant species differ in responsiveness to elevated CO2 (Hunt 1991; Poorter, 1993) and we may be certain that patterns of response detected under controlled conditions will be subject, in more natural habitats, to the modifying effects of other environmental factors, some of which (temperature, rainfall, UV-B) are themselves implicated in global environmental change. At this point in the analysis it is tempting to conclude that the task of predicting the ecological impacts of rising CO2 falls almost exclusively in the domain of plant physiology (e.g., Schulze and Mooney, 1993). Little doubt remains that physiological insights are needed for a mechanistic and predictive understanding of vegetation responses to elevated CO2. However, in this chapter I shall argue that the most urgent requirement is to place CO2 research in the context of other global and regional changes in vegetation driven by more powerful forces. and

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Copyright 9 1996 by Academic Press, Inc. All rights of reproduction in any form reserved.

At the present time, the most potent forces for change acting on vegetation are the effects of land use. These arise from the direct effects of human activity (habitat modification by agriculture, forestry, industry, human settlements, overgrazing) and indirect effects (eutrophication through groundwater and atmospheric pollutants, and phytotoxicity resulting from aerial and soil contamination). Reviewed on a world scale, the most consistent effect of these phenomena is the inexorable replacement of mature, often species-rich ecosystems by early successional states in which the vegetation is composed of recently established, fast-growing clonal herbs and ephemeral species. This process has two important implications for studies which seek to predict the impacts of rising CO2. The first is the notion that vegetation is already experiencing such radical processes of change that impacts of CO2 are perhaps most appropriately analyzed as a fine-tuning of the rates and trajectories of changes which are already well advanced and are driven by land use. The second implication arises from the faster growth rates and reduction in the average life span in the constituent species of vegetation arising from modern forms of intensive or disruptive land use (Grime 1988). Later in this chapter we will examine evidence that these expanding species are more responsive to elevated CO2. Moreover, the higher rates of population turnover characteristic of the vegetation of disturbed and intensively exploited landscapes create conditions in which the plant cover is likely to respond more quickly to selection driven by elevated CO2 either by permitting more invasions and extinctions or by allowing rapid genetic changes within component populations. Hence land use is likely to be an essential factor in any calculations of the direction and rate of vegetation responses to elevated CO2. In order to explore further the interaction between changing land use and CO2 responses, let us now look at recent evidence of floristic change in Western Europe.

In a comparative discriminant analysis of the functional traits of increasing and decreasing species in the vascular plant floras of the British Isles, The Netherlands, and West Germany (Thompson, 1994), three main conclusions have been drawn: 1. A key measure discriminating between increasing and decreasing species is S radius. S radius is a measure of proximity to the stress-tolerant corner of a CSR strategic triangle of plant functional types (Grime, 1974; Grime 1988); a large S radius is correlated with low growth rate, low rates of tissue turnover, and low mineral nutrient requirements. In densely

6.

populated England, the Netherlands, and to a lesser extent, West Germany, decreasing species are stress-tolerators (large S radius), whereas increasing species are fast-growing and typical of eutrophic, disturbed habitats. 2. In the sparsely populated northern and western regions of the British Isles differences between "winners" and "losers" are very slight. 3. Surprisingly, regenerative attributes (seed weight, seed persistence in soil, wind dispersal) are very poor predictors of success and failure in the modern northwest European landscape. The same sources are used in Fig. I to plot the mean Sradius of increasing and decreasing species against human population density in seven European countries. Thompson's (1994) interpretation of these results accords with an earlier hypothesis of Hodgson (1986a,b) in suggesting that in the densely populated countries of Western Europe, land use is increasingly polarizing the flora into two parts. The successful, fast-growing part is tolerant of human activities and is ecologically attuned to intensively managed grassland, arable fields, road verges, gardens, spoil, and urban waste-

Figure 1 Relationship between mean S radius of increasing and decreasing species and h u m a n population density in seven European countries. S radius of the two groups is not significantly different in Scotland, N. Ireland, or Wales. The two groups are significantly different in Republic of Ireland (P = 0.049), England, western Germany, and The Netherlands (all P < 0.001).

88

j. t'. ~ m e

land. Because these habitats are common, and because soils, seeds, and plant fragments are moved freely between them by human agencies, these plants are highly mobile, rapidly colonizing new sites as they become available. Species of this type will have little difficulty in migrating in response to land use change. In contrast, the slow-growing, stress-tolerant part of the flora, typical of unimproved grassland, lowland heath and old woodland, is increasingly excluded from the wider landscape. How will rising COs influence these vegetation changes resulting from land use? Has responsiveness to COs concentration already played a significant role in the promotion of fast-growing, resource-demanding species in intensively developed landscapes? To address these questions it is necessary to consider our present understanding of how different types of plants respond to elevated COs.

Over the period from 1987 to 1994 a comprehensive screening program (Integrated Screening Programme, ISP) was conducted at Sheffield (with links to other centers) to compile standardized information on the laboratory characteristics of a large number of common herbaceous vascular plants of the British Isles. As part of the ISP a series of CO2 screening experiments were carried out at Horticulture Research International's site at Littlehampton (Hunt 1991, 1993, and 1995). These experiments covered 36 different species; many of them were later restudied to provide confirmation. Strong responses to elevated CO2 were recorded when plants were held at 18~ In some species there was a 27% increase in biomass after only 8 weeks' growth. However, such levels of response mainly occurred in robust, fast-growing perennials (e.g., of the kind which often dominate vegetation in productive and undisturbed habitats, such as river banks and recently abandoned farmland and gardens. These plants exhibit sustained vegetative growth and develop large roots, shoots, and storage organs prompting the hypothesis that responsiveness to elevated COs may be related to possession of rapidly expanding carbon sinks. This interpretation is supported by the observation (Hunt 1995) that the benefit of elevated COs to the fast-growing ephemeral, is not sustained beyond the early vegetative phase of development. A consistent feature of the ISP results has been the low level of response by slowgrowing evergreen species of unproductive habitats (i.e., high S radius plants). These results suggest that the capacity to respond strongly to elevated COs is prominent among the species that are currently expanding in abundance in the more intensively developed landscapes of heavily populated countries of Western Europe.

89

6.

The need for caution in extrapolating from the responses of individual potted plants in growth chambers to the dynamics of communities of plants in the field is self-evident. The majority of laboratory studies (including the ISP) are designed to standardize conditions and facilitate comparison and interpretation. Realism is sacrificed to the extent that the complexities of season, weather, soil microbiology, decomposition, nutrient dynamics, interspecific competition, and plant-animal interactions are excluded. Some insights into the complications that can arise when attention is turned to "real" systems are evident in Fig. 2 (A,B), which presents results from an experiment (Diaz 1993) in which early-successional plant communities were allowed to reassemble from natural seed banks and soils removed to

Shoot biomass n

s

Cover

~

~ n s

Dominance Carbohydrates Nitrogen SOIL 9

Microbial N ..

-40

-30

-20

-10

0

10

20

30

MicrobialC 40

% change under doubling CO2 Figure 2 (A) Responses of and soil microflora grown in microcosms to a doubling of atmospheric CO2 (700 ppm) as compared to controls at 350 ppm. Vegetation was allowed to develop for 84 days by natural recruitment from seed banks in soils removed from a tall herb community in Derbyshire and placed in microcosms (6 replicates per treatment) in cabinets without nutrient addition. Shoot biomass was measured as milligram dry weight, cover as n u m b e r of touches in a point-quadrat analysis, dominance as biomass of R. total community biomass, carbohydrates (starch + glucose + sucrose) as milligram/gram fresh weight and nitrogen as milligram/gram dry weight of fully expanded young leaves, microbial C and N as milligram/gram dry soil; ns, nonsignificant; *, P < 0.05; **, P < 0.01 (ANOVA). (B) Effects of atmospheric doubling of CO2 concentration (ppm) and fertilizer addition on foliar N content of grown in microcosm for 60 days. Deionized water (control) and full-strength Rorison solution (fertilized) were added throughout the experiment as 100 ml per microcosms every 4 days. Bars designated by the same letter are not different at P < 0.05 (ANOVA).

90

j.P. Gr/me 25 o l

2 0 ow

15 o l

Q ~

10~

z

5 --

0

~ 350 ppm

700 ppm

Continued

laboratory microcosms providing ambient and elevated

CO

2 concentra-

tions.

In the example shown in Fig. 2A the potentially responsive showed leaf stunting when exposed to elevated CO2. These symptoms coincided with carbohydrate accumulation and reduced levels of foliar nitrogen. From soil analyses, circumstantial evidence showed that deficiency had been induced by export of carbohydrate from roots to soil and subsequent sequestration of nitrogen in a massively expanded soil microflora. This hypothesis was supported by the results of a second experiment (Fig. 2B) in which the leaf nitrogen content of plants grown at elevated CO2 did not increase when additional mineral nutrients were added to the soil. These results are a useful reminder of the feedbacks that can occur in response to elevated CO2. Species responses within ecosystems are likely to be determined by factors such as soil microbiology, which are additional to those (e.g., sink strength) that emerge as key factors in simple laboratory assays.

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91

This chapter assembles circumstantial evidence that the types of herbaceous plants which are currently expanding in a b u n d a n c e in heavily populated countries of Western Europe are also strongly responsive to elevated concentrations of carbon dioxide. This evidence suggests that responses to carbon dioxide may be contributing to the recent success of these species. An attractive feature of this hypothesis is the observation that the responsive species occupy habitats in which other essential resources are relatively a b u n d a n t and are unlikely, therefore, to limit the stimulatory effect of carbon dioxide enrichment. There are several reasons why we should treat this interpretation with caution. The data comparing responses to elevated CO2 are based on simplified laboratory conditions and refer mainly to herbaceous plants grown for short periods of time with nonlimiting supplies of moisture and mineral nutrients. It may be especially i m p o r t a n t to recognize that on natural soils responses to CO2 may be limited by n u t r i e n t stress arising from microbial sequestration of mineral nutrients. In attempts to u n d e r s t a n d the interactions between land use and elevated CO2 it may be essential to differentiate between short and long cycles of secondary succession. Where vegetation destruction and mineral n u t r i e n t release occurs frequently, it seems likely that selection associated with elevated CO2 may act in parallel with eutrophication in p r o m o t i n g fast-growing clonal herbs. However, it can be argued that where the intervals between major disturbance events are longer (coppiced woodlands, plantations, long-rotation grasslands, b u r n e d heathlands), elevated CO2 could accelerate succession by favoring plants that develop m o r e slowly but provide m o r e substantial sinks for carbon and mineral nutrients. These hypotheses require experiments of sufficient scale and duration to allow rigorous tests of the effects of CO2 e n r i c h m e n t on successional processes.

This chapter draws on information collected with colleagues at UCPE as part of the Integrated Screening Programme and the Terrestrial Initiative in Global Environmental Research, both of which are supported by the Natural Environment Research Council.

Diaz, S., Grime,J. P., Harris,J., and McPherson, E. (1993). Evidence of a feedback mechanism limiting plant response to elevated carbon dioxide. 364, 616-617.

Grime, J. P. (1974). Vegetation classification by reference to strategies. 250, 26-31. Grime, J. P., Hodgson, J. G., and Hunt, R. (1988). "Comparative Plant Ecology: A Functional Approach to Common British Plants." Unwin Hyman, London. Hodgson, J. G. (1986a). Commonness and rarity in plants with special reference to the Sheffield flora. I. The identity, distribution, and habitat characteristics of the common and rare species. 36, 199-252. Hodgson, J. G. (1986b). Commonness and rarity in plants with special reference to the Sheffield flora. II. The relative importance of climate, soils, and land use. 36, 254-274. Hunt, R., Hand, D. W., Hannah, M. A., and Neal, A, M. (1991). Response to COz enrichment in 27 herbaceous species. 5, 410-421. Hunt, R., Hand, D. W., Hannah, M. A., and Neal, A. M. (1993). Further responses to CO2 enrichment in British herbaceous species. 7, 661-668. Hunt, R., Hand, D. W., Hannah, M. A., and Neal, A. M. (1995). Temporal and nutritional influences on the CO2 response in selected British grasses. 76, 207-216. International Panel on Climate Change Report (1992). "Climate Change 1992: The Supplementary Report to the IPCC Scientific Assessment." Cambridge Univ. Press, Cambridge, UK. Keeling, C. D., Bacastow, R. B., and Whorf, T. P. (1982). Measurements of the concentration of carbon dioxide at Mauna Loa Observatory, Hawaii. "Carbon Dioxide Review" (W. C. Clark, ed.). Korner, C. H. (1993). CO2 fertilization: The great uncertainty in future vegetation development. "Vegetation Dynamics and Global Change" (A. M. Solomon and H. H. Shugart, eds.), pp 53-70. Chapman and Hall, London. Poorter, H. (1993). Interspecific variation in the growth response of plants to an elevated ambient CO2 concentration. 104/105, 77-97. Schulze, E. D., and Mooney, H. A., eds. (1993). "Design and Execution of Experiments on CO2 Enrichment." Commission of the European Communities, Brussels. Thompson, K. (1994). Predicting the fate of temperate species in response to human disturbance and global change. "NATO Advanced Research Workshop on Biodiversity, Temperate Ecosystems, and Global Change" (T. J. B. Boyle and C. E. B. Boyle, eds.), pp. 6176. Springer Verlag, Berlin.

7 Changing Community Composition and Elevated CO2

Anthropogenic forcing of biogeochemical cycles, such as the global carbon cycle, can potentially alter community composition (e.g., Bazzaz and Carlson, 1984; Bazzaz and Fajer, 1992; Melillo 1990; Gates, 1994). Likewise, alterations in the species composition of communities can alter ecosystem processes (Tilman and Downing, 1994; Naeem 1994a, 1995; Schulze and Mooney, 1993). Together these interactions describe a potential feedback between changing levels of biotic diversity and changing levels of CO2. This potential feedback between biotic diversity and the carbon biogeochemical cycle may be significant on a global scale. Ecosystems worldwide are simultaneously experiencing both anthropogenic alterations in diversity (e.g., Wilson and Peter, 1988; Soul~, 1991; Ehrlich and Wilson, 1991; Groombridge, 1992; Sisk 1994) and anthropogenic increases in atmospheric CO2. Such feedbacks between biotic factors and biogeochemical cycles are important for modeling global change (Lashof, 1989; Schneider, 1992). Empirical evidence for the feedback between diversity and carbon cycling is limited. We present, however, evidence from two mesocosm experiments using a controlled environmental facility referred to as the "Ecotron" 93

Copyright 9 1996 by Academic Press, Inc. All rights of reproduction in any form reserved.

94 (Lawton 1993) which support the possibility of interactions between community composition and C02 flux through an ecosystem (biomass accumulation) and the possible feedback between them. In the first experiment, henceforth the "biodiversity experiment," community composition was manipulated and ecosystem biomass accumulation was measured as a response variable. In the second, henceforth the "elevated C02 experiment," C02 levels were manipulated and community composition and biomass accumulation were measured as response variables. We discuss the implications of these results for global-change research on elevated C02.

A. The Biodiversity Experiment The Ecotron is described in both Lawton (1993) and Thompson (1993). The materials, methods, and results concerning the association between biodiversity and ecosystem functioning (the biodiversity experiment) can be found in Naeem (1994a,b, 1995). Briefly, in this experiment plant and animal species composition within model terrestrial communities were experimentally manipulated to produce 3 levels of diversity: low (4 replicates), intermediate (4 replicates), and high diversity (6 replicates) mesocosms (see Table I for a list of species). The Ecotron consists of 16 chambers which are divided into 2 banks of 8 chambers each. Because each bank is serviced by separate environmental regulating machinery, random assignment of treatments to chambers was statistically blocked by bank to test for block effects. Diversity was manipulated in all trophic levels (Table I). CO2 flux was measured continuously throughout the experiment after Day 120 (total experiment duration was 210 days), but only data collected over 48-hour periods, on a biweekly basis, when chambers were closed and undisturbed by the activities of researchers, were used for statistical analyses. B. The Elevated CO2 Experiment This experiment conducted in the Ecotron consisted of one bank of chambers with eight replicate mesocosms exposed to ambient levels of CO2 and eight replicates of the second bank exposed to ambient +200 ppm CO2. CO2 flux was measured as above, but data used for statistical analyses were collected weekly. C. Differences between the Two Experiments Although the edaphic, daily temperature and humidity conditions were the same for both experiments, the elevated CO2 experiment differed from the biodiversity experiment in several significant ways. First, more light

Biodiversity Species

Low

Int.

High

C02

Plants

u

Animals Mollusk

Earthworm W o o d louse Collembola

cf. cf. Insect herbivores

Parasitoids

a Note similarities in community composition between intermediate (Int.) diversity treatment and the current COs experiment.

96 (18% full sunlight) was provided in the elevated C O 2 experiment (10% full sunlight was provided for the biodiversity experiment). Second, though trophic complexity and number of species were similar between the elevated CO2 experiment and the intermediate-diversity treatment of the biodiversity experiment, some species substitutions were made (Table I). Third, unlike the biodiversity experiment, the Ecotron does not permit random assignment of atmospheric treatments, such as ambient versus elevated CO2, to replicate mesocosms. This results in a pseudoreplicated design which necessitates a follow-up experiment in which treatments to banks (enhanced and ambient CO2) are reversed (currently running, but not reported here). Fourth, injection of augmented CO2 into the atmospheric stream servicing the elevated CO2 communities occasionally resulted in spurious levels of recorded CO2 exhausts in five of the eight chambers during the period of measurement reported here (the problem has since been rectified). We therefore estimated COz flux using only the chambers (chambers 3, 5, and 6) whose CO2 flux readings were not suspect. Finally, periodic harvests were conducted for standing biomass estimation. This practice periodically reduced net CO2 flux.

The biodiversity experiment showed that manipulating community composition alters biomass accumulation, as measured by CO2 flux (Fig. 1). In our model system, higher diversity assemblages sequestered more carbon, a result that is robust for other combinations of plant species (Naeem 1994a, 1995). Although communities rarely differed within intervals, over the duration of the experiment a repeated measures analysis of variance (RMANOVA) showed that higher diversity communities sequestered more carbon than lower diversity communities (RMANOVA; among group = 2, 8; F = 4.5; P < 0.05; interaction = 22, 88; F = 2.7; P < 0.001). Results from the CO2 experiment show that overall levels of biomass accumulation (as measured by COz flux) are statistically different between ambient and elevated CO2 communities of intermediate diversity (RMANOVA; = 26, 1; F = 5.6; P < 0.001, Fig. 1). Note that this statistic was obtained by the conservative method of comparing weekly mean CO2 fluxes of elevated CO2 communities with the weekly mean COz fluxes of ambient CO2 communities. Periodic harvests, estimates of community composition, and additional analyses reveal that a complex number of ecological changes over the course of the experiment are associated with these results. These results are still in a preliminary form and will be reported in detail elsewhere.

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Figure 1 CO~ flux (mol m -2 d -x) in the biodiversity and elevated experiments. Time is measured in weeks from start of experiment. For the purposes of comparison, this figure shows only a partial set (that which corresponds temporally to the shorter sequence in the biodiversity experiment) of the data from the elevated CO2 experiment. Arrows indicate harvest dates ("winters") in which most of the vegetation is removed and the system is allowed to recover. The top graph (a) plots results from the elevated COs experiment. The lower graph (b) plots results from the biodiversity experiment. Note that negative values indicate sequestered carbon whereas positive values indicate greater microbial, invertebrate, and plant respiration than photosynthetic activity. Note also the different scales and note the greater negative values for the elevated CO2 experiment are partly the result of additional light provided in this experiment. Error bars represent one SE. AMB, ambient CO2; ELEV, elevated CO2; HI, high diversity; INT, intermediate diversity; LOW, low diversity.

Results from these experiments suggest that declining diversity within an ecosystem can decrease biomass accumulation and, conversely, that elevated CO2 can change the biomass accumulation of an ecosystem. Interpreted more broadly, our results suggest that ecosystem response to elevated CO2 is a function of both diversity and CO2 levels.

Though biomass accumulation may be trivially a function of the species found within an ecosystem, the response of biomass accumulation to random declines in diversity is not a trivial problem. For example, neither theory nor experiments in intercropping provide steadfast rules for how diversity and yield (biomass accumulation) might be associated in even simple agroecosystems (Vandermeer, 1989; Swift and Anderson, 1993). Our biodiversity experiment suggested that if a decline in plant diversity is associated with decreasing interception of light by the canopy, then CO2 sequestration by an ecosystem may decline. Our elevated CO2 experiment, however, suggests that changes in ecosystem biomass accumulation generated by elevated COz could compensate for such a loss of carbon sequestration. Although we cannot readily extrapolate from these simple experimental systems to larger more complex naturally occurring systems, these experiments point to an often neglected possibility that understanding how ecosystems will respond to elevated COz will be a function of how diversity changes over the next few decades. Our results suggest that manipulating both CO2 and community composition may improve our understanding of global change. Most research on the ecological consequences of elevated CO2 has been conducted using, on average, 550-700 ppm CO2, or levels likely to occur 50-60 years from now (Houghton 1990) and this research has rarely manipulated community composition. By the time these 50-60 years pass, changing COz, in addition to many other globally changing factors (e.g., N fertilization and habitat fragmentation) (Vitousek, 1994), may have already changed community composition. Indeed, some authors (e.g., K6rner, Chapters 11 and 28; Polley 1994, and Chapter 12) have argued that some of these effects have already occurred. Even without the effects of elevated CO2, the community composition of most ecosystems is likely to be substantially altered in the near future (e.g., Wilson and Peter, 1988; Soul6, 1991; Ehrlich and Wilson, 1991; Groombridge, 1992; Sisk 1994; Lawton and May, 1995). Understanding the interactions and feedbacks between ecosystem processes and community composition and how human impacts contribute to these processes will prove useful for predicting and understanding the effects of elevated CO2 on global change.

Current research on the ecological consequences of elevated C O 2 supports two direct interactions between communities and atmospheric CO2. First, altering levels of CO2 can change the relative abundance of species in communities. Second, altering the species composition of communities can change the ecosystem's ability to absorb CO2 (accumulate biomass).

7.

99

T h e s e two d i r e c t i n t e r a c t i o n s c o n s t i t u t e a f e e d b a c k b e t w e e n c h a n g i n g diversity a n d c h a n g i n g CO2 levels. Results f r o m two e x p e r i m e n t s c o n d u c t e d in a c o n t r o l l e d e n v i r o n m e n t a l facility ( t h e E c o t r o n ) s u p p o r t t h e e c o l o g i c a l bases f o r t h e s e i n t e r a c t i o n s . S i n c e virtually all e c o s y s t e m s a r e c u r r e n t l y b e i n g s i m u l t a n e o u s l y e x p o s e d to b o t h a n t h r o p o g e n i c a l l y i n d u c e d d e c l i n e s in diversity a n d i n c r e a s e d CO2, s t u d i e s t h a t m a n i p u l a t e b o t h CO2 a n d diversity as e x p e r i m e n t a l f a c t o r s will p r o v i d e m o r e p o w e r f u l i n s i g h t s i n t o g l o b a l c h a n g e t h a n single f a c t o r s t u d i e s c a n p r o v i d e a l o n e .

Bazzaz, F. A., and Carlson, R. W. (1984). The response of plants to elevated C O 2 . I. Competition among an assemblage of annuals at different levels of soil moisture. 62, 196-198. Bazzaz, F. A., and Fajer, E. D. (1992). Plant life in a CO2-rich world. 266, 68-74. Ehrlich, P. R., and Wilson, E. O. (1991). Biodiversity studies: Science and policy. 253, 758-762. Gates, D. M. (1994). "Climate Change and Its Biological Consequences." Sinauer, Sunderland, MA. Groombridge, B. (1992). "Global Biodiversity: Status of the Earth's Living Resources." A report compiled by the World Conservation Monitoring Centre. Chapman & Hall, London. Houghton, J. T., Jenkins, G. J., and Ephraums, J. J. (1990). "Climate Change: The IPPC Scientific Assessment." Cambridge Univ. Press, Cambridge, UK. Lashof, D. A. (1989). The dynamic greenhouse: Feedback processes that may influence future concentrations of atmospheric trace gases and climatic change. 11, 7-31. Lawton, J. H., and May, R. M. (1995). "Extinction Rates." Oxford Univ. Press, Oxford, UK. Lawton, J. H., Naeem, S., Woodfin, R. M., Brown, V. K., Gange, A., Godfray, H. C.J., Heads, P. A., Lawler, S., Magda, D., Thomas, C. D., Thompson, L. J., and Young, S. (1993). The Ecotron: A controlled environmental facility for the investigation of population and ecosystem processes. 341, 181-194. Melillo, J. M., Callaghan, T. V., Woodward, F. I., Salati, E., and Sinha, S. K. (1990). Effects on ecosystems. "IPCC, Climate Change, The IPCC Scientific Assessment" pp. 282-310. Cambridge Univ. Press, Cambridge, UK. Naeem, S., Thompson, L.J., Lawler, S. P., Lawton,J. H., and Woodfin, R. M. (1994a). Declining biodiversity can alter the performance of ecosystems. 368, 734-737. Naeem, S., Thompson, L. J., Lawler, S. P., Lawton, J. H., and Woodfin, R. M. (1994b). Biodiversity loss in model ecosystems: A reply to Andr6 371, 565. Naeem, S., Thompson, L.J., Lawler, S. P., Lawton, J. H., and Woodfin, R. M. (1995). Empirical evidence that declining species diversity may alter the performance of terrestrial ecosystems. 347, 249-262. Polley, H. W., Johnson, H. B., and Mayeux, H. S. (1994). Increasing CO2: Comparative responses of the C4 grass and grassland invader 75, 976-988. Schneider, S. H. (1992). The climate response to greenhouse gases. 22, 1-32. Schulze, E. D., and Mooney, H. A. (1993). "Biodiversity and Ecosystem Function." SpringerVerlag, New York. Sisk, T. D., Lauder, A. E., Switky. K. B., and Ehrlich, P. R. (1994). Identifying extinction 44, 592-604. threats. Soul6, M. E. (1991). Conservation: Tactics for a constant crisis. 253, 744-750.

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Swift, M.J., and Anderson, J. M. (1993). Biodiversity and ecosystem function in agricultural systems. "Biodiversity and Ecosystem Function" (E. D. Schulze and H. A. Mooney, eds.), pp. 15-41. Springer-Verlag, New York. Thompson, L.J., Thomas, C. D., Radley, J. M., Williamson, S., and Lawton, J. H. (1993). The effect of earthworms and snails in a simple plant community. 95, 171-178. Tilman, D., and Downing, J. A. (1994). Biodiversity and stability in grasslands. 367, 363-365. Vandermeer, J. (1989). "The Ecology of Intercropping." Cambridge Univ. Press, Cambridge, UK. Vitousek, e. (1994). Beyond global warming: Ecology and global change. 75,1861-1902. Wilson, E. O., and Peter, F. M. (1988). "Biodiversity." National Academy of Science, Washington, DC.

Predicting Responses of Tropical Plant Communities to Elevated C02: Lessons from Experiments with Model Ecosystems

Tropical ecosystems and plant communities contain an enormous proportion of the world's known species and represent about 42% of the world's biomass carbon reserves (Brown and Lugo, 1982; Olson 1983). Furthermore, these ecosystems are expected to be among the most responsive to the direct effects of rising atmospheric carbon dioxide concentrations (Long, 1991; Hogan 1991; Lugo, 1992). Despite the inevitable importance of tropical ecosystems to global species conservation and to the world's C balance, no experimental data exist on the response of native tropical plant communities to elevated atmospheric CO2! Our knowledge to date is based on a total of seven actual experiments conducted using moist tropical plant species either grown under conditions of nonlimiting nutrient supply as individuals (Oberbauer 1985; Reekie and Bazzaz, 1989; Ziska 1991) or in competitive arrays in model communities (Reekie and Bazzaz, 1989), or in model plant communities with varying degrees of nutrient limitation (Ktrner and Arnone, 1992; Arnone and Ktrner, 1993; Arnone and Ktrner, 1995; and Arnone 1995). In order to improve our chances at accurately predicting the responses of the tropical biome, it is essential to more accurately represent the predominantly low to moderately low soil fertilities found in these regions (e.g., Whittaker, 1975; Sfmchez, 1976). For example, 63% of the soils in the moist tropics is represented by Oxisols and Ultisols (Vitousek and Sanford, 1986). Perhaps a 1 01

Copyright 9 1996 by Academic Press, Inc. All rights of reproduction in any form reserved.

more critical deficit is the complete lack of data on the responses to elevated CO2 of dry tropical vegetation and communities (savannas and scrub vegetation) and even tropical seasonal forests. These terrestrial systems may be among the most responsive to rising atmospheric CO2 because high CO2 reduces leaf stomatal conductance and can reduce plant water use, at least in the short term (e.g., Strain and Cure, 1985; Jackson 1994; see Chiarello and Field, Chapter 10). Despite these deficits in our knowledge and although studies conducted in native tropical systems are desperately needed, we have gained substantial insights into the range of possible responses of native tropical plant communities to elevated CO2 as a result of the diverse data sets generated by these seven experimental studies. Perhaps the most significant finding is that nutrient supply plays a pivotal role in determining the magnitude and speed of responses of various species in a community to elevated CO2. The objective of this chapter is to synthesize our current understanding of how, and through which mechanisms, tropical plant communities will likely respond to rising atmospheric CO2. I particularly emphasize results from the studies with multispecies plant assemblages in which intra- and interspecific competition for above- and belowground resources was incorporated into the experimental design. The reason for this focus stems from the recognition that responses at the community level often cannot be reliably predicted from responses seen in individually grown plants (e.g., Bazzaz and Carlson, 1984; Zangerl and Bazzaz, 1984; Bazzaz and McConnaughay, 1992; K6rner, 1995). However, I attempt to integrate results from pot and model community studies in this synthesis. I would also like to refer the reader to earlier syntheses on the responses of multispecies model communities to elevated CO2 (Bazzaz 1985; K6rner, 1995; Bazzaz, 1990), as well as to works on the potential response of native vegetation (Strain and Bazzaz, 1983; Bazzaz, 1990; Hogan 1991) to high CO2. In addition, K6rner (1993) reviewed the utility of model ecosystems in CO2 research.

Hogan (1991) reviewed the results of the only three experiments to be conducted on individually grown (i.e., potted) tropical plants, and then speculated on the potential responses which might occur at the levels of the plant population, community, and ecosystem. These studies by Oberbauer (1985), Reekie and Bazzaz (1989), and Ziska (1991) have shown that a variety of species from the moist tropics respond both physiologically and in terms of growth to elevated atmospheric CO2. How-

8.

ever, the results from these studies paint a picture that is far from consistent. The responses of the six C~, one C4, and two CAM species observed by Ziska were the most consistent with results typically reported for a wide range of agricultural plants and other temperate species growing under ample nutrient supply (cf. Strain and Cure, 1985). Oberbauer reported a substantial increase in biomass accumulation under elevated CO2 in seedlings of both species tested, but actually measured decreases in leaf-level photosynthesis. Reekie and Bazzaz observed no CO2 effect on biomass or photosynthesis of individually grown plants but did measure decreases in stomatal conductance. Hogan and Ziska attributed the discrepancies among these studies to the negative effects of pot size on sink strength and the potential to respond to elevated CO2 (Ziska used relatively large pots, whereas Oberbauer and Reekie and Bazzaz used relatively small pots) (cf. Thomas and Strain, 1991). Berntson (1993) refuted this claim by showing that the effects of small pot size can be eliminated by increasing nutrient additions. Certainly both pot size and the actual amount of nutrients available to the plant can affect plant growth. Furthermore, all three of these experiments were conducted under unnaturally high nutrient conditions indicating that the species responses to elevated C O 2 observed may be quite untypical. Undoubtedly, the interpretation of C02 responses of potted individuals is confounded by extremes in pot size and by relatively large additions of fertilizer.

A. Species Shifts Although still artificial, model plant communities allow us to assess the responses of species to elevated atmospheric CO2 in an environment which, in most cases, more closely reflects natural competitive conditions than those represented by isolated plants (K6rner 1993). The four experiments with model communities of moist tropical plant species completed to date demonstrate some significant common responses to high CO2 as well as some important differences. All of these studies began with the establishment of replicate plant communities containing either several to many species planted in relatively homogeneous substrates (but all containing some amount of native soil) or, in Arnone and K6rner (1993), a twostoried monoculture in which the responses of overstory and understory plants were compared (Table I). Aside from the number of species used, experimental conditions differed dramatically, especially between the Atnone and K6rner studies and that of Reekie and Bazzaz (1989). Ground area, substrate depth, and average volume of substrate available per individual plant were in some cases orders of magnitude different. Planting density

Substrate

Species Reekie and Bazzaz (1989) 5 species

Functional groups

Moist tropical

Tree Tree Tree Tree Tree KOrner and Arnone (1992) "Experiment I" 15 species Moist tropical

Pioneer tree Tree Shrub Shrub Climbing vine Climbing vine Climbing vine G r o u n d vine G r o u n d vine Herb. m o n c o t Herb. m o n c o t Herb. m o n c o t Herb. m o n c o t Herb. m o n c o t

Planting density (m -s)

400

Ground area (m -s)

0.075

0.30 0.45 0.75 0.30 0.30 0.30 0.30 0.90 0.45 0.30 0.30 0.60 0.30 0.60 0.45

soil: turface (1:1) Fertilizer 4 • ?

11

Vol. (liters)

8

CO2 levels (/~11 -~)

300 525 700

111

340 610

94

LAI

NPP equivalent ( g m - S y r -1)

6.65

sand: vermiculite (1:1) + compost-soil layer Fertilizer 20 g m -s Osmocote NPK and micro. Tot. N equiv, of 400 kg N ha -~

1300

Shift in Biomass spp. abund. response at harvest ~ at harvest (A % rel. to (% of c o n t r o l ) c o n t r o l [COs])

n.s.

n.s.

n.s.

12.3 b 11.9 b 11.4 b

1875 1840 1940

control -2 +3 at 525, 700 +40 +100 +122 +115 -40 -45 +55 +60 -30 +15

6.9 6.6

P = 0.09 2780 3377

P = 0.10 control +11 at 610 +10 +1 +20 +13 +22 -17 + 4 0 (*) +5 +15 +47 (*) +17 +23 - 9 (*) +5 +8

Peter's NPK m Very high: "nonlimiting"

80 80 80 80 80

6.6

Type

Depth (cm)

Effective trt. period (d)

significant

33.0 35.4 at 525, 700 +1.8 +1.6 +4.1 +5.3 -8.0 -17.7 +10.6 +8.5 -8.5 +2.3 P = 0.10

n.s.

13.4 at 610 +0.06 - 5 . 2 3 (*) -0.19 +0.16 +0.74 +0.16 +1.99 (*) -0.08 -0.15 +0.69 (*) +0.12 +2.76 -0.88 -0.15 0.00

Number of communities (n)

Arnone and K6mer (1993) "Experiment II" 1 species Moist tropical (two-storied canopies) Over-/understory

5.7

6.65

same as K6rner & Arnone (1992) Tot. N equiv, of ca. 360 kg N ha -t

3.0/2.7

20

1300

340 610 340

21

Arnone and K6rner (1995) "Experiment HI"

Moist tropical

Tree Tree G r o u n d vine dcot. G r o u n d vine mcot. Herb. m o n c o t Herb. m o n c o t Herb. moncot

a Shifts in species contribution

n.s.

11.6

6.65

0.30 0.45 0.90 0.45 0.30 0.60 0.30

to t o t a l c o m m u n i t y

bIncludes foliage which extended

sand and tropical soil inoculum top layer (1 cm) and dried ground plant material Fertilizer 129 g m -~ NPK and micro. Total N equiv, of 118 kg N ha -~ yr -~

aboveground

beyond the ground

25

1700

340 610

530

4.0 3.9

b i o m a s s ; * * P < 0.01, * P < 0.05, (*) P < 0.15.

area of the tubs (most probably).

cIncludes leaf litter and standing necromass, but excludes root litter.

P = 0.02 375 c

P = 0.02 +18"

n.s. (% understory)

47O ~

1.75/ 0.11 1.73/ 0.08

610

7 species

n.s. 1.86 1.81

+ 1 8 " / + 1 6 n.s.

n.s.

n.s.

n,s. (sig. by spp. groups) 20.4

-18 +35 +136 0 +9 -40 -18

-4.4 +6.4 +0.9 0 +2.9 -4.1 -1.7

815 ~ 910 c

106 was also lower (6.6-11.6 versus 400 individuals per square meter) as was the a m o u n t of nutrients supplied/available in the Arnone and K6rner experiments. The following is a relative ranking of the nutrient availabilities of the four studies: Reekie and Bazzaz (1989)~>)K6rner and Arnone, 1992 > Arnone and K6rner 1993 ~> Arnone and K6rner, 1995. Furthermore, the starting size of individuals used in each experiment varied. Reekie and Bazzaz began with very small seedlings, Arnone and K6rner (1993 and 1995) with larger (30-70 cm tall) but still relatively small stamred individuals, and K6rner and Arnone (1992) with larger (up to 1 m tall) individuals in order to create a highly structured stand from the start which enabled the analysis of the CO2 effects on various life-forms occupying different positions along the vertical light gradient. Finally, the duration of these experiments varied considerably ranging from 21 to 530 days (Table I), and Reekie and Bazzaz were able to include four replicate communities per CO2 treatment, instead of the two used in the Arnone and K6rner studies. Despite the significant increases in community biomass accumulation observed under both ambient and elevated CO2 over the course of all of these experiments, significant CO2-induced shifts in species dominance (or in composition of overstory versus understory plants) were reported for only two of them (Table I). Reekie and Bazzaz (1989) found highly significant and substantial shifts in the contribution of individual tree species to community aboveground biomass with increasing CO2 concentration in stands planted with equal densities of each species. For example, increased in abundance while decreased at elevated CO2. Perhaps most striking is that these shifts occurred even though CO2 level had no effect on overall community aboveground biomass or on leaf area index (LAI). The authors showed that the success of a species was positively related to its mean canopy height measured at harvest. In much more nutrient-poor systems, Arnone and K6rner (1995, Experiment III) reported significant changes in the abundance of groups of species under elevated CO2 but no significant shifts in any single species (Table I). The magnitude of the CO2-induced shifts Arnone and K6rner observed over 530 days were considerably less than those observed by Reekie and Bazzaz (1989). The contribution of a pioneer species, to community biomass was reduced over the course of the experiment and this shift was slightly (n.s.) enhanced under elevated CO2 (Fig. 1). In contrast, the slower-growing and the understory monocot increased in abundance in all communities, with a trend toward even greater increases u n d e r elevated CO2. No significant changes in biomass accumulation or LAI were observed u n d e r elevated CO2. Although no significant overall species shifts were observed in the relatively fast-growing nutrient-rich systems of Experiment I (K6rner and Arnone, 1992), showed a substantial 5% mean decrease in its share of community aboveground

8.

107

Figure 1 Mean changes in the contribution of the seven species of moist tropical plants to communitybiomass (including coarse root biomass) over 530 daysin Experiment III in systems maintained at ambient and elevated atmospheric CO2 concentrations.

biomass (P = 0.11) u n d e r elevated C O 2 measured at harvest, while two other and species showed marginally significant increases in their share of community aboveground biomass (P = 0.14 and 0.08, respectively, Table I). The success of at elevated CO2 u n d e r one set of competitive experimental conditions and its relative failure at elevated CO2 u n d e r another set of conditions does, however, point to the difficulty of predicting species-specific responses to elevated CO2 based on results from model systems alone. Thus, it appears that the most reliable prediction is that some level of shifts in species dominance will take place in native moist tropical communities in a CO2-rich world, and shifts may occur more rapidly in nutrient-rich systems containing very young individuals than in nutrient-poorer systems or in those containing older plants. However, we are unable to predict with any degree of certainty which species will win and which will lose.

B. Individually Grown Versus Competitively Grown Plants How well do the responses of individually grown plants extrapolate to their responses when grown u n d e r competition? Generally, existing data support the notion of a poor correspondence between responses in individually grown plants and competitively grown plants. Reekie and Bazzaz (1989) report correlations between some autecological morphological traits and responses to elevated CO2 in their tropical plants growing u n d e r competitive conditions. However, they found no correlations for other morphological and physiological traits. Perhaps their most interesting finding was that mean canopy height and shape (leaf area profiles) were strongly influ-

108

enced by competition and C O 2 level. Bazzaz and McConnaughay (1992) use data from an experiment by Williams (1988), with serpentine grassland species, to illustrate the pronounced mismatch between projections of community species composition derived from CO2 responses of isolated individuals and their actual success in heterospecific stands. Likewise, the experiments of Arnone and K6rner with model communities of tropical plant species indicate a relatively poor correspondence between prognostications made based on single-plant experiments (Hogan 1991) and responses of plants in multispecies stands. For example, Arnone and K6rner found no uniform increase across all species in leaf area per plant under competitive conditions in any of their three experiments, as is implied by Hogan (1991) and predicted from models (e.g., Oikawa, 1990). Moreover, in none of the three community experiments did Arnone and K6rner find the often predicted CO2-induced increase of LAI (Eamus andJarvis, 1989; Nijs 1989). Even under nonlimiting nutrient conditions, Reekie and Bazzaz (1989) found no effect of CO2 concentration on leaf area per plant of either individuals or plants grown in model communities. When nutrients were supplied at near natural levels, LAI even tended to decrease under elevated CO2 (K6rner and Arnone, 1992; Arnone and K6rner, 1993, 1995). This was associated with higher leaf mortality in a number of species at high CO2 (Fig. 2). These leaf area responses are remarkably consistent over a wide range of nutrient conditions, species mixes, plant life-forms, overall LAIs, and durations of experiments, further exemplifying the danger of simple extrapolation from singleplant responses obtained under unlimited nutrient supply to responses under competition and more realistic nutrient regimes. C. Effects of Plant Morphology on Competitive Performance: Biomass Allocation Patterns and Plant Life-form

In tropical plant species growing competitively in model communities in Experiment III (Arnone and K6rner, 1995), the effects of elevated CO2 on patterns of biomass allocation were similar to those observed in a very large number of other species grown as individual plants (e.g., Strain and Cure, 1985; Rogers 1994; Poorter, 1993). These patterns include greater (initial) enhancement of root growth than shoot growth under elevated CO2 (Fig. 3) and consequently increased allocation to root biomass. These changes are commonly associated with greater root:shoot ratios, lower leaf weight ratios (LWR), and leaf area ratios (LAR) (e.g., Norby 1992) but may not be so pronounced when mineral nutrients are abundant (Oberbauer 1985; Reekie and Bazzaz, 1989; Ziska 1991). For instance, Ziska and coworkers (1991) only found increases in root:shoot ratio in two of nine species, and lower LWRs in half of the C3 species studied.

8.

-

+t I-

E

v m

[~ Arab0~ I

_.1

Time courses of leaf area index (LAI) development in Experiments I, II, and III for communities maintained at ambient (open symbols) and elevated (filled symbols) atmospheric CO2 concentrations (mean _+ SE of two communities per CO2 level).

LWR appears to explain the relative competitive success of the seven species in Experiment III (Arnone and K6rner, 1995). They found that the greater the LWR of a species the larger the positive shifts observed in species dominance within the plant community over the 530-d experiment (Fig. 4). Since no CO2-induced changes were observed in specific leaf area (SLA) for any of the species (Arnone 1995), this relationship also holds true for LAR. This effect was independent of CO2 treatment, however, and the relationship appears to reverse itself if the very high

-2'o o Relative effects of growth under elevated CO2 on LAI, biomass accumulation of various organs, and on production of aboveground necromass in Experiments I, II, and III (difference between mean ambient and elevated values expressed as a percentage of the ambient mean; a, senescing leaves; **, P < 0.01; *, P < 0.05; (*), P < 0.15).

110

o

0-

ffl

Ct

Relationship between leaf weight ratios (LWR, including coarse roots) measured for each of the seven species at the start of the 530-day Experiment III and their competitive outcomes as measured by the change in a species' contribution to total Community biomass over the course of the experiment. Each point represents one species in one of the four communities. Each curve represents a second-order polynomial fitted either to all points (longer curve, r z = 0.52) or to all but the four data points from (shorter curve, r 2 = 0.48). Curves fitted separately to ambient and elevated CO2 points were not different, so the curve shown was fitted to the entire set of points (save Species key: Ct = Ce = Ep = He = E1 = Fib = Fip =

a g r o u n d - c r e e p i n g vine, were i n c l u d e d in the analysis. R e e k i e a n d Bazzaz (1989) u s e d p r i n c i p l e c o m p o n e n t analysis a n d stepwise r e g r e s s i o n to evaluate which m o r p h o l o g i c a l a n d physiological characteristics o f individually g r o w n plants o f five tropical p l a n t species w o u l d best e x p l a i n t h e i r success w h e n g r o w i n g in c o m p e t i t i v e arrays. T h e two m e a s u r e s w h i c h e x p l a i n e d almost 75% o f the variation in c o m p e t i t i v e success were m o r p h o l o g i c a l traits: m e a n c a n o p y h e i g h t a n d leaf a r e a ratio. N e t leaf-level p h o t o s y n t h e s i s e x p l a i n e d less t h a n 9% o f the variability in the data. I n d e e d even in p o t t e d tropical plants, O b e r b a u e r (1985) f o u n d t h a t b i o m a s s a c c u m u l a t i o n was g r e a t e r in plants g r o w n u n d e r elevated CO2 even t h o u g h leaf-level p h o t o s y n t h e s i s was lower in these plants! All o f these o b s e r v a t i o n s g e n e r a l l y suggest t h a t CO2-induced alterations in p l a n t m o r p h o l o g y a n d p l a n t d e v e l o p m e n t may be m o r e useful p r e d i c t o r s o f species' c o m p e t i t i v e success t h a n c h a n g e s in t h e i r p h o t o s y n t h e t i c p e r f o r m a n c e . Biomass allocation p a t t e r n s are closely tied to p l a n t life-form in t h a t c e r t a i n life-forms e x h i b i t various d e g r e e s o f m o r p h o l o g i c a l plasticity in r e s p o n s e to e n v i r o n m e n t a l stimuli a n d to c o m p e t i t i o n . Thus, m o r p h o l o g i -

8.

111

cal constraints can profoundly affect the type and magnitude of response to atmospheric CO2 level (Table I). Once one begins to think in this vein one must consider constraints imposed on a species' resource (light and nutrients) capturing ability conferred on it by both its lateral and vertical space occupancy in the canopy and in the soil. Indeed, Reekie and Bazzaz (1989) showed the importance of differences in canopy height and architecture in determining the success of tropical tree seedlings u n d e r elevated CO2. In Experiment III, Arnone and K6rner also found that plant lifeform could help explain its response in model communities. For example, herbaceous monocots such as were able to proliferate rapidly in lateral directions but could not grow significantly in height, whereas tree species such as and were not able to grow laterally very quickly but could grow in height (Arnone and K6rner, 1995; see also Hunt 1991). the pioneer with its short-lived leaves and rapid growth in open stands, gained an early advantage in all communities. In contrast, the slower growing tree species with its long-lived leaves and its continuous occupation of the soil with its roots allowed it to gradually increase in dominance in all communities, but more so u n d e r elevated CO2. Within the herbaceous monocots, the success of (20% of start biomass and 38% of harvest biomass at ambient CO2, and 41% at elevated CO2) and the relative failure of (39% at the start, 12% and 8%, respectively at harvest) was largely due to the relative slowness of leaf and lateral filler proliferation in more rapid proliferation of new tillers in Furthermore, root systems of were more extensive than those of

D. The Vertical Dimension: Interactive Effects of LAI, Light, and Light Quality Plants growing in competitive arrays shade themselves and each other and create gradients of decreasing light availability from the top to the bottom of the canopy. As LAI increases, light transmittance in the stand decreases. These changes are known to have variable effects on different plant species depending on their position in the community. Under conditions of elevated atmospheric CO2 it has often been hypothesized that LAIs should increase (e.g., Nijs et al., 1989; Eamus and Jarvis, 1989). One reason that this could occur is through an increased production and retention of leaves of understory plants growing in deep shade. Greater leaf retention u n d e r very low photon flux densities (PFDs) u n d e r elevated CO2 could result from improved leaf carbon balance (Pearcy and Bj6rkmann, 1983) afforded by CO2-induced reductions in light compensation point and by increases in q u a n t u m use efficiency (e.g., Ehleringer and Bj6rkmann, 1977). In all three of the Arnone and K6rner experiments and in the study of Reekie and Bazzaz (1989) no evidence in support of this hypothesis was

observed (Table I). In fact, as a consequence of the unchanged LAIs under elevated CO2 (Fig. 2; Reekie and Bazzaz, 1989), no differences in light transmittance within stands has been observed. Accordingly, we found no CO2-induced shifts in vertical leaf area distribution for any of the 15 species growing in the communities in Experiment I (Fig. 5). Thus, LAI appears to be relatively insensitive to atmospheric CO2 concentration. In Experiment II, Arnone and K6rner (1993) specifically examined the responses to elevated CO2 ofunderstory plants growing in two-storied monospecific stands of the extremely fast-growing tropical species Both understory and overstory plants in all communities increased significantly in size over the 21-d CO2 treatment. However, they observed no differences in LAI of either the overstory or understory plant canopies between ambient and elevated CO2 communities (Fig. 3). They also found no enhancement of biomass accumulation in understory plants in high CO2 communities, as was hypothesized, but did observe significantly greater (17%) height growth and internode length of understory plants growing in communities maintained at elevated CO2 (Fig. 3). These growth responses are typical of shade avoidance reactions in response to reductions in the red:far-red ratio (e.g., Smith, 1982), and suggested that elevated CO2 may alter properties of leaves such that they absorb more red light a n d / o r reflect more far-red light (e.g., Ballar6 1987). Indeed, Arnone and K6rner measured significantly lower R:FR ratios beneath overstory leaves produced under elevated CO2 than under leaves produced under ambient CO2. Although these results do not rule out other possible direct effects of elevated CO2 on understory plant behavior, they do suggest that CO2-induced alterations in light quality within a community could eventually have a pronounced effect on plant-plant interactions and competitive outcomes. For example, recruitment patterns and species composition of later successional stages in tree-fall gaps may be affected by shifts in R:FR ratios and variable inherent sensitivities to reductions in R:FR ratio of gapcolonizing species.

250]

Meanleaf area profiles of each of the 15 species growing in model communities in Experiment I after 94 days of exposure to ambient (open symbols) and elevated (filled symbols) atmospheric CO2 concentrations.

8.

E. Photosynthetic Performance as a Determinant of Species' Competitive Success

M. Gruber (unpublished data) measured whole-shoot CO2 exchange of the most dominant species in Experiment III in order to evaluate species' contributions to ecosystem CO2 flux and to test how well shootlevel physiology would correspond to species' competitive performance. Measurements were made in the last third of the experiment with an openIRGA system by enclosing individual shoots from each species in each community in transparent polyethylene bags. During this phase of the experiment relatively pronounced "successional" shifts in species dominance were underway in all communities, however no obvious CO2 treatment effects were seen. Net shoot CO2 flux on each individual was measured at the growth CO2 concentration for about 16 hours, which included the latter half of the photoperiod and most of the dark period. In Experiment III, Gruber found greater shoot assimilation rates under elevated CO2 in all of the four species evaluated (Table II). In and these increases were marginally significant (P < 0.15) and amounted to 53% and 123% of the rates measured at ambient CO2, respectively. Higher assimilation rates under elevated CO2 in may have

Shoot dark respiration

S h o o t assimilation (/~mol CO2 m -2 leaf s -1) Species

Amb. CO 2 2.57 1.41 0.99 0.77

_+ _+ + _+

Elev. CO2

0.39 0.14 0.08 0.20

2.85 2.16 1.04 1.71

+ + _+ _+

0.16 0.27 0.08 0.17

(/~mol CO2 m -2 leaf s -1) Diff. Diff. (%) +11 + 5 3 (*) +6 + 1 2 3 (*)

A m b . COz 0.69 0.24 0.12 0.09

+ +_ +_ _+

0.10 0.04 0.03 0.02

Elev. CO2 0.76 0.27 0.09 0.04

+_ +_+ _+

0.01 0.02 0.02 0.04

(%) +10 +12 -25 -55

a.f ANOVA

CO 2

1

Results

Resid.

2

Species

3

Sp. • C O 2 Residual

3 6

n.s.

n.s.

(*)

Levels of statistical significance: ** = P < 0.01; * = P < 0.05; (*) = P < 0.15. a All parameters were measured at growth CO2 concentrations. Mean net assimilation rates measured on individual leaves on Day 305 were 72% greater (P = 0.03) under elevated CO2 (13.6 _+ 0.2 /~mol CO2 m -s leaf s-1) than under ambient COs (7.9 _+ 1.1 /.~mol COs m -2 leaf s-l). The values in the table are means _+ SE with n = 2 communities per COs level.

114 contributed to its relative greater gains in these communities than in communities maintained at ambient CO2 (Table I). on the other hand, suffered marginally greater losses under elevated CO2 despite its greater shoot assimilation rates and its reduced dark respiration rates. Likewise, the 25% lower (n.s.) shoot dark respiration rates measured in may have conferred a substantial advantage to this species over time and facilitated its relative greater expansion in elevated CO2 communities. Species such as which had similar shoot CO2 assimilation and dark respiration under both ambient and elevated CO2, but surprisingly 72% greater leaf-level photosynthesis (see legend of Table II), tended to lose a greater share in community biomass by the end of the experiment. This again illustrates the unreliability of using physiological traits alone to predict competitive outcomes. Thus it can be argued that physiological performance with respect to shoot C O 2 balance may have contributed to competitive outcome in some species but may have been relatively unimportant determinants of success in other species. The same held true for the connections between leaf stomatal conductance and species competitive outcome in Experiment III. In the latter third of this experiment, A. Kocyan (unpublished data) measured substantial decreases in leaf diffusive conductance under elevated CO2 in the five most dominant species, but only small reductions (5%) in whole ecosystem evapotranspiration. It is unclear how lower water consumption by any of the species would confer any particular competitive advantage since water was not limiting in this experiment. No differences in leaf stomatal conductance between ambient and elevated CO2 were found in Experiment I, and this corresponded well with the absence of differences in ecosystem evapotranspirational water losses. Due to the 75 % greater LAI in this experiment (--- 7), relative to Experiment III (~- 4), air humidity was higher and may have precluded stomatal responses to CO2.

F. Belowground Interactions among Plants' and Species' Competitive Success Under elevated atmospheric CO2 levels, competition for nutrients (e.g., phosphorus) should increase as a result of greater root growth, greater allocation of carbon to root systems, and maintenance of larger fine root populations of many or all plant species within a community. Thus the importance of interactions among roots and between roots and soil organisms would also be expected to increase in a CO2-rich world, but these have not been quantified. However, qualitative observations on the timing and extent of root growth and proliferation of various species in model communities confirm the major role they play in determining competitive outcome regardless of CO2 effects. For example, Bazzaz (1990) attributed the relatively successful outcome of higher atmospheric CO2 concentrations

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(see Reekie and Bazzaz, 1989) to its greater allocation to roots and ultimately to its rapid occupation of the soil volume early in the experiment. Arnone and K6rner (1995) observed a similar p h e n o m e n o n in their Experiment III under relatively nutrient-poor conditions. Early in the experiment (first 100 d), the pioneer species quickly occupied the entire top several centimeters of the soil with its fine roots and grew equally rapidly in height under both ambient and elevated CO2. As the experiment progressed, root systems and shoots of the understory herbaceous monocots (especially and the relatively slow growing trees began to compete strongly with its growth. By the end of the experiment (530 days) in all communities had lost tremendous share in its contribution to community leaf area and biomass, especially. Belowground competitive pressure from a species with leaves unable to shade those of appeared to be the main cause for the severe suppression of growth in all communities, and this effect tended to increase at high CO2. In another experiment embedded in Experiment III (J. Arnone, unpublished data), abilities of species to exploit nutrient-rich soil microsites in an otherwise "nutrient-limited" system were investigated. A pronounced increase in proliferation of fine roots (-<2 mm) in nutrient patches (created using fertilizer sticks inserted vertically over the entire soil depth) was observed under both CO2 regimes. Surprisingly, however, no overall increase in proliferation was observed under elevated CO2, nor were any species-specific fine root responses evident. Apparently, fine root proliferation in this system was not carbon limited.

G. Insect Herbivory and Plant Species Dominance When other biological factors which are known to influence plant community structure are incorporated in analyses of vegetation responses to elevated CO2, the need for field experimentation becomes more obvious. For example, Coley (1983) showed that insect herbivores can dramatically affect plant growth and ecology in tropical ecosystems, and further demonstrated differential species responses to herbivory as affected by resource availability and investment in defense compounds (Coley 1985). In all but two experiments (Thompson and Drake, 1994; Arnone 1995) reported so far designed to evaluate the effects of elevated CO2 on insect herbivory, feeding responses have been measured either by providing larvae in petri dishes with leaf material produced under ambient and elevated CO2, or by placing larvae on individual plants (cf. Lincoln 1993). Predictions based on these studies indicate that larvae will eat more leaf tissue on high CO2-grown plants in order to compensate for lower leaf nutritional quality (i.e., lower C:N ratios) and that larval fitness will decline (e.g., Fajer 1991). Although these studies have provided useful infor-

m a t i o n a b o u t the r e s p o n s e s of insect herbivores to c h a n g e s in leaf tissue quality, they are i n h e r e n t l y i n a d e q u a t e for p r e d i c t i n g how herbivory may be affected in c o m p l e x c o m m u n i t i e s w h e r e h e r b i v o r e s n o t only r e s p o n d to variations in leaf n u t r i t i o n a l quality, b u t w h e r e they can c h o o s e a m o n g species a n d positions in the c a n o p y in which to feed. Results f r o m an e x p e r i m e n t c o n d u c t e d at the e n d of E x p e r i m e n t III (Arnone 1995) illustrate these points. A r n o n e a n d co-workers i n t r o d u c e d e q u i v a l e n t p o p u l a t i o n s of f o u r t h instar a lepidopteran generalist, to c o m p l e x m o d e l ecosystems c o n t a i n i n g seven species of moist tropical plants m a i n t a i n e d u n d e r low m i n e r a l n u t r i e n t supply. Larvae were allowed to feed freely for 14 days by which time they h a d r e a c h e d the seventh instar. Prior to larval i n t r o d u c t i o n s , p l a n t c o m m u n i t i e s h a d b e e n c o n t i n u o u s l y e x p o s e d to e i t h e r a m b i e n t or elevated CO2 for 1.5 years. In c o n t r a s t to E x p e r i m e n t I w h e r e n u t r i e n t supply was relatively h i g h ( K 6 r n e r a n d A r n o n e , 1992, Table III), n o m a j o r shifts in leaf n u t r i t i o n a l quality (e.g., leaf n i t r o g e n c o n c e n t r a t i o n , Fig. 6) were observed in this low fertility system b e t w e e n CO2 t r e a t m e n t s for any of the seven species. F u r t h e r m o r e , n o c o r r e l a t i o n s were observed b e t w e e n leaf quality a n d leaf biomass cons u m p t i o n by larvae (e.g., Fig. 6). In situations w h e r e significant r e d u c t i o n s in l e a f N c o n c e n t r a t i o n s o c c u r (Table III, E x p e r i m e n t I), h e r b i v o r e f e e d i n g

Species

Amb. CO2

Elev. CO2

Diff. (A%)

20.6 +- 1.2 12.4 + 0.1 15.6 + 0.4 18.6 + 0.5 22.0 + 0.7 18.9 _+ 0.6 14.6 + 0.3 20.7 + 0.8 16.3 _+ 0.6 16.6 +_ 0.6 16.1 +_ 0.7 18.8 _+ 0.6 17.7 _+ 0.8 12.7 -+ 0.3 12.8 _+ 0.4

16.0 _+ 0.6 10.9 + 0.2 12.8 + 0.2 17.1 _+ 0.4 18.9 +_ 0.8 16.8 _+ 0.7 11.7 _+ 0.3 19.1 + 0.3 15.1 _+ 0.4 15.1 _+ 0.4 14.9 _+ 0.5 18,3 _+ 0.5 15.0 _+ 0.7 11.3 +_ 0.2 13.0 +_ 0.4

-4.6 -1.5 -2.8 -1.5 -3.1 -2.1 -2.9 -1.6 -1.5 -1.5 -1.2 -0.5 -2.7 -1.4 +0.2

8. 0.4

0.3" J... r

0.2-

t~

0.1"13

E tO

0.0 0.4

. . . .

. . . .

E

. 0~ ..Q

_1

|

|

20 Leaf nitrogen concentration (mg N g-l) Figure 6 Species' leaf biomass consumption by late-instar larvae after 14 days of feeding as a function of leaf nitrogen concentration for plants growing in communities which had been exposed for 515 days to either ambient (open symbols) or elevated (filled symbols) atmospheric CO2 concentrations in Experiment III. Key: (a) through (d): men 9 (e) and (f): dicots. LeafN concentrations shown as insets represent the mean _ SE of two communities per CO2 level.

may still be strongly determined by this factor. Total leaf area (IAI = 4) and biomass of all plant communities were similar when caterpillars were introduced. However, leaf biomass of some species was slightly g r e a t e r - and for other species slightly less (e.g., communities exposed to elevated CO2. Larvae showed the strongest preference for leaves, the plant species that was least abundant in all communities (and which lost in relative abundance under high CO2), and fed relatively little on plants species which were more abundant. Interspecific differences in leaf quality most certainly influence feeding patterns of these generalists. Low concentrations of defense compounds in leaves may have accounted at least in part for the overwhelming preference shown for them by the larvae (cf. Coley 1985). These results indicate leaf tissue quality is not necessarily affected by elevated CO2 when nutrient supply is very restricted. However, on nutrientrich sites, and where "choice" of food is limited (e.g., only two species of graminoids), leaf nutritional quality may still be a major determinant of herbivory (Thompson and Drake, 1994). Herbivores appear to become

more dependent on less-preferred plant species in cases where elevated CO2 results in reduced availability of leaves of a favored plant species. This greater dependency may eventually affect insect populations adversely. Thus, once again we see a more complex and quite different response to an elevation of atmospheric carbon dioxide when results from leaf/ individual-plant studies are compared with those obtained in relatively complex systems. In native systems, insect herbivores may either amplify or suppress changes in plant species' abundance caused directly by variable responses to elevated CO2.

Perhaps the most significant lesson from this handful of experimental studies with tropical plants is that responses of individually grown plants to high CO2 do not scale well (with consistent predictability) to those obtained when individuals are grown under competitive conditions. For example, predictions of dramatic increases in biomass accumulation and leaf area production at the level of the community, especially in naturally "nutrient-limited" systems, is consistently contradicted by evidence from model and communities (e.g., see also K6rner, 1995). More astonishing is that shifts in species' abundance have occurred in model systems under elevated CO2 even in the absence of significant overall stimulation of biomass accumulation. Sufficient evidence now exists to state with some degree of confidence that the speed and extent to which shifts occur under elevated CO~ is linked to the age of the plants and to the availability of other growth-limiting resourcesmespecially nutrients. Furthermore, results from Experiments I-III, where Arnone and K6rner attempted to link community-level changes with those occurring at the level of the entire ecosystem, indicate that in nature innumerable positive and negative feedbacks occurring at all levels of system complexity will influence the structure and composition of plant communities (e.g., effects of herbivory, changes in light quality within the stand, and increased rhizodeposition on nitrogen availability) (cf. Diaz 1993; Arnone, 1995; Zak 1993). For the most part, the consequences of such complicated interactions among biotic and abiotic factors and elevated atmospheric CO2 cannot be predicted with any degree of satisfaction for any native system. At present, we are incapable of making sound predictions of the nature and extent of shifts in native communities. Working in native vegetation may help us overcome some of the major limitations of working in model systems-effects on the actual specific competitive outcomes and species' shifts created by the particular choice of species, life-forms, and their relative abundances and arrangements used in artificial communities. However, it

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will also introduce greater experimental noise and may make the detection of CO2 effects more difficult. Therefore, specifically designed and coordinated experiments in both native and model systems will yield the most fruitful results. The ecologically important c o m m o n responses observed across all of these model systems, in spite of the strong effects which resulted from a given community design and growth conditions, attests to their robustness. Thus the best place to begin perhaps is to test whether and to what extent the c o m m o n responses to elevated COz found in all model systems thus far occur in native systems in the field. For now, all we can say with any degree of certainty is that elevated atmospheric COz concentrations will lead to changes in species dominance in tropical plant communities, just as it will in other geographic regions. Eventually this will alter patterns of plant succession and vegetation cover.

I am grateful to my colleagues at the Botanisches Institut of the University of Basel who generously assisted me with many aspects of the studies