Plant Physiological Ecology

Hans Lambers • Rafael S. Oliveira

Plant PhysiologicalEcologyThird Edition

Hans LambersSchool of Biological SciencesUniversity of Western AustraliaCrawley, WA, Australia

Rafael S. OliveiraInstitute of BiologyUniversity of CampinasCampinas, Brazil

ISBN 978-3-030-29638-4 ISBN 978-3-030-29639-1 (eBook)https://doi.org/10.1007/978-3-030-29639-1

# Springer Nature Switzerland AG 1998, 2008, 2019This work is subject to copyright. All rights are reserved by the Publisher, whether the whole orpart of the material is concerned, specifically the rights of translation, reprinting, reuse ofillustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way,and transmission or information storage and retrieval, electronic adaptation, computer software, orby similar or dissimilar methodology now known or hereafter developed.The use of general descriptive names, registered names, trademarks, service marks, etc. in thispublication does not imply, even in the absence of a specific statement, that such names areexempt from the relevant protective laws and regulations and therefore free for general use.The publisher, the authors, and the editors are safe to assume that the advice and information inthis book are believed to be true and accurate at the date of publication. Neither the publisher northe authors or the editors give a warranty, expressed or implied, with respect to the materialcontained herein or for any errors or omissions that may have been made. The publisher remainsneutral with regard to jurisdictional claims in published maps and institutional affiliations.

Cover Illustration: Photo credit: Hazel Dempster.

This Springer imprint is published by the registered company Springer Nature Switzerland AG.The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

Foreword Third Edition

How do and will ‘plants cope’ in the face of global environmental change?Temperatures, carbon dioxide, and other trace gases are rising at an unprece-dented rate. Urbanization, with its expanding and destructive human footprint,continues to sweep across and impact all ecosystems. Climatic extremes, likehurricane- or typhoon-associated floods, deep frosts and even deeper snows,and the most extreme droughts ever recorded are now part of every day, everyyear, and in every place. These are, Earth’s ‘new normals’. And as alarming asthese facts are, the field of plant physiological ecology (P2E) thrives, becauseit is a field of science that is and will provide some of the most criticalevidence and fundamental understanding about how the diversity of plantadaptations, at the center of its investigations, will allow plants to handle theconditions of the Anthropocene. Such understanding will also reveal how wecan best use the information gathered from basic ecophysiological research tohelp stakeholders – humanity – ‘change course’ and take new roads to craftingsolutions for preserving biodiversity and the planet that harbors it writ large.

Investigations focused on the physiological adaptations plants have cometo possess over their long evolutionary history can teach us not only about thenature of the adaptation-environment nexus, but also reveal what to expectwhen plants are challenged by the conditions they now face on Earth that areoutside of their previous (evolutionary) experiences. Since the last addition ofthis book, the aforementioned issues have become the centerpiece aroundwhich modern plant ecophysiological investigations often hinge. The dataplant physiological ecologists gather on how plants function and cope withenvironmental challenges also serve to inform other types of plant research atlevels of biological organization, both below at the cellular and molecularscales and above at the population, community, and ecosystem levels. Plantecophysiological information also continues to be integral to the study ofbiological evolution, as it helps to reveal how adaptations are identified andhow they serve the plants that possess them. For me, I have long advocated forthe central role that plant physiological ecology has, can, and should play inour fundamental understanding of plant adaptations (e.g., the field of physio-logical ecology is essentially studying the ‘basis’ of plant adaptations to theirbiotic and abiotic environments). But plant ecophysiology is also likely toplay a greater and greater role in designing best practices for mitigatinghumanity’s assault on the organisms that sustain us and Earth – plants.

v

As the third edition of this textbook emerges, the students and scientistswho will build upon the information it contains have a new responsibility, anew weight, and new opportunities to add their voices in new ways. As acommunity, plant ecophysiologists also have a frontier of new prospects tonot just build upon our fundamental knowledge, but to also innovate andsurprise ‘science’ and the academy. New technological advances in micro-scopic imaging, in quantifying fluxes into and out of plants (at scales from thesub-cellular to the globe), in characterizing with much more rigor plantinteractions with their microbiome, and in modeling form-functionrelationships and how they inform plant trait evolution and ecosystemfunctions are firmly part of the ‘new toolkit’ of modern plant ecophysiology.Healthy debate on best (new) methods and best practices still marshals on andthis is good – good for the credibility of the information we as a communityare providing to the plant sciences and for those who are adding their talentsand ideas on how we can deepen our understanding of plant functions.Without debate and opinions, we cease to have a productive dialogue, andour science becomes ‘comfortable’, even complacent and risks becoming lessrelevant. But plant physiological ecology is very relevant in the many wayshighlighted above, and may more ways.

Students continue to ponder the age-old questions of – what will I do in mylife ahead, how can I make a difference with my profession or vocation, andhow can I, we, make our planet a better place? Such questions move to answer– through knowledge, understanding, a belief in evidence, a passion for‘place’, and then participating in doing plant physiological ecology (P2E).P2E is a hub around which the plant world and the Earth revolves – onwards.

Berkeley, CA, USA Todd DawsonMay 2019

vi Foreword Third Edition

Acknowledgments

Numerous people have contributed to the text and illustrations in this book.Most importantly, Terry Chapin and Thijs Pons provided significant input intochapters that appeared in earlier editions and formed the basis of revised textsin this third edition. Others commented on sections and chapters, providedphotographic material, or made electronic files of graphs and illustrationsavailable. In addition to those who wrote book reviews or sent us specificcomments on the first and second edition of Plant Physiological Ecology, wewish to thank the following colleagues, in alphabetical order, for their valu-able input into the third edition: Felipe Albornoz, Paulo Bittencourt, DevBritto, Brendan Choat, Tim Colmer, Elaine Davison, Wenli Ding, CleitonEller, Patrick Hayes, Bethany Huot, Hamlyn Jones, Ulrike Mathesius, IanMaxMøller, Francis Nge, Ko Noguchi, Ole Pedersen, Luciano Pereira, KennyPng, Rafael Ribeiro, Megan Ryan, Lucas Silva, Fernando Silveira, ChristianaStaudinger, Ichiro Terashima, François Teste, Robert Turgeon, ErikVeneklaas, and Rafael Villar.

The authors

vii

Contents

1 Introduction: History, Assumptions, and Approaches . . . . . . 11.1 What Is Ecophysiology? . . . . . . . . . . . . . . . . . . . . . . . . . 11.2 The Roots of Ecophysiology . . . . . . . . . . . . . . . . . . . . . . 11.3 Physiological Ecology and the Distribution

of Organisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21.4 Time Scale of Plant Response to Environment . . . . . . . . . 51.5 Conceptual and Experimental Approaches . . . . . . . . . . . . 71.6 New Directions in Ecophysiology . . . . . . . . . . . . . . . . . . 81.7 The Structure of the Book . . . . . . . . . . . . . . . . . . . . . . . 8References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

2 Photosynthesis, Respiration, and Long-Distance Transport:Photosynthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 112.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 112.2 General Characteristics of the Photosynthetic Apparatus . . . 11

2.2.1 The ‘Light’ and ‘Dark’ Reactions ofPhotosynthesis . . . . . . . . . . . . . . . . . . . . . . . . . 11

2.2.2 Supply and Demand of CO2 in thePhotosynthetic Process . . . . . . . . . . . . . . . . . . . 18

2.3 Response of Photosynthesis to Light . . . . . . . . . . . . . . . . 282.3.1 The Light Climate Under a Leaf Canopy . . . . . . 282.3.2 Physiological, Biochemical, and Anatomical

Differences Between Sun and Shade Leaves . . . . 292.3.3 Effects of Excess Irradiance . . . . . . . . . . . . . . . . 392.3.4 Responses to Variable Irradiance . . . . . . . . . . . . 47

2.4 Partitioning of the Products of Photosynthesis andRegulation by Feedback . . . . . . . . . . . . . . . . . . . . . . . . . 512.4.1 Partitioning Within the Cell . . . . . . . . . . . . . . . . 512.4.2 Short-Term Regulation of Photosynthetic Rate

by Feedback . . . . . . . . . . . . . . . . . . . . . . . . . . . 522.4.3 Sugar-induced Repression of Genes Encoding

Calvin-Benson-Cycle Enzymes . . . . . . . . . . . . . 562.4.4 Ecological Impacts Mediated by Source-Sink

Interactions . . . . . . . . . . . . . . . . . . . . . . . . . . . . 562.4.5 Petiole and Stem Photosynthesis . . . . . . . . . . . . 59

ix

2.5 Responses to Availability of Water . . . . . . . . . . . . . . . . . 592.5.1 Regulation of Stomatal Opening . . . . . . . . . . . . . 592.5.2 The An–Cc Curve as Affected by Water Stress . . . 612.5.3 Carbon-Isotope Fractionation in Relation to

Water-Use Efficiency . . . . . . . . . . . . . . . . . . . . 612.5.4 Other Sources of Variation in Carbon-Isotope

Ratios in C3 Plants . . . . . . . . . . . . . . . . . . . . . . 642.6 Effects of Soil Nutrient Supply on Photosynthesis . . . . . . 65

2.6.1 The Photosynthesis-Nitrogen Relationship . . . . . 652.6.2 Interactions of Nitrogen, Light, and Water . . . . . 662.6.3 Photosynthesis, Nitrogen, and Leaf Life Span . . . 67

2.7 Photosynthesis and Leaf Temperature: Effects andAdaptations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 672.7.1 Effects of High Temperatures on Photosynthesis . . . 672.7.2 Effects of Low Temperatures on Photosynthesis . . . 70

2.8 Effects of Air Pollutants on Photosynthesis . . . . . . . . . . . 712.9 C4 Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72

2.9.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . 722.9.2 Biochemical and Anatomical Aspects . . . . . . . . . 732.9.3 Intercellular and Intracellular Transport

of Metabolites of the C4 Pathway . . . . . . . . . . . . 762.9.4 Photosynthetic Efficiency and Performance

at High and Low Temperatures . . . . . . . . . . . . . 762.9.5 C3–C4 Intermediates . . . . . . . . . . . . . . . . . . . . . 802.9.6 Evolution and Distribution of C4 Species . . . . . . 822.9.7 Carbon-Isotope Composition of C4 Species . . . . . 842.9.8 Growth Rates of C4 Species . . . . . . . . . . . . . . . . 84

2.10 CAM Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 852.10.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . 852.10.2 Physiological, Biochemical, and Anatomical

Aspects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 862.10.3 Water-Use Efficiency . . . . . . . . . . . . . . . . . . . . 912.10.4 Incomplete and Facultative CAM Plants . . . . . . . 912.10.5 Distribution and Habitat of CAM Species . . . . . . 932.10.6 Carbon-Isotope Composition of CAM Species . . . 93

2.11 Specialized Mechanisms Associated with PhotosyntheticCarbon Acquisition in Aquatic Plants . . . . . . . . . . . . . . . 932.11.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . 932.11.2 The CO2 Supply in Water . . . . . . . . . . . . . . . . . 942.11.3 The Use of Bicarbonate by Aquatic

Macrophytes . . . . . . . . . . . . . . . . . . . . . . . . . . . 952.11.4 The Use of CO2 from the Sediment . . . . . . . . . . 962.11.5 Crassulacean Acid Metabolism (CAM)

in Aquatic Plants . . . . . . . . . . . . . . . . . . . . . . . . 972.11.6 Carbon-Isotope Composition of Aquatic Plants . . . 972.11.7 The Role of Aquatic Plants in Carbonate

Sedimentation . . . . . . . . . . . . . . . . . . . . . . . . . . 99

x Contents

2.12 Effects of the Rising CO2 Concentration in theAtmosphere . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1002.12.1 Acclimation of Photosynthesis to Elevated CO2

Concentrations . . . . . . . . . . . . . . . . . . . . . . . . . 1022.12.2 Effects of Elevated CO2 on Transpiration -

Differential Effects on C3, C4,and CAM Plants . . . . . . . . . . . . . . . . . . . . . . . . 103

2.13 Summary: What Can We Gain from Basic Principlesand Rates of Single-Leaf Photosynthesis? . . . . . . . . . . . . 103

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 104

3 Photosynthesis, Respiration, and Long-Distance Transport:Respiration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1153.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1153.2 General Characteristics of the Respiratory System . . . . . . 115

3.2.1 The Respiratory Quotient . . . . . . . . . . . . . . . . . . 1153.2.2 Glycolysis, the Pentose Phosphate Pathway,

and the Tricarboxylic (TCA) Cycle . . . . . . . . . . 1173.2.3 Mitochondrial Metabolism . . . . . . . . . . . . . . . . . 1183.2.4 A Summary of the Major Points of Control

of Plant Respiration . . . . . . . . . . . . . . . . . . . . . . 1213.2.5 ATP Production in Isolated Mitochondria

and in Vivo . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1233.2.6 Regulation of Electron Transport via the

Cytochrome and the Alternative Paths . . . . . . . . 1253.3 The Ecophysiological Function of the Alternative Path . . . 128

3.3.1 Heat Production . . . . . . . . . . . . . . . . . . . . . . . . 1283.3.2 Can We Really Measure the Activity of the

Alternative Path? . . . . . . . . . . . . . . . . . . . . . . . . 1303.3.3 The Alternative Path as an Energy Overflow . . . . 1333.3.4 NADH Oxidation in the Presence of a High

Energy Charge . . . . . . . . . . . . . . . . . . . . . . . . . 1333.3.5 NADH Oxidation to Oxidize Excess Redox

Equivalents from the Chloroplast . . . . . . . . . . . . 1353.3.6 Continuation of Respiration When the Activity

of the Cytochrome Path Is Restricted . . . . . . . . . 1363.3.7 A Summary of the Various Ecophysiological

Roles of the Alternative Oxidase . . . . . . . . . . . . 1363.4 Environmental Effects on Respiratory Processes . . . . . . . 137

3.4.1 Flooded, Hypoxic, and Anoxic Soils . . . . . . . . . 1373.4.2 Salinity and Water Stress . . . . . . . . . . . . . . . . . . 1403.4.3 Nutrient Supply . . . . . . . . . . . . . . . . . . . . . . . . 1413.4.4 Irradiance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1423.4.5 Temperature . . . . . . . . . . . . . . . . . . . . . . . . . . . 1463.4.6 Low pH and High Aluminum Concentrations . . . 1493.4.7 Partial Pressures of CO2 . . . . . . . . . . . . . . . . . . 1503.4.8 Effects of Nematodes and Plant Pathogens . . . . . 151

Contents xi

3.4.9 Leaf Dark Respiration as Affected byPhotosynthesis . . . . . . . . . . . . . . . . . . . . . . . . . 152

3.5 The Role of Respiration in Plant Carbon Balance . . . . . . . 1533.5.1 Carbon Balance . . . . . . . . . . . . . . . . . . . . . . . . 1533.5.2 Respiration Associated with Growth,

Maintenance, and Ion Uptake . . . . . . . . . . . . . . . 1553.6 Plant Respiration: Why Should It Concern Us

from an Ecological Point of View? . . . . . . . . . . . . . . . . . 164References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 165

4 Photosynthesis, Respiration, and Long-Distance Transport:Long Distance Transport of Assimilates . . . . . . . . . . . . . . . . . 1734.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1734.2 Major Transport Compounds in the Phloem: Why Not

Glucose? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1734.3 Phloem Structure and Function . . . . . . . . . . . . . . . . . . . . 176

4.3.1 Symplastic and Apoplastic Transport . . . . . . . . . 1764.3.2 Minor Vein Anatomy . . . . . . . . . . . . . . . . . . . . 1774.3.3 Phloem-Loading Mechanisms . . . . . . . . . . . . . . 178

4.4 Evolution and Ecology of Phloem Loading Mechanisms . . . 1804.5 Phloem Unloading . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1814.6 The Transport Problems of Climbing Plants . . . . . . . . . . . 1844.7 Phloem Transport: Where to Move from Here? . . . . . . . . 185References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 185

5 Plant Water Relations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1875.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 187

5.1.1 The Role of Water in Plant Functioning . . . . . . . 1875.1.2 Transpiration as an Inevitable Consequence

of Photosynthesis . . . . . . . . . . . . . . . . . . . . . . . 1895.2 Water Potential . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1895.3 Water Availability in Soil . . . . . . . . . . . . . . . . . . . . . . . . 193

5.3.1 The Field Capacity of Different Soils . . . . . . . . . 1945.3.2 Water Movement Toward the Roots . . . . . . . . . . 1955.3.3 Rooting Profiles as Dependent on Soil Moisture

Content . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1965.3.4 Roots Sense Moisture Gradients and Grow

Toward Moist Patches . . . . . . . . . . . . . . . . . . . . 2025.4 Water Relations of Cells . . . . . . . . . . . . . . . . . . . . . . . . . 202

5.4.1 Osmotic Adjustment . . . . . . . . . . . . . . . . . . . . . 2035.4.2 Cell-Wall Elasticity . . . . . . . . . . . . . . . . . . . . . . 2035.4.3 Osmotic and Elastic Adjustment as Alternative

Strategies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2065.4.4 Evolutionary Aspects . . . . . . . . . . . . . . . . . . . . 207

5.5 Water Movement Through Plants . . . . . . . . . . . . . . . . . . 2075.5.1 The Soil-Plant-Atmosphere Continuum . . . . . . . . 2075.5.2 Water in Roots . . . . . . . . . . . . . . . . . . . . . . . . . 2095.5.3 Water in Stems . . . . . . . . . . . . . . . . . . . . . . . . . 215

xii Contents

5.5.4 Water in Leaves and Water Loss from Leaves . . . 2305.5.5 Aquatic Angiosperms . . . . . . . . . . . . . . . . . . . . 242

5.6 Water-Use Efficiency . . . . . . . . . . . . . . . . . . . . . . . . . . . 2425.6.1 Water-Use Efficiency and Carbon-Isotope

Discrimination . . . . . . . . . . . . . . . . . . . . . . . . . 2425.6.2 Leaf Traits That Affect Leaf Temperature

and Leaf Water Loss . . . . . . . . . . . . . . . . . . . . . 2435.7 Water Availability and Growth . . . . . . . . . . . . . . . . . . . . 2445.8 Adaptations to Drought . . . . . . . . . . . . . . . . . . . . . . . . . 248

5.8.1 Desiccation-Avoidance: Annuals and Drought-Deciduous Species . . . . . . . . . . . . . . . . . . . . . . 248

5.8.2 Dessication-Tolerance: Evergreen Shrubs . . . . . . 2495.8.3 ‘Resurrection Plants’ . . . . . . . . . . . . . . . . . . . . . 249

5.9 Winter Water Relations and Freezing Tolerance . . . . . . . . 2525.10 Salt Tolerance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2525.11 Final Remarks: The Message That Transpires . . . . . . . . . 253References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 254

6 Plant Energy Budgets: The Plant’s Energy Balance . . . . . . . . 2656.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2656.2 Energy Inputs and Outputs . . . . . . . . . . . . . . . . . . . . . . . 265

6.2.1 A Short Overview of a Leaf’s Energy Balance . . . 2656.2.2 Shortwave Solar Radiation . . . . . . . . . . . . . . . . . 2666.2.3 Longwave Terrestrial Radiation . . . . . . . . . . . . . 2696.2.4 Convective Heat Transfer . . . . . . . . . . . . . . . . . 2716.2.5 Evaporative Energy Exchange . . . . . . . . . . . . . . 2736.2.6 Metabolic Heat Generation . . . . . . . . . . . . . . . . 276

6.3 Modeling the Effect of Components of the EnergyBalance on Leaf Temperature . . . . . . . . . . . . . . . . . . . . . 276

6.4 A Global Perspective of Hot and Cool Topics . . . . . . . . . 277References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 277

7 Plant Energy Budgets: Effects of Radiationand Temperature . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2797.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2797.2 Radiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 279

7.2.1 Effects of Excess Irradiance . . . . . . . . . . . . . . . . 2797.2.2 Effects of Ultraviolet Radiation . . . . . . . . . . . . . 279

7.3 Effects of Extreme Temperatures . . . . . . . . . . . . . . . . . . 2837.3.1 How Do Plants Avoid Damage by Free Radicals

at Low Temperature? . . . . . . . . . . . . . . . . . . . . . 2837.3.2 Heat-Shock Proteins . . . . . . . . . . . . . . . . . . . . . 2847.3.3 Are Isoprene and Monoterpene Emissions an

Adaptation to High Temperatures? . . . . . . . . . . . 2847.3.4 Chilling Injury and Chilling Tolerance . . . . . . . . 2857.3.5 Carbohydrates and Proteins Conferring Frost

Tolerance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 285

Contents xiii

7.4 Global Change and Future Crops . . . . . . . . . . . . . . . . . . 288References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 288

8 Scaling-Up Gas Exchange and Energy Balance fromthe Leaf to the Canopy Level . . . . . . . . . . . . . . . . . . . . . . . . . 2918.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2918.2 Canopy Water Loss . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2948.3 Canopy CO2 Fluxes . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2968.4 Canopy Water-Use Efficiency . . . . . . . . . . . . . . . . . . . . . 2978.5 Canopy Effects on Microclimate: A Case Study . . . . . . . . 2988.6 Aiming for a Higher Level . . . . . . . . . . . . . . . . . . . . . . . 298References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 299

9 Mineral Nutrition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3019.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3019.2 Acquisition of Nutrients . . . . . . . . . . . . . . . . . . . . . . . . . 302

9.2.1 Nutrients in the Soil . . . . . . . . . . . . . . . . . . . . . 3029.2.2 Root Traits That Determine Nutrient

Acquisition . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3099.2.3 Sensitivity Analysis of Parameters Involved

in Pi Acquisition . . . . . . . . . . . . . . . . . . . . . . . . 3319.3 Nutrient Acquisition from ‘Toxic’ or ‘Extreme’ Soils . . . . 331

9.3.1 Acid Soils . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3339.3.2 Calcium-Rich Soils . . . . . . . . . . . . . . . . . . . . . . 3389.3.3 Soils with High Levels of Metals . . . . . . . . . . . . 3419.3.4 Saline Soils: An Ever-Increasing Problem in

Agriculture . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3499.3.5 Flooded Soils . . . . . . . . . . . . . . . . . . . . . . . . . . 354

9.4 Plant Nutrient-Use Efficiency . . . . . . . . . . . . . . . . . . . . . 3559.4.1 Variation in Nutrient Concentration . . . . . . . . . . 3559.4.2 Nutrient Productivity and Mean Residence

Time . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3619.4.3 Nutrient Loss from Plants . . . . . . . . . . . . . . . . . 3639.4.4 Ecosystem Nutrient-Use Efficiency . . . . . . . . . . . 367

9.5 Mineral Nutrition: A Vast Array of Adaptationsand Acclimations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 369

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 370

10 Growth and Allocation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38510.1 Introduction: What Is Growth? . . . . . . . . . . . . . . . . . . . . 38510.2 Growth of Whole Plants and Individual Organs . . . . . . . . 385

10.2.1 Growth of Whole Plants . . . . . . . . . . . . . . . . . . 38610.2.2 Growth of Cells . . . . . . . . . . . . . . . . . . . . . . . . 387

10.3 The Physiological Basis of Variation in RGR—PlantsGrown with Free Access to Nutrients . . . . . . . . . . . . . . . 39410.3.1 SLA Is a Major Factor Associated with

Variation in RGR . . . . . . . . . . . . . . . . . . . . . . . 39410.3.2 Leaf Thickness and Leaf Mass Density . . . . . . . . 39610.3.3 Anatomical and Chemical Differences

Associated with Leaf Mass Density . . . . . . . . . . 396

xiv Contents

10.3.4 Net Assimilation Rate, Photosynthesis, andRespiration . . . . . . . . . . . . . . . . . . . . . . . . . . . . 398

10.3.5 RGR and the Rate of Leaf Elongationand Leaf Appearance . . . . . . . . . . . . . . . . . . . . . 398

10.3.6 RGR and Activities per Unit Mass . . . . . . . . . . . 39910.3.7 RGR and Suites of Plant Traits . . . . . . . . . . . . . . 399

10.4 Allocation to Storage . . . . . . . . . . . . . . . . . . . . . . . . . . . 40110.4.1 The Concept of Storage . . . . . . . . . . . . . . . . . . . 40110.4.2 Chemical Forms of Stores . . . . . . . . . . . . . . . . . 40210.4.3 Storage and Remobilization in Annuals . . . . . . . 40310.4.4 The Storage Strategy of Biennials . . . . . . . . . . . 40310.4.5 Storage in Perennials . . . . . . . . . . . . . . . . . . . . . 40410.4.6 Costs of Growth and Storage: Optimization . . . . 405

10.5 Environmental Influences . . . . . . . . . . . . . . . . . . . . . . . . 40610.5.1 Growth as Affected by Irradiance . . . . . . . . . . . . 40710.5.2 Growth as Affected by Temperature . . . . . . . . . . 41310.5.3 Growth as Affected by Soil Water Potential

and Salinity . . . . . . . . . . . . . . . . . . . . . . . . . . . 41710.5.4 Growth at a Limiting Nutrient Supply . . . . . . . . . 41910.5.5 Plant Growth as Affected by Soil Compaction . . . 42410.5.6 Growth as Affected by Soil Flooding . . . . . . . . . 42810.5.7 Growth as Affected by Submergence . . . . . . . . . 43010.5.8 Growth as Affected by Touch and Wind . . . . . . . 43210.5.9 Growth as Affected by Elevated Atmospheric

CO2 Concentrations . . . . . . . . . . . . . . . . . . . . . 43410.6 Adaptations Associated with Inherent Variation

in Growth Rate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43510.6.1 Fast-Growing and Slow-Growing Species . . . . . . 43510.6.2 Growth of Inherently Fast- and Slow-Growing

Species under Resource-Limited Conditions . . . . 43610.6.3 Are There Ecological Advantages Associated

with a High or Low RGR? . . . . . . . . . . . . . . . . . 43710.7 Growth and Allocation: The Messages About Plant

Messages . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 440References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 441

11 Life Cycles: Environmental Influences and Adaptations . . . . . 45111.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 45111.2 Seed Dormancy, Quiescence, and Germination . . . . . . . . 451

11.2.1 Hard Seed Coats . . . . . . . . . . . . . . . . . . . . . . . . 45311.2.2 Germination Inhibitors in the Seed . . . . . . . . . . . 45411.2.3 Effects of Nitrate . . . . . . . . . . . . . . . . . . . . . . . . 45511.2.4 Other External Chemical Signals . . . . . . . . . . . . 45611.2.5 Effects of Light . . . . . . . . . . . . . . . . . . . . . . . . . 45711.2.6 Effects of Temperature . . . . . . . . . . . . . . . . . . . 45911.2.7 Physiological Aspects of Dormancy . . . . . . . . . . 46211.2.8 Summary of Ecological Aspects of Seed

Germination and Dormancy . . . . . . . . . . . . . . . . 462

Contents xv

11.3 Developmental Phases . . . . . . . . . . . . . . . . . . . . . . . . . . 46311.3.1 Seedling Phase . . . . . . . . . . . . . . . . . . . . . . . . . 46311.3.2 Juvenile Phase . . . . . . . . . . . . . . . . . . . . . . . . . 46511.3.3 Reproductive Phase . . . . . . . . . . . . . . . . . . . . . . 46911.3.4 Fruiting . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47711.3.5 Senescence . . . . . . . . . . . . . . . . . . . . . . . . . . . . 478

11.4 Seed Dispersal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47911.4.1 Dispersal Mechanisms . . . . . . . . . . . . . . . . . . . . 47911.4.2 Life-History Correlates . . . . . . . . . . . . . . . . . . . 480

11.5 The Message to Disperse: Perception, Transduction,and Response . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 481

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 481

12 Biotic Influences: Symbiotic Associations . . . . . . . . . . . . . . . . 48712.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 48712.2 Mycorrhizas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 487

12.2.1 Mycorrhizal Structures: Are They Beneficialfor Plant Growth? . . . . . . . . . . . . . . . . . . . . . . . 488

12.2.2 Nonmycorrhizal Species and Their Interactionswith Mycorrhizal Species . . . . . . . . . . . . . . . . . . 497

12.2.3 Phosphate Relations . . . . . . . . . . . . . . . . . . . . . 49712.2.4 Effects on Nitrogen Nutrition and Water

Acquisition . . . . . . . . . . . . . . . . . . . . . . . . . . . . 50312.2.5 Role of Mycorrhizas in Defense . . . . . . . . . . . . . 50612.2.6 Carbon Costs of the Mycorrhizal Symbiosis . . . . 50612.2.7 Agricultural and Ecological Perspectives . . . . . . . 507

12.3 Associations with Nitrogen-Fixing Organisms . . . . . . . . . 51012.3.1 Symbiotic N2 Fixation Is Restricted to a Fairly

Limited Number of Plant Species . . . . . . . . . . . . 51112.3.2 Host–Guest Specificity in the

Legume–Rhizobium Symbiosis . . . . . . . . . . . . . 51312.3.3 The Infection Process in the

Legume–Rhizobium Association . . . . . . . . . . . . 51312.3.4 Nitrogenase Activity and Synthesis of Organic

Nitrogen . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 51912.3.5 Carbon and Energy Metabolism of the

Nodules . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 52012.3.6 Quantification of N2 Fixation In Situ . . . . . . . . . 52112.3.7 Ecological Aspects of the Symbiotic Association

with N2-Fixing Microorganisms That Do NotInvolve Specialized Structures . . . . . . . . . . . . . . 525

12.3.8 Carbon Costs of the Legume-RhizobiumSymbiosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 526

12.3.9 Suppression of the Legume-RhizobiumSymbiosis at Low pH and in the Presenceof a Large Supply of Combined Nitrogen . . . . . . 526

12.4 Endosymbionts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 52812.5 Plant Life Among Microsymbionts . . . . . . . . . . . . . . . . . 530References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 530

xvi Contents

13 Biotic Influences: Ecological Biochemistry: Allelopathy andDefense Against Herbivores . . . . . . . . . . . . . . . . . . . . . . . . . . 54113.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 54113.2 Allelopathy (Interference Competition) . . . . . . . . . . . . . . 54113.3 Chemical Defense Mechanisms . . . . . . . . . . . . . . . . . . . . 545

13.3.1 Defense Against Herbivores . . . . . . . . . . . . . . . . 54613.3.2 Qualitative and Quantitative Defense

Compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . 54913.3.3 The Arms Race of Plants and Herbivores . . . . . . 55113.3.4 How Do Plants Avoid Being Killed by Their

Own Poisons? . . . . . . . . . . . . . . . . . . . . . . . . . . 55313.3.5 Secondary Metabolites for Medicines and Crop

Protection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 55613.4 Environmental Effects on the Production of Secondary

Plant Metabolites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 56013.4.1 Abiotic and Biotic Factors . . . . . . . . . . . . . . . . . 56013.4.2 Induced Defense and Communication Between

Neighboring Plants . . . . . . . . . . . . . . . . . . . . . . 56113.4.3 Communication Between Plants and Their

Bodyguards . . . . . . . . . . . . . . . . . . . . . . . . . . . 56813.5 The Costs of Chemical Defense . . . . . . . . . . . . . . . . . . . 570

13.5.1 Diversion of Resources from Primary Growth . . . 57013.5.2 Strategies of Predators . . . . . . . . . . . . . . . . . . . . 570

13.6 Detoxification of Xenobiotics by Plants:Phytoremediation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 573

13.7 Secondary Chemicals and Messages That Emergefrom This Chapter . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 575

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 575

14 Biotic Influences: Effects of Microbial Pathogens . . . . . . . . . . 58314.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58314.2 Constitutive Antimicrobial Defense Compounds . . . . . . . 58314.3 The Plant’s Response to Attack by Microorganisms . . . . . 58714.4 Cross-Talk Between Induced Systemic Resistance

and Defense Against Herbivores . . . . . . . . . . . . . . . . . . . 59114.5 Messages from One Organism to Another . . . . . . . . . . . . 593References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 593

15 Biotic Influences: Parasitic Associations . . . . . . . . . . . . . . . . . 59715.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59715.2 Growth and Development . . . . . . . . . . . . . . . . . . . . . . . . 599

15.2.1 Seed Germination . . . . . . . . . . . . . . . . . . . . . . . 59915.2.2 Haustoria Formation . . . . . . . . . . . . . . . . . . . . . 60215.2.3 Effects of the Parasite on Host Development . . . . 605

15.3 Water Relations and Mineral Nutrition . . . . . . . . . . . . . . 60615.4 Carbon Relations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 608

Contents xvii

15.5 What Can We Extract from This Chapter? . . . . . . . . . . . . 610References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 610

16 Biotic Influences: Interactions Among Plants . . . . . . . . . . . . . 61516.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61516.2 Theories of Competitive Mechanisms . . . . . . . . . . . . . . . 62016.3 How Do Plants Perceive the Presence of Neighbors? . . . . 62116.4 Relationship of Plant Traits to Competitive Ability . . . . . . 624

16.4.1 Growth Rate and Tissue Turnover . . . . . . . . . . . 62416.4.2 Allocation Pattern, Growth Form,

and Tissue Mass Density . . . . . . . . . . . . . . . . . . 62716.4.3 Plasticity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 628

16.5 Traits Associated with Competition for SpecificResources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63116.5.1 Nutrients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63116.5.2 Water . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63216.5.3 Light . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63416.5.4 Carbon Dioxide . . . . . . . . . . . . . . . . . . . . . . . . 634

16.6 Positive Interactions among Plants . . . . . . . . . . . . . . . . . 63516.6.1 Physical Benefits . . . . . . . . . . . . . . . . . . . . . . . . 63616.6.2 Nutritional Benefits . . . . . . . . . . . . . . . . . . . . . . 63616.6.3 Allelochemical Benefits . . . . . . . . . . . . . . . . . . . 637

16.7 Plant–Microbial Symbioses . . . . . . . . . . . . . . . . . . . . . . 63716.8 Succession and Long-Term Ecosystem Development . . . . 64016.9 What Do We Gain from This Chapter? . . . . . . . . . . . . . . 642References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 643

17 Biotic Influences: Carnivory . . . . . . . . . . . . . . . . . . . . . . . . . . 64917.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64917.2 Structures Associated with the Catching of the Prey

and Subsequent Withdrawal of Nutrients from the Prey . . . 64917.3 Some Case Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 654

17.3.1 Dionaea muscipula . . . . . . . . . . . . . . . . . . . . . . 65417.3.2 The Suction Traps of Utricularia . . . . . . . . . . . . 65417.3.3 The Tentacles of Drosera . . . . . . . . . . . . . . . . . 65717.3.4 Pitchers of Nepenthes . . . . . . . . . . . . . . . . . . . . 65817.3.5 Passive Traps of Philcoxia . . . . . . . . . . . . . . . . . 660

17.4 The Message to Catch . . . . . . . . . . . . . . . . . . . . . . . . . . 660References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 662

18 Role in Ecosystem and Global Processes: Decomposition . . . . 66518.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 66518.2 Litter Quality and Decomposition Rate . . . . . . . . . . . . . . 666

18.2.1 Species Effects on Litter Quality: Links withEcological Strategy . . . . . . . . . . . . . . . . . . . . . . 666

18.2.2 Environmental Effects on Decomposition . . . . . . 669

xviii Contents

18.3 The Link Between Decomposition Rate and NutrientSupply . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 66918.3.1 The Process of Nutrient Release . . . . . . . . . . . . . 66918.3.2 Effects of Litter Quality on Mineralization . . . . . 67018.3.3 Root Exudation and Rhizosphere Effects . . . . . . 672

18.4 The End-Product of Decomposition . . . . . . . . . . . . . . . . . 673References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 674

19 Role in Ecosystem and Global Processes: EcophysiologicalControls . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 67719.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 67719.2 Ecosystem Biomass and Production . . . . . . . . . . . . . . . . 677

19.2.1 Scaling from Plants to Ecosystems . . . . . . . . . . . 67719.2.2 Physiological Basis of Productivity . . . . . . . . . . 67819.2.3 Disturbance and Succession . . . . . . . . . . . . . . . . 68019.2.4 Photosynthesis and Absorbed Radiation . . . . . . . 68119.2.5 Net Carbon Balance of Ecosystems . . . . . . . . . . 68319.2.6 The Global Carbon Cycle . . . . . . . . . . . . . . . . . 685

19.3 Nutrient Cycling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 68719.3.1 Vegetation Controls Over Nutrient Uptake

and Loss . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 68719.3.2 Vegetation Controls Over Mineralization . . . . . . 688

19.4 Ecosystem Energy Exchange and the HydrologicalCycle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 68819.4.1 Vegetation Effects on Energy Exchange . . . . . . . 68819.4.2 Vegetation Effects on the Hydrological Cycle . . . 691

19.5 Moving to a Higher Level: Scaling from Physiologyto the Globe . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 694

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 695

Glossary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 699

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 721

Contents xix

About the Authors

Hans Lambers is an Emeritus Professor of Plant Biology at the University ofWestern Australia, in Perth, Australia, and a Distinguished Professor at ChinaAgricultural University, in Beijing, China. He did his undergraduate degree atthe University of Groningen, the Netherlands, followed by a PhD project oneffects of hypoxia on flooding-sensitive and -tolerant Senecio species at thesame institution. From 1979 to 1982, he worked as a postdoc at the Universityof Western Australia, Melbourne University, and the Australian NationalUniversity in Australia, working on respiration and nitrogen metabolism.After a postdoc at his alma mater, he became Professor of Ecophysiology atUtrecht University, the Netherlands, in 1985, where he focused on plantrespiration and the physiological basis of variation in growth rate amongherbaceous plants. In 1998, he moved to the University of WesternAustralia, where he focused on plant mineral nutrition, especially in legumecrops and native species occurring on severely phosphorus-impoverished soilsin a global biodiversity hotspot in southwestern Australia and southeasternBrazil. He has been Editor-in-Chief of the journal Plant and Soil since 1992and featured on the first ISI list of highly cited authors in the field of animaland plant sciences (since 2002), and on several other ISI lists more recently.He was elected Fellow of the Royal Netherlands Academy of Arts andSciences in 2003, and Fellow of the Australian Academy of Science in2012. He received Honorary Degrees from three Universities and from theAcademy of Sciences in China.

xxi

Rafael S. Oliveira is a Professor of Ecology at the University of Campinas(UNICAMP), Brazil. He did his undergraduate degree at the University ofBrasília, Brazil, followed by a PhD on water relations of Amazonian andsavanna trees at the University of California, Berkeley, USA. He worked as apostdoc from 2005 to 2007 at the National Institute of Space Research and theUniversity of São Paulo in Brazil to improve the representation of keyvegetation processes on climate models, followed by a project on theecohydrology of tropical montane cloud forests. In 2007, he became Professorat UNICAMP. His research focuses on plant hydraulics, vegetation-climatefeedbacks, and mineral nutrition of tropical plants. He is an Associate Editorfor the journal Functional Ecology and Section Editor for Plant and Soil.

xxii About the Authors

Abbreviations

a radius of a root (ar) or root plus root hairs (ae)A rate of CO2 assimilation; also total root surfaceAn net rate of CO2 assimilationAf foliage areaAmax light-saturated rate of net CO2 assimilation at ambient Ca

As sapwood areaABA abscisic acidADP adenosine diphosphateAM arbuscular mycorrhizaAMP adenosine monophosphateAPAR absorbed photosynthetically active radiationATP adenosine triphosphateb individual plant biomass; buffer power of the soilB stand biomasscs concentration of the soluteC nutrient concentration in solution; also convective heat transferC3 photosynthetic pathway in which the first product of CO2 fixation

is a 3-carbon intermediateC4 photosynthetic pathway in which the first product of CO2 fixation

is a 4-carbon intermediateCa atmospheric CO2 concentrationCc CO2 concentration in the chloroplastCi intercellular CO2 concentrationCli initial nutrient concentrationCmin solution concentration at which uptake is zeroC:N carbon:nitrogen ratioCAM crassulacean acid metabolismCC carbon concentrationCE carbohydrate equivalentchl chlorophyllCPF carbon dioxide production valued plant density; also leaf dimensionD diffusivity of soil waterDe diffusion coefficient of ion in soilDHAP dihydroxyacetone phosphateDM dry massDNA deoxyribonucleic acid

xxiii

e water vapor pressure in the leaf (ei; or el in section 2.5 of theplant’s energy balance) or atmosphere (ea); also emissivity of asurface

E transpiration ratef tortuosityF rate of nutrient supply to the root surface; also chlorophyll fluo-

rescence, minimal fluorescence (F0), maximum (Fm), in a pulse ofsaturating light (Fm’), variable (Fv)

FAD(H2) flavin adenine dinucleotide (reduced form)FM fresh massFR far-redg diffusive conductance for CO2 (gc) and water vapor (gw); bound-

ary layer conductance (ga); mesophyll conductance (gm); stomatalconductance (gs); boundary layer conductance for heat transport(gah)

GA gibberellic acidGE glucose equivalentGOGAT glutamine 2-oxoglutarate aminotransferaseHCH hydroxycyclohexenoneHIR high-irradiance responseI irradiance, above (Io) or beneath (I ) a canopy; irradiance

absorbed; also nutrient inflowImax maximum rate of nutrient inflowIAA indoleacetic acidIRs short-wave infrared radiationJ rate of photosynthetic electron flowJmax maximum rate of photosynthetic electron flow measured at

saturating I and Ca

Jv water flowk rate of root elongation; extinction coefficient for lightK carrying capacity (e.g., K species)kcat catalytic constant of an enzymeKi inhibitor concentration giving half-maximum inhibitionKm substrate concentration at half Vmax (or Imax)l leaf area indexL rooting density; also latent heat of evaporation; also length of

xylem elementLp root hydraulic conductanceLAI leaf area indexLAR leaf area ratioLFR low-fluence responseLHC light-harvesting complexLMA leaf mass per unit areaLMR leaf mass ratioLR long-wave infrared radiation that is incident (LRin), reflected

(LRr), emitted (LRem), absorbed (SRabs), or net incoming (LRnet);also leaf respiration on an area (LRa) and mass (LRm) basis

xxiv Abbreviations

mRNA messenger ribonucleic acidmiRNA micro ribonucleic acidM energy dissipated by metabolic processesME malic enzymeMRT mean residence timeNw mol fraction, that is, the number of moles of water divided by the

total number of molesNAD(P) nicotinamide adenine dinucleotide(phosphate) (in its oxidized

form)NAD(P)H nicotinamide adenine dinucleotide(phosphate) (in its reduced

form)NAR net assimilation rateNDVI normalized difference vegetation indexNEP net ecosystem productionNIR near-infrared reflectance; net rate of ion uptakeNMR nuclear magnetic resonanceNP nitrogen productivity, or nutrient productivityNPP net primary productionNPQ nonphotochemical quenchingNUE nitrogen-use efficiency, or nutrient-use efficiencyp vapor pressurepo vapor pressure of air above pure waterP atmospheric pressure; also turgor pressurePfr far-red-absorbing configuration of phytochromePi inorganic phosphatePr red-absorbing configuration of phytochromePAR photosynthetically active radiationPC phytochelatinsPEP phosphoenolpyruvatePEPC phosphoenolpyruvate carboxylasePEPCK phosphoenolpyruvate carboxykinasepH hydrogen ion activity; negative logarithm of the H+ concentrationPGA phosphoglyceratepmf proton-motive forcePNC plant nitrogen concentrationPNUE photosynthetic nitrogen-use efficiencyPQ photosynthetic quotient; also plastoquinonePR pathogenesis-related proteinPS photosystemPV0 amount of product produced per gram of substrateqN quenching of chlorophyll fluorescence due to nonphotochemical

processesqP photochemical quenching of chlorophyll fluorescenceQ ubiquinone (in mitochondria), in reduced state (Qr¼ ubiquinol) or

total quantity (Qt); also quinone (in chloroplast)Q10 temperature coefficientQA primary electron acceptor in photosynthesis

Abbreviations xxv

r diffusive resistance, for CO2 (rc), for water vapor (rw), boundarylayer resistance (ra), stomatal resistance (rs), mesophyll resistance(rm); also radial distance from the root axis; also respiration; alsogrowth rate (in volume) in the Lockhart equation; also propor-tional root elongation; also intrinsic rate of population increase(e.g., r species)

ri spacing between rootsro root diameterR redR radius of a xylem element; also universal gas constantRa molar abundance ratio of 13C/12C in the atmosphereRd dark respirationRday dark respiration during photosynthesisRe ecosystem respirationRp whole-plant respiration; also molar abundance ratio of 13C/12C in

plantsRh heterotrophic respirationR� minimal resource level utilized by a speciesRGR relative growth rateRH relative humidity of the airRMR root mass ratioRNA ribonucleic acidRQ respiratory quotientRR rate of root respirationRuBP ribulose-1,5-bisphosphateRubisco ribulose-1,5-bisphosphate carboxylase/oxygenaseRWC relative water contentS nutrient uptake by rootsSc/o specificity of carboxylation relative to oxygenation by RubiscoSHAM salicylichydroxamic acidSLA specific leaf areaSMR stem mass ratioSR short-wave solar radiation that is incident (SRin), reflected (SRr),

transmitted (SRtr), absorbed (SRabs), used in photosynthesis(SRA), emitted in fluorescence (SRFL), or net incoming (SRnet);also rate of stem respiration

SRL specific root lengtht� time constanttRNA transfer ribonucleic acidT temperatureTL leaf temperatureTCA tricarboxylic acidTR total radiation that is absorbed (TRabs) or net incoming (TRnet)u wind speedUV ultravioletV volume

xxvi Abbreviations

Vc rate of carboxylationVo rate of oxygenationVcmax maximum rate of carboxylationVw

o molar volume of waterVIS visible reflectanceVLFR very low fluence responseVmax substrate-saturated enzyme activityVPD vapor pressure deficitw mole fraction of water vapor in the leaf (wi) or atmosphere (wa)WUE water-use efficiencyY yield threshold (in the Lockhart equation)γ surface tensionΓ CO2-compensation pointΓ� CO2-compensation point in the absence of dark respirationδ boundary layer thickness; also isotopic contentΔ isotopic discriminationΔT temperature differenceε elastic modulus; also emissivityη viscosity constantθ curvature of the irradiance response curve; also volumetric mois-

ture content (mean value, θ’, or at the root surface, θa)λ energy required for transpirationμw chemical potential of waterμwo chemical potential of pure water under standard conditionsσ Stefan-Boltzmann constantϕ quantum yield (of photosynthesis); also yield coefficient (in the

Lockhart equation); also leakage of CO2 from the bundle sheath tothe mesophyll; also relative yield of de-excitation processes

Ψ water potentialΨair water potential of the airΨm matric potentialΨp pressure potential; hydrostatic pressureΨπ osmotic potential

Abbreviations xxvii