Functional Plant Ecology Second Edition potx

Functional
Plant
Ecology
Second Edition
Francisco Pugnaire/Functional Plant Ecology 7488_C000 Final Proof page i 12.5.2007 2:00pm Compositor Name: JGanesan
BOOKS IN SOILS, PLANTS, AND THE ENVIRONMENT
Editorial Board
Agricultural Engineering Robert M. Peart, University of Florida, Gainesville
Crops Mohammad Pessarakli, University of Arizona, Tucson
Environment Kenneth G. Cassman, University of Nebraska,
Lincoln
Irrigation and Hydrology Donald R. Nielsen, University of California, Davis
Microbiology Jan Dirk van Elsas, Research Institute for Plant
Protection, Wageningen, The Netherlands
Plants L. David Kuykendall, U.S. Department of
Agriculture, Beltsville, Maryland
Kenneth B. Marcum, Arizona State University, Tempe
Soils Jean-Marc Bollag, Pennsylvania State University,
University Park
Tsuyoshi Miyazaki, University of Tokyo, Japan
Soil Biochemistry,Volume 1, edited by A. D. McLaren
and G. H. Peterson
Soil Biochemistry,Volume 2, edited by A. D. McLaren and J. Skujins
Soil Biochemistry,Volume 3, edited by E. A. Paul and A. D. McLaren
Soil Biochemistry,Volume 4, edited by E. A. Paul and A. D. McLaren
Soil Biochemistry,Volume 5, edited by E. A. Paul and J. N. Ladd
Soil Biochemistry,Volume 6, edited by Jean-Marc Bollag
and G. Stotzky
Soil Biochemistry,Volume 7, edited by G. Stotzky
and Jean-Marc Bollag

Soil Biochemistry,Volume 8, edited by Jean-Marc Bollag
and G. Stotzky
Francisco Pugnaire/Functional Plant Ecology 7488_C000 Final Proof page ii 12.5.2007 2:00pm Compositor Name: JGanesan
Soil Biochemistry,Volume 9, edited by G. Stotzky
and Jean-Marc Bollag
Organic Chemicals in the Soil Environment,Volumes 1 and 2,
edited by C. A. I. Goring and J. W. Hamaker
Humic Substances in the Environment, M. Schnitzer and S. U. Khan
Microbial Life in the Soil: An Introduction, T. Hattori
Principles of Soil Chemistry, Kim H. Tan
Soil Analysis: Instrumental Techniques and Related Procedures,
edited by Keith A. Smith
Soil Reclamation Processes: Microbiological Analyses and
Applications, edited by Robert L. Tate III and Donald A. Klein
Symbiotic Nitrogen Fixation Technology, edited by Gerald H. Elkan
Soil-–Water Interactions: Mechanisms and Applications, Shingo Iwata
and Toshio Tabuchi with Benno P. Warkentin
Soil Analysis: Modern Instrumental Techniques, Second Edition,
edited by Keith A. Smith
Soil Analysis: Physical Methods, edited by Keith A. Smith
and Chris E. Mullins
Growth and Mineral Nutrition of Field Crops, N. K. Fageria,
V. C. Baligar, and Charles Allan Jones
Semiarid Lands and Deserts: Soil Resource and Reclamation,
edited by J. Skujins
Plant Roots: The Hidden Half, edited by Yoav Waisel, Amram Eshel,
and Uzi Kafkafi
Plant Biochemical Regulators, edited by Harold W. Gausman
Maximizing Crop Yields, N. K. Fageria
Transgenic Plants: Fundamentals and Applications, edited by

Andrew Hiatt
Soil Microbial Ecology: Applications in Agricultural and Environmental
Management, edited by F. Blaine Metting, Jr.
Principles of Soil Chemistry: Second Edition, Kim H. Tan
Water Flow in Soils, edited by Tsuyoshi Miyazaki
Handbook of Plant and Crop Stress, edited by Mohammad Pessarakli
Genetic Improvement of Field Crops, edited by Gustavo A. Slafer
Agricultural Field Experiments: Design and Analysis,
Roger G. Petersen
Environmental Soil Science, Kim H. Tan
Mechanisms of Plant Growth and Improved Productivity: Modern
Approaches, edited by Amarjit S. Basra
Selenium in the Environment, edited by W. T. Frankenberger, Jr.
and Sally Benson
Plant–Environment Interactions, edited by Robert E. Wilkinson
Francisco Pugnaire/Functional Plant Ecology 7488_C000 Final Proof page iii 12.5.2007 2:00pm Compositor Name: JGanesan
Handbook of Plant and Crop Physiology, edited by
Mohammad Pessarakli
Handbook of Phytoalexin Metabolism and Action, edited by M. Daniel
and R. P. Purkayastha
Soil–Water Interactions: Mechanisms and Applications, Second
Edition, Revised and Expanded, Shingo Iwata, Toshio Tabuchi,
and Benno P. Warkentin
Stored-Grain Ecosystems, edited by Digvir S. Jayas, Noel D. G. White,
and William E. Muir
Agrochemicals from Natural Products, edited by C. R. A. Godfrey
Seed Development and Germination, edited by Jaime Kigel
and Gad Galili
Nitrogen Fertilization in the Environment, edited by
Peter Edward Bacon

Phytohormones in Soils: Microbial Production and Function,
William T. Frankenberger, Jr., and Muhammad Arshad
Handbook of Weed Management Systems, edited by Albert E. Smith
Soil Sampling, Preparation, and Analysis, Kim H. Tan
Soil Erosion, Conservation, and Rehabilitation, edited by
Menachem Agassi
Plant Roots: The Hidden Half, Second Edition, Revised and
Expanded, edited by Yoav Waisel, Amram Eshel,
and Uzi Kafkafi
Photoassimilate Distribution in Plants and Crops: Source–Sink
Relationships, edited by Eli Zamski and Arthur A. Schaffer
Mass Spectrometry of Soils, edited by Thomas W. Boutton
and Shinichi Yamasaki
Handbook of Photosynthesis, edited by Mohammad Pessarakli
Chemical and Isotopic Groundwater Hydrology: The Applied
Approach, Second Edition, Revised and Expanded,
Emanuel Mazor
Fauna in Soil Ecosystems: Recycling Processes, Nutrient Fluxes,
and Agricultural Production, edited by Gero Benckiser
Soil and Plant Analysis in Sustainable Agriculture and Environment,
edited by Teresa Hood and J. Benton Jones, Jr.
Seeds Handbook: Biology, Production, Processing, and Storage,
B. B. Desai, P. M. Kotecha, and D. K. Salunkhe
Modern Soil Microbiology, edited by J. D. van Elsas, J. T. Trevors,
and E. M. H. Wellington
Growth and Mineral Nutrition of Field Crops: Second Edition,
N. K. Fageria, V. C. Baligar, and Charles Allan Jones
Fungal Pathogenesis in Plants and Crops: Molecular Biology
and Host Defense Mechanisms, P. Vidhyasekaran
Francisco Pugnaire/Functional Plant Ecology 7488_C000 Final Proof page iv 12.5.2007 2:00pm Compositor Name: JGanesan

Plant Pathogen Detection and Disease Diagnosis, P. Narayanasamy
Agricultural Systems Modeling and Simulation, edited by
Robert M. Peart and R. Bruce Curry
Agricultural Biotechnology, edited by Arie Altman
Plant–Microbe Interactions and Biological Control, edited by
Greg J. Boland and L. David Kuykendall
Handbook of Soil Conditioners: Substances That Enhance
the Physical Properties of Soil, edited by Arthur Wallace
and Richard E. Terry
Environmental Chemistry of Selenium, edited by
William T. Frankenberger, Jr., and Richard A. Engberg
Principles of Soil Chemistry: Third Edition, Revised and Expanded,
Kim H. Tan
Sulfur in the Environment, edited by Douglas G. Maynard
Soil–Machine Interactions: A Finite Element Perspective, edited by
Jie Shen and Radhey Lal Kushwaha
Mycotoxins in Agriculture and Food Safety, edited by Kaushal K.
Sinha and Deepak Bhatnagar
Plant Amino Acids: Biochemistry and Biotechnology, edited by
Bijay K. Singh
Handbook of Functional Plant Ecology, edited by Francisco I.
Pugnaire and Fernando Valladares
Handbook of Plant and Crop Stress: Second Edition, Revised
and Expanded, edited by Mohammad Pessarakli
Plant Responses to Environmental Stresses: From Phytohormones
to Genome Reorganization, edited by H. R. Lerner
Handbook of Pest Management, edited by John R. Ruberson
Environmental Soil Science: Second Edition, Revised and Expanded,
Kim H. Tan
Microbial Endophytes, edited by Charles W. Bacon

and James F. White, Jr.
Plant–Environment Interactions: Second Edition, edited by
Robert E. Wilkinson
Microbial Pest Control, Sushil K. Khetan
Soil and Environmental Analysis: Physical Methods, Second Edition,
Revised and Expanded, edited by Keith A. Smith
and Chris E. Mullins
The Rhizosphere: Biochemistry and Organic Substances at the
Soil–Plant Interface, edited by Roberto Pinton, Zeno Varanini,
and Paolo Nannipieri
Woody Plants and Woody Plant Management: Ecology, Safety,
and Environmental Impact, Rodney W. Bovey
Metals in the Environment, M. N. V. Prasad
Francisco Pugnaire/Functional Plant Ecology 7488_C000 Final Proof page v 12.5.2007 2:00pm Compositor Name: JGanesan
Plant Pathogen Detection and Disease Diagnosis: Second Edition,
Revised and Expanded, P. Narayanasamy
Handbook of Plant and Crop Physiology: Second Edition, Revised
and Expanded, edited by Mohammad Pessarakli
Environmental Chemistry of Arsenic, edited by
William T. Frankenberger, Jr.
Enzymes in the Environment: Activity, Ecology, and Applications,
edited by Richard G. Burns and Richard P. Dick
Plant Roots: The Hidden Half,Third Edition, Revised and Expanded,
edited by Yoav Waisel, Amram Eshel, and Uzi Kafkafi
Handbook of Plant Growth: pH as the Master Variable, edited by
Zdenko Rengel
Biological Control of Major Crop Plant Diseases edited by
Samuel S. Gnanamanickam
Pesticides in Agriculture and the Environment, edited by
Willis B. Wheeler

Mathematical Models of Crop Growth and Yield, , Allen R. Overman
and Richard Scholtz
Plant Biotechnology and Transgenic Plants, edited by
Kirsi-Marja Oksman Caldentey and Wolfgang Barz
Handbook of Postharvest Technology: Cereals, Fruits,Vegetables,Tea,
and Spices, edited by Amalendu Chakraverty,
Arun S. Mujumdar, G. S. Vijaya Raghavan,
and Hosahalli S. Ramaswamy
Handbook of Soil Acidity, edited by Zdenko Rengel
Humic Matter in Soil and the Environment: Principles
and Controversies, edited by Kim H. Tan
Molecular Host Plant Resistance to Pests, edited by S. Sadasivam
and B. Thayumanayan
Soil and Environmental Analysis: Modern Instrumental Techniques,
Third Edition, edited by Keith A. Smith and Malcolm S. Cresser
Chemical and Isotopic Groundwater Hydrology,Third Edition,
edited by Emanuel Mazor
Agricultural Systems Management: Optimizing Efficiency
and Performance, edited by Robert M. Peart
and W. David Shoup
Physiology and Biotechnology Integration for Plant Breeding,
edited by Henry T. Nguyen and Abraham Blum
Global Water Dynamics: Shallow and Deep Groundwater: Petroleum
Hydrology: Hydrothermal Fluids, and Landscaping, , edited by
Emanuel Mazor
Principles of Soil Physics, edited by Rattan Lal
Seeds Handbook: Biology, Production, Processing, and Storage,
Second Edition, Babasaheb B. Desai
Francisco Pugnaire/Functional Plant Ecology 7488_C000 Final Proof page vi 12.5.2007 2:00pm Compositor Name: JGanesan
Field Sampling: Principles and Practices in Environmental Analysis,

edited by Alfred R. Conklin
Sustainable Agriculture and the International Rice-Wheat System,
edited by Rattan Lal, Peter R. Hobbs, Norman Uphoff,
and David O. Hansen
Plant Toxicology, Fourth Edition, edited by Bertold Hock
and Erich F. Elstner
Drought and Water Crises: Science,Technology, and Management
Issues, edited by Donald A. Wilhite
Soil Sampling, Preparation, and Analysis, Second Edition, Kim H. Tan
Climate Change and Global Food Security, edited by Rattan Lal,
Norman Uphoff, B. A. Stewart, and David O. Hansen
Handbook of Photosynthesis, Second Edition, edited by
Mohammad Pessarakli
Environmental Soil-Landscape Modeling: Geographic Information
Technologies and Pedometrics, edited by Sabine Grunwald
Water Flow In Soils, Second Edition, Tsuyoshi Miyazaki
Biological Approaches to Sustainable Soil Systems, edited by
Norman Uphoff, Andrew S. Ball, Erick Fernandes, Hans Herren,
Olivier Husson, Mark Laing, Cheryl Palm, Jules Pretty, Pedro
Sanchez, Nteranya Sanginga, and Janice Thies
Plant–Environment Interactions,Third Edition, edited by Bingru Huang
Biodiversity In Agricultural Production Systems, edited by
Gero Benckiser and Sylvia Schnell
Organic Production and Use of Alternative Crops, Franc Bavec
and Martina Bavec
Handbook of Plant Nutrition, edited by Allen V. Barker
and David J. Pilbeam
Modern Soil Microbiology, Second Edition, edited by
Jan Dirk van Elsas, Janet K. Jansson, and Jack T. Trevors
The Rhizosphere: Biochemistry and Organic Substances

at the Soil-Plant Interface, Second Edition, edited by
Roberto Pinton, Zeno Varanini, and Paolo Nannipieri
Functional Plant Ecology, Second Edition, edited by
Francisco I. Pugnaire and Fernando Valladares
Francisco Pugnaire/Functional Plant Ecology 7488_C000 Final Proof page vii 12.5.2007 2:00pm Compositor Name: JGanesan
Francisco Pugnaire/Functional Plant Ecology 7488_C000 Final Proof page viii 12.5.2007 2:00pm Compositor Name: JGanesan
Functional
Plant
Ecology
edited by
Francisco I. Pugnaire
Fernando Valladares
Second Edition
CRC Press is an imprint of the
Taylor & Francis Group, an informa business
Boca Raton London New York
Francisco Pugnaire/Functional Plant Ecology 7488_C000 Final Proof page ix 12.5.2007 2:00pm Compositor Name: JGanesan
CRC Press
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© 2007 by Taylor & Francis Group, LLC
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Library of Congress Cataloging-in-Publication Data
Functional plant ecology / edited by Francisco Pugnaire and Fernando Valladares. 2nd ed.
p. cm. (Books in soils, plants, and the environment ; 120)
Rev. ed. of: Handbook of functional plant ecology / edited by Francisco I. Pugnaire, Fernando
Valladares. c1999.
Includes bibliographical references and index.
ISBN 978-0-8493-7488-3
1. Plant ecology. 2. Plant ecophysiology. I. Pugnaire, Francisco I., 1957- II. Valladares, Fernando,
1965- III. Handbook of functional plant ecology. IV. Title. V. Series.
QK901.H295 2007
581.7 dc22 2007000591
Visit the Taylor & Francis Web site at

and the CRC Press Web site at

Francisco Pugnaire/Functional Plant Ecology 7488_C000 Final Proof page x 12.5.2007 2:00pm Compositor Name: JGanesan
Table of Contents
Preface xiii
Editors xv

Contributors xvii
Chapter 1 Methods in Comparative Functional Ecology 1
Carlos M. Duarte
Chapter 2 Opportunistic Growth and Desiccation Tolerance: The Ecological
Success of Poikilohydrous Autotrophs 7
Ludger Kappen and Fernando Valladares
Chapter 3 Ecological Significance of Inherent Variation in Relative Growth Rate
and Its Components 67
Hendrik Poorter and Eric Garnier
Chapter 4 The Architecture of Plant Crowns: From Design Rules to Light
Capture and Performance 101
Fernando Valladares and U
¨
lo Niinemets
Chapter 5 Structure and Function of Root Systems 151
Robert B. Jackson, William T. Pockman, William A. Hoffmann, Timothy M. Bleby,
and Cristina Armas
Chapter 6 Water Relations and Hydraulic Architecture 175
Melvin T. Tyree
Chapter 7 Responses of Plants to Heterogeneous Light Environments 213
Robert W. Pearcy
Chapter 8 Acquisition, Use, and Loss of Nutrients 259
Frank Berendse, Hans de Kroon, and Wim G. Braakhekke
Chapter 9 Functional Attributes in Mediterranean-Type Ecosystems 285
Richard Joffre, Serge Rambal, and Claire Damesin
Francisco Pugnaire/Functional Plant Ecology 7488_C000 Final Proof page xi 12.5.2007 2:00pm Compositor Name: JGanesan
xi
Chapter 10 Tropical Forests: Diversity and Function of Dominant Life-Forms 313
Ernesto Medina
Chapter 11 Plant Diversity in Tropical Forests 351

S. Joseph Wright
Chapter 12 Arctic Ecology 369
Sarah E. Hobbie
Chapter 13 Plant Life in Antarctica 389
T.G. Allan Green, Burkhard Schroeter, and Leopoldo G. Sancho
Chapter 14 Facilitation in Plant Communities 435
Ragan M. Callaway and Francisco I. Pugnaire
Chapter 15 Plant Interactions: Competition 457
Heather L. Reynolds and Tara K. Rajaniemi
Chapter 16 Plant–Herbivore Interaction: Beyond a Binary Vision 481
Elena Baraza, Regino Zamora, Jose
´
A. Ho
´
dar, and Jose
´
M. Go
´
mez
Chapter 17 Ecology of Plant Reproduction: Mating Systems and Pollination 515
Anna Traveset and Anna Jakobsson
Chapter 18 Seed and Seedling Ecology 549
Kaoru Kitajima
Chapter 19 Biodiversity and Interactions in the Rhizosphere: Effects
on Ecosystem Functioning 581
Susana Rodrı
´
guez-Echeverrı
´
a, Sofia R. Costa, and Helena Freitas

Chapter 20 Resistance to Air Pollutants: From Cell to Community 601
Jeremy Barnes, Alan Davison, Luis Balaguer, and Esteban Manrique-Reol
Chapter 21 Canopy Photosynthesis Modeling 627
Wolfram Beyschlag and Ronald J. Ryel
Chapter 22 Ecological Applications of Remote Sensing at Multiple Scales 655
John A. Gamon, Hong-Lie Qiu, and Arturo Sanchez-Azofeifa
Chapter 23 Generalization in Functional Plant Ecology: The Species-Sampling
Problem, Plant Ecology Strategy Schemes, and Phylogeny 685
Mark Westoby
Index 705
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xii Table of Contents
Preface
Diversity of plant form and life history and their distribution onto different habitats suggest
that plant functions should underlie this diversity, providing tools to successfully and differ-
entially thrive in every habitat. The knowledge of these functions is then the key to under-
stand community and ecosystem structure and functioning, something that attracted the
interest and effort of many plant ecologists trying to establish patterns of adaptive special-
ization in plants.
This volume on Functional Plant Ecology is an updated version of a successful first edition
in which we tried to put together chapters from all areas of plant ecology to provide readers
the broadest view of functional approaches to plant ecology. Our aim was to gather original
reviews with an attractive presentation, giving a comprehensive overview of the topic with a
historical perspective when needed. The book is intended for a broad audience, from plant
ecologists to students, with characteristics of both a textbook and an essay book. We were not
interested in presentation of new experimental data, novel theoretical interpretations, or
hypotheses, but rather asked the authors to provide easy-to-read, up-to-date, and suggestive
introductions to each topic.
Deciding the book composition was not an easy task, as many attractive, substantial
topics emerged at first glimpse. Finally, only a short number made their way into the book,

and we are aware that many important questions have been left out, but practical and
technical reasons limited the extent of the volume. The book follows a bottom-up approach,
from the more specific, detailed studies focusing on plant organs to the broadest ecosystem
approaches, each gathering chapters on the most outstanding aspects.
The history, aims, and potentials of functional approaches are established in the first
chapter, which also sets the limits of functional plant ecology, a science centered in the study
of whole plants and that attempts to predict responses in plant functioning caused by envir-
onmental clues, emphasizing plant influence on ecosystem functions, services, and products,
and aiming to extract patterns and functional laws from comparative analyses. The search for
these patterns is likely to be most effective if driven by specific hypotheses tested on the basis of
comparative analyses at the broadest possible scale. Functional laws thus developed may hold
predictive power irrespective of whether they represent direct cause–effect relationships. Yet,
the nested nature of the control of functional responses implies uncertainties when scaling
functional laws, either toward lower or higher levels of organization.
We would like to express our sincere thanks to the authors who contributed to this
volume for their efforts in updating their chapters and for meeting the deadlines over already
busy timetables. Finally, we want to thank John Sulzycki for his support throughout and Pat
Roberson for her help and patience. All of them made possible and greatly improved the
quality of this work.
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xiii
Francisco Pugnaire/Functional Plant Ecology 7488_C000 Final Proof page xiv 12.5.2007 2:00pm Compositor Name: JGanesan
Editors
Francisco I. Pugnaire is a research scientist at the Arid Zones Experimental Station in
Almerı
´
a, Spain, an Institute of the Spanish National Council for Scientific Research. Author
of numerous publications, his research interests focus on physiological ecology and commu-
nity dynamics and on the effects of current environmental changes on biodiversity. He is
actively involved in several EU and national initiatives in the science–policy interface.

Centered on semiarid environments, he has also worked in desert ecosystems, tropical forests,
and high mountain environments. Member of the editorial board of several international
journals, he is also a member of the ecological societies of Spain, UK, and USA and vice
president of the European Ecological Federation.
Fernando Valladares is currently a senior scientist of the Spanish Research Council (CSIC) at
the Centre of Environmental Sciences and associate professor at the Rey Juan Carlos
University of Madrid. He has published more than 150 scientific articles, and is the author
or coauthor of 5 books. Dr. Valladares is a member of the editorial board of three of the most
prestigious international journals of plant ecology and physiology, and he is an active
member of the main ecological societies of Spain, UK, and USA. Dr. Valladares is involved
in several panels and expert committees addressing global change issues and transferring
ecological knowledge to society and policy makers at both national and international levels.
His research on functional plant ecology and evolution is focused on phenotypic plasticity
and on the physiological and morphological strategies of photosynthetic organisms to cope
with changing and adverse environmental conditions. The research has been carried out in a
range of ecosystems, spanning from Antarctica to the tropical rain forest, although his
current research objectives are centered on low-productivity Mediterranean ecosystems.
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xv
Francisco Pugnaire/Functional Plant Ecology 7488_C000 Final Proof page xvi 12.5.2007 2:00pm Compositor Name: JGanesan
Contributors
Cristina Armas
Department of Biology
Duke University
Durham, North Carolina
Luis Balaguer
Department of Plant Biology
Complutense University
Madrid, Spain
Elena Baraza

Laboratory of Ecology of Communities
Institute of Ecology
UNAM, Mexico D.F.
Jeremy Barnes
Institute for Research on the Enviornment
and Sustainability
Newcastle University
Newcastle upon Tyne, England
Frank Berendse
Centre for Ecosystem Studies
Wageningen University
Wageningen, The Netherlands
Wolfram Beyschlag
Department of Experimental and
Systems Ecology
University of Bielefeld
Bielefeld, Germany
Timothy M. Bleby
Department of Biology
Duke University
Durham, North Carolina
Wim G. Braakhekke
Centre for Ecosystem Studies
Wageningen University
Wageningen, The Netherlands
Ragan M. Callaway
Division of Biological Sciences
University of Montana
Missoula, Montana
Sofia R. Costa

Department of Botany
University of Coimbra
Coimbra, Portugal
Claire Damesin
Plant Ecophysiology
Paris-Sud University
Orsay, France
Alan Davison
School of Biology and Psychology:
Division of Biology
Newcastle University
Newcastle upon Tyne, England
Carlos M. Duarte
Mediterranean Institute for
Advanced Studies
Spanish Council for Scientific
Research
Blanes, Spain
Helena Freitas
Department of Botany
University of Coimbra
Coimbra, Portugal
John A. Gamon
Department of Biology and
Microbiology
California State University
Los Angeles, California
Francisco Pugnaire/Functional Plant Ecology 7488_C000 Final Proof page xvii 12.5.2007 2:00pm Compositor Name: JGanesan
xvii
Eric Garnier

Centre for Functional and Evolutionary
Ecology
CNRS
Montpellier, France
Jose
´
M. Go
´
mez
Department of Ecology
University of Granada
Granada, Spain
T.G. Allan Green
Department of Biological Sciences
Waikato University
Hamilton, New Zealand
Sarah E. Hobbie
Department of Ecology, Evolution,
and Behavior
University of Minnesota
St. Paul, Minnesota
Jose
´
A. Ho
´
dar
Terrestrial Ecology Group
Department of Ecology
University of Granada
Granada, Spain

William A. Hoffmann
Department of Plant Biology
North Carolina State University
Raleigh, North Carolina
Robert B. Jackson
Department of Biology
Duke University
Durham, North Carolina
Anna Jakobsson
Mediterranean Institute for
Advanced Studies
Esporles, Mallorca
Balearic Islands, Spain
Richard Joffre
Centre for Functional and Evolutionary
Ecology
CNRS
Montpellier, France
Ludger Kappen
Department of Botany
University of Kiel
Kiel, Germany
Kaoru Kitajima
Department of Botany
University of Florida
Gainesville, Florida
Hans de Kroon
Department of Experimental Plant Ecology
Institute of Water and Wetland Research
Radboud University

Nijmegen, The Netherlands
Esteban Manrique-Reol
Department of Agricultural and
Environmental Science
University of Newcastle
Newcastle upon Tyne, England
Ernesto Medina
Center of Ecology
Venezuelan Institute for Scientific
Investigations
Caracas, Venezuela
U
¨
lo Niinemets
Institute of Environment and
Agriculture
Estonian University of Life Sciences
Tartu, Estonia
Robert W. Pearcy
Division of Biological Sciences
University of California
Davis, California
William T. Pockman
Department of Biology
University of New Mexico
Albuquerque, New Mexico
Hendrik Poorter
Institute of Environmental Biology
Utrecht University
Utrecht, The Netherlands

Francisco Pugnaire/Functional Plant Ecology 7488_C000 Final Proof page xviii 12.5.2007 2:00pm Compositor Name: JGanesan
xviii Contributors
Francisco I. Pugnaire
Arid Zones Research Station
Spanish Council for Scientific Research
Almeria, Spain
Hong-Lie Qiu
Department of Geography and Urban
Analysis
California State University
Los Angeles, California
Tara K. Rajaniemi
Biology Department
University of Massachusetts
Dartmouth, Massachusetts
Serge Rambal
Centre for Functional and Evolutionary
Ecology
CNRS
Montpellier, France
Heather L. Reynolds
Department of Biology
Indiana University
Bloomington, Indiana
Susana Rodrı
´
guez-Echeverrı
´
a
Department of Botany

University of Coimbra
Coimbra, Portugal
Ronald J. Ryel
Department of Wildland Resources
and the Ecology Center
Utah State University
Logan, Utah
Arturo Sanchez-Azofeifa
Department of Earth and Atmospheric
Sciences
University of Alberta
Edmonton, Alberta, Canada
Leopoldo G. Sancho
Department Vegetal II
Complutense University
Madrid, Spain
Burkhard Schroeter
Botanical Institute
University of Kiel
Kiel, Germany
and
IPN – Leibniz Institute for Science
Education
University of Kiel
Kiel, Germany
Anna Traveset
Mediterranean Institute for Advanced
Studies
Esporles, Mallorca
Balearic Islands, Spain

Melvin T. Tyree
Aiken Forestry Sciences Laboratory
Burlington, Vermont
Fernando Valladares
Centre for Environmental Studies
Spanish Council for Scientific
Research
Madrid, Spain
Mark Westoby
Department of Biological Sciences
Macquarie University
Sydney, Australia
S. Joseph Wright
Smithsonian Tropical Research
Institute
Balboa, Republic of Panama
Regino Zamora
Department of Ecology
University of Granada
Granada, Spain
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Contributors xix
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1
Methods in Comparative
Functional Ecology
Carlos M. Duarte
CONTENTS
Development of Functional Plant Ecology 1
Screening, Broad-Scale Comparisons, and the Development of Functional Laws 3

References 5
DEVELOPMENT OF FUNCTIONAL PLANT ECOLOGY
The quest to describe the diversity of extant plants and the identification of the basic
mechanisms that allow them to occupy different environments have shifted scientists’ atten-
tion from ancient Greece to the present. This interest was prompted by two fundamental
aims: (1) a pressing need to understand the basic functions and growth requirements of plants
because they provide direct and indirect services to human kind and (2) the widespread belief
that the distribution of organisms was not random, for there was essential order in nature,
and that there ought to be a fundamental link between differences in the functions of these
organisms and their dominance in contrasting habitats. The notion that differences in plant
functions are essential components of their fitness, accounting for their relative dominance in
differential habitats, was, therefore, deeply rooted in the minds of early philosophers and,
later on, naturalists. While animal functions were relatively easy to embrace from a simple
parallel with our own basic functions, those of plants appeared more inaccessible to our
ancestors, and the concepts of ‘‘plant’’ and ‘‘plant functions’’ have unfolded through the
history of biology.
The examination of plant functions in modern science has largely followed a reduction-
istic path aimed at the explanation of plant functions in terms of the principles of physics and
chemistry (Salisbury and Ross 1992). This reductionistic path is linked to the parallel
transformation of traditional agricultural science into plant science and the technical develop-
ments needed to evolve from the examination of the coarser, integrative functions to those
occurring at the molecular level. While this reductionistic path has led us toward a thorough
catalog and understanding of plant functions, its limited usefulness to explain and predict the
distribution of plants in nature has been a source of frustration. This is largely because of the
multiple interactions that are expected to be involved in the responses of plants to a changing
environment (Chapin et al. 1987). Yet, the need to achieve this predictive power has now
transcended the academic arena to be a critical component of our ability to forecast the large-
scale changes expected from on-going climatic change. For instance, increased CO
2
concen-

trations are expected to affect the water and nutrient requirements of plants, but resource
availability is itself believed to be influenced by rising temperatures. Such feedback effects
cannot be appropriately predicted from knowledge of the controls that individual factors
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1
exert on specific functions. Moreover, the changes expected to occur from climate change are
likely to derive mostly from changes in vegetation and dominant plant types rather than from
altered physiological responses of extant plants to the new conditions (Betts et al. 1997).
Failure of plant physiology and plant science to provide reliable predictions of the
response of vegetation to changes in their environment likely derives from the hierarchical
nature of plants. The response of higher organizational levels is not predictable from the
dynamics of those at smaller scales, although these set constraints on the larger-scale responses
of hierarchical systems. Component functions do not exist in isolation, as the dominant
molecular approaches in modern plant physiology investigate them. Rather, these individual
functions are integrated within the plants, which can modulate the responses expected
from particular functions, leading to synergism, whether amplifying the responses through
multiplicative effects or maintaining homeostasis against external forcing.
Recognition of the limitations of modern physiology to provide the needed predictions at
the ecological scale led to the advent of plant ecophysiology, which tried to produce more
relevant knowledge by the introduction of larger plant components, such as plant organs
(instead of cells or organelles), as the units of analysis. Plant ecophysiology represented,
therefore, an effort toward approaching the relevant scale of organization, by examining
the functions of plant organs. Most often, however, practitioners of the discipline laid
somewhere between the molecular approaches dominant in plant physiology and the more
integrative approaches championed by plant physiological ecology. Because of the strong
roots in the tradition of plant physiology, the suite of plant functions addressed by plant
ecophysiology still targeted basic functions (e.g., photosynthesis, respiration, etc.) that can be
studied through chemical and physical laws (Salisbury and Ross 1992). As a consequence,
plant ecophysiology failed to consider more integrative plant functions, such as plant growth,
which do not have a single physiological basis, but which are possibly the most relevant

function for the prediction of plant performance in nature (cf. Chapter 3).
The efforts of plant ecophysiology proved, therefore, to be insufficient to achieve the
prediction of how plant function allows the prediction of plant distribution and changes in
plant abundance in a changing environment. Realization that the knowledge required to
effectively address this question would be best achieved through a more integrative approach
led to the advent of a new approach, hereafter referred to as ‘‘Functional Plant Ecology,’’
which is emerging as a coherent research program (cf. Duarte et al. 1995). Functional plant
ecology is centered on whole plants as the units of analysis, the responses of which to external
forcing are examined in nature or under field conditions. Functional plant ecology, therefore,
attempts to bypass the major uncertainties derived from the extrapolation of responses to
nature (tested in isolated plant organs maintained under carefully controlled laboratory
conditions) and to incorporate the integrated responses to multiple stresses displayed by
plants onto the research program.
Although centered in whole plants, functional plant ecology encompasses lower
and higher scales of organization, including studies at the organ or cellular level (e.g.,
Chapter 8), as well as the effect of changes in plant architecture or functions (e.g., Chapters
4 and 5), and the importance of life history traits (e.g., Chapters 15 and 16), interactions with
neighbors (e.g., Chapters 17 and 18), and those with other components of the ecosystem (e.g.,
Chapter 19). In fact, this research program is also based on a much broader conception of
plant functions than hitherto formulated. The plant functions that represent the core of
present efforts in functional plant ecology are those by which plants influence ecosystem
functions, particularly those that influence the services and products provided by ecosystems
(Costanza et al. 1997). Hence, studies at lower levels of organization are conducted with the
aim of being subsequently scaled up to the ecosystem level (e.g., Chapter 10).
Because of the emphasis on the prediction of the consequences of changes in vegetation
structure and distribution for the ecosystem, functional plant ecology strives to encompass
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2 Functional Plant Ecology
the broadest possible range of functional responses encountered within the biosphere.
Yet, the elucidation of the range of possible functional responses of plants is not possible

with the use of model organisms that characterize most of plant (and animal) physiology.
Functional plant ecology arises, therefore, as an essentially comparative science concerned
with the elucidation of the range of variations in functional properties among plants and the
search for patterns and functional laws accounting for this variation (Duarte et al. 1995).
While practitioners of functional plant ecology share the emphasis on the comparative
analysis of plant function, the approaches used to achieve these comparisons range broadly.
These differences rely largely on the breadth of the comparison and the description of the
subject organisms in the analysis. The implications of these choices have not, however, been
subject of explicit discussions despite their considerable epistemological implications and
their impact on the power of the approach.
SCREENING, BROAD-SCALE COMPARISONS, AND THE DEVELOPMENT
OF FUNCTIONAL LAWS
The success and the limitations of comparative functional plant ecology depend on the
choices of approach made, involving the aims and scope of the comparison, as well as the
methods to achieve them. The aims of the comparisons range widely, from the compilation of
a ‘‘functional taxonomy’’ of particular sets of species or floras to efforts to uncover patterns
of functional properties that may help formulate predictions or identify possible controlling
factors. Many available floras incorporate considerable knowledge, albeit rarely quantitative,
on the ecology of the species, particularly as to habitat requirements. An outstanding example
is the Biological Flora of the British Isles (cf. Journal of Ecology), which incorporates
some functional properties of the plants (e.g., Aksoy et al. 1998). The likely reason why
‘‘functional’’ floras are still few is the absence of standardized protocols to examine these
properties while ensuring comparability of the results obtained. A step toward solving this
bottleneck was provided by Hendry and Grime (1993), who described a series of protocols to
obtain estimates of selected basic functional traits of plants in a comparable manner. Unfor-
tunately, while exemplary, those protocols were specifically designed for use within the
screening program of the British flora conducted by those investigators (Grime et al. 1988),
rendering them of limited applicability in broader comparisons or comparisons of other
vegetation types.
The screening approach may, if pursued further, generate an encyclopedic catalog

of details on functional properties of different plants. Some ecologists may hold the hope
that, once completed, such catalogs will reveal by themselves a fundamental order in the
functional diversity of the plants investigated, conforming to a predictive sample similar to a
‘‘periodic table’’ of plant functional traits. While I do not dispute here that this goal may
be eventually achieved, the resources required to produce such catalogs are likely to be
overwhelming, since, by definition, such a screening procedure is of an exploratory nature,
where the search for pattern is made a posteriori. Provided the number of elements to be
screened and the potentially large number of traits to be tested, the cost-effectiveness of the
approach is likely to prove suboptimal. A screening approach to functional plant ecology is,
therefore, unlikely to improve our predictive power or to uncover basic patterns unless driven
by specific hypotheses. Moreover, a hypothesis-driven search for pattern is likely to be most
effective if based on a comparative approach, encompassing the broadest possible relevant
range of plants. It is not necessary to test every single plant species to generate and test such
general laws.
The comparisons attempted may differ greatly in scope, from comparisons of variability
within species to broad-scale comparisons encompassing the broadest possible range of
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Methods in Comparative Functional Ecology 3
phototrophic organisms, from the smallest unicells to trees (e.g., Agustı
´
et al. 1994, Nielsen
et al. 1996). Experience shows, however, that the patterns obtained at one level of analysis
may differ greatly from those observed at a broader level (Duarte 1990), without necessarily
involving a conflict (Reich 1993). The scope of the comparison depends on the question that
is posed. However, whenever possible, progress in comparative functional plant ecology
should evolve from the general to the particular, thereby evolving from comparisons at the
broadest possible scales to comparisons within species or closely related species. In doing so,
we shall first draw the overall patterns, which yield the functional laws that help identify the
constraints of possible functional responses in organisms.
The simplest possible comparison involves only two subjects, which are commonly

enunciated under the euphemism of ‘‘contrasting’’ plant types. Such simple comparisons
between one or a few subject plants are very common in the literature. These simple
comparisons are, however, deceiving, for they cannot possibly be conclusive as to the nature
of the differences or similarities identified. The implicit suggestion in these contrasts is that
the trait on which the contrast is based (e.g., stress resistance vs. stress tolerance) is the cause
underlying any observed differences in functional traits. This is fallacious and at odds with the
simplest principles of method in science. Hence, contrasts are unlikely to be an effective
approach to uncover regular patterns in plant function, since the degrees of freedom involved
are clearly insufficient to venture any strong inferences on the outcome of the comparison.
Broad-scale comparisons involving functional responses across widely different species
are, therefore, the approach of choice when the description of general laws is sought. The
formulation of the comparative analysis of plant functions at the broadest possible level has
been strongly advocated (Duarte et al. 1995), on the grounds that it will be most likely to
disclose the basic rules that govern functional differences among plants. Broad-scale com-
parisons are most effective when encompassing the most diverse range of plant types possible
(e.g., Agustı
´
et al. 1994, Niklas 1994). In addition, they are most powerful when the functional
properties are examined in concert with quantification of plant traits believed to influence the
functions examined, for comparisons based on qualitative or nominal plant traits cannot be
readily falsified and remain, therefore, unreliable tools for prediction. Hence, the develop-
ment of broad-scale comparisons requires that both the functional property examined and the
plant traits, which account for the differences in functional properties among the plants, are
to be tested and carefully selected.
Broad-scale comparisons must be driven by a sound hypothesis or questions. Yet, this
approach is of a statistical nature, often involving allometric relationships (e.g., Niklas 1994),
so that observation of robust patterns is no guaranty of underlying cause and effect relation-
ships, which must be tested experimentally. Nevertheless, the functional laws developed
through broad-scale comparative analysis may hold predictive power, irrespective of whether
they represent direct cause–effect relationships. This use requires, however, that the inde-

pendent, predictor variable be simpler than the functional trait examined, if the law is to have
practical application. Examples of such functional laws are many (e.g., Niklas 1994, Agustı
´
et al. 1994, Duarte et al. 1995, Enrı
´
quez et al. 1996, Nielsen et al. 1996) and have been
generally derived from the compilation of literature data and the use of plant cultures in
phytotrons or the use of the functional diversity found, for instance, in botanical gardens
(e.g., Nielsen et al. 1998). This choice of subject organisms is appropriate whenever the
emphasis is on the functional significance of intrinsic properties. However, the effect of
environment conditions can hardly be approached in this manner, and functional ecologists
must transport the research to the field, which is the ultimate framework of relevance for this
research program.
The comparative approach is also a powerful tool to examine the effect of environmental
conditions in situ. Gradient analysis, where functional responses are examined along a
clearly defined environmental gradient, has proven a powerful approach to investigate the
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4 Functional Plant Ecology