Exploitation of Environmental Heterogeneity by Plants. Ecophysiological Processes Above- and Below-ground

433 Pages·1994·7.34 MB·English

by  Jacques Roy

Physiological Ecology
A Series of Monographs, Texts, and Treatises
Series Editor
Harold A. Mooney
Stanford University, Stanford, California
Editorial Board
Fakhri Bazzaz F. Stuart Chapin James R. Ehleringer
Robert W. Pearcy Martyn M. Caldwell E.-D. Schulze
T. T. KOZLOWSKI (Ed.). Growth and Development of Trees,
Volumes I and II, 1971
D. HILLEL (Ed.). Soil and Water: Physical Principles and Processes,
1971
V. B. YOUNGER and C. M. McKELL (Eds.). The Biology and
Utilization of Grasses, 1972
J. B. MUDD and T. T. KOZLOWSKI (Eds.). Responses of Plants to
Air Pollution, 1975
R. DAUBENMIRE (Ed.). Plant Geography, 1978
J. LEVITT (Ed.). Responses of Plants to Environmental Stresses, 2nd
Edition.
Volume I: Chilling, Freezing, and High Temperature Stresses, 1980
Volume II: Water, Radiation, Salt, and Other Stresses, 1980
J. A. LARSEN (Ed.). The Boreal Ecosystem, 1980
S. A. GAUTHREAUX, JR. (Ed.). Animal Migration, Orientation, and
Navigation, 1981
F.J. VERNBERG and W. B. VERNBERG (Eds.). Functional
Adaptations of Marine Organisms, 1981
R. D. DURBIN (Ed.). Toxins in Plant Disease, 1981
C. P. LYMAN, J. S. WILLIS, A. MALAN, and L. C. H. WANG (Eds.).
Hibernation and Torpor in Mammals and Birds, 1982
T. T. KOZLOWSKI (Ed.). Flooding and Plant Growth, 1984
E. L. RICE (Ed.). Allelopathy, Second Edition, 1984
M. L. CODY (Ed.). Habitat Selection in Birds, 1985
R.J. HAYNES, K. C. CAMERON, K. M. GOH, and R. R.
SHERLOCK (Eds.). Mineral Nitrogen in the Plant-Soil System, 1986
T. T. KOZLOWSKI, P.J. KRAMER, and S. G. PALLARDY (Eds.).
The Physiological Ecology of Woody Plants, 1991
H. A. MOONEY, W. E. WINNER, and E. J. PELL (Eds.). Response of
Plants to Multiple Stresses, 1991
A complete list of titles in this series appears at the end of this volume.
Exploitation of
Environmental
Heterogeneity
by Plants
Ecophysiological Processes
Above- and Belowground
Edited by
Martyn M. Caldwell
Department of Range Science
and the Ecology Center
Utah State University
Logan, Utah
Robert W. Pearcy
Department of Botany
University of California, Davis
Davis, California
Academic Press
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Copyright © 1994 by ACADEMIC PRESS, INC.
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Library of Congress Cataloging-in-Publication Data
Exploitation of environmental heterogeneity by plants :
ecophysiological process above- and below ground / edited by Martyn
M. Caldwell, Robert W. Pearcy.
p. cm. — (Physiological ecology)
Includes bibliographical references and index.
ISBN 0-12-155070-2
1. Plant ecophysiology. I. Caldwell Martyn M. Date
II. Pearcy, R. W. (Rober W.), Date III. Series.
QK905.E96 1994
581.5-dc20 93-14291
CIP
PRINTED IN THE UNITED STATES OF AMERICA
94 95 96 97 98 99 BC 9 8 7 6 5 4 3 2 1
Contributors
Numbers in parentheses indicate the pages on which the authors' contributions begin.
Dennis Baldocchi (21), Atmospheric Turbulence and Diffusion Divi­
sion, Air Resources Laboratory, National Oceanic and Atmospheric
Administration, Oak Ridge, Tennessee 37831
Carlos L. Ballaré (73), Department de Ecologia, Facultad de Agronomia,
Universidad de Buenos Aires, 1417 Buenos Aires, Argentina
F. A. Bazzaz (349), Department of Organismic and Evolutionary Biology,
Harvard University, Cambridge, Massachusetts 02138
Graham Bell (391), Department of Biology, McGill University, Montreal,
Quebec, Canada H3A 1B1
Martyn M. Caldwell (325), Department of Range Science and the Ecol­
ogy Center, Utah State University, Logan, Utah 84322
Robin L. Chazdon (175), Department of Ecology and Evolutionary Biol­
ogy, University of Connecticut, Storrs, Connecticut 06269
Serge Collineau (21), Atmospheric Turbulence and Diffusion Division,
Air Resources Laboratory, National Oceanic and Atmospheric Admin­
istration, Oak Ridge, Tennessee 37831
A. H. Fitter (305), Department of Biology, University of York, York YOl
5DD, England
J. P. Grime (1), NERC Unit of Comparative Plant Ecology, Department
of Animal and Plant Sciences, The University of Sheffield, Sheffield
S10 2TN, England
Katherine L. Gross (237), W. K. Kellogg Biological Station, and Depart­
ments of Botany and Zoology, Michigan State University, Hickory
Corners, Michigan 49060
Louis J. Gross (175), Department of Mathematics, University of Tennes­
see, Knoxville, Tennessee 37996
Manfred Kuppers (111), Institut fur Botanik, Technische Hochschule
Darmstadt, D-64287 Darmstadt, Germany
Martin J. Lechowicz (391), Department of Biology, McGill University,
Montreal, Quebec, Canada H3A 1B1
Keith A. Mott (175), Department of Biology, Utah State University,
Logan, Utah 84322
xiii
XIV Contributors
Park S. Nobel (285), Department of Biology, and Laboratory of Biomedi­
cal and Environmental Sciences, University of California, Los Angeles,
California 90024
Alma Orozco-Segovia (209), Centro de Ecologia, UNAM, Ciudad Uni-
versitaria 04510, Mexico
Robert W. Pearcy (145, 175), Department of Botany, University of Cali­
fornia, Davis, Davis, California 95616
G. Philip Robertson (237), W. K. Kellogg Biological Station, and Depart­
ment of Crop and Soil Sciences, Michigan State University, Hickory
Corners, Michigan 49060
Daniel A. Sims (145), Department of Botany, University of California,
Davis, Davis, California 95616
John M. Stark (255), Department of Biology, Utah State University,
Logan, Utah 84322
Carlos Vazquez-Yanes (209), Centro de Ecologia, UNAM, Ciudad Uni-
versitaria 04510, Mexico
P. M. Wayne (349), Department of Organismic and Evolutionary Biol­
ogy, Harvard University, Cambridge, Massachusetts 02138
Preface
Considerable interest in the role played by temporal and spatial hetero­
geneity in ecological organization and biodiversity has emerged in the
past decade. Pertinent aspects of heterogeneity are involved in the scaling
of patterns and operational organization among different levels of time
and space. Yet, the functional responses of organisms to heterogeneity in
different environments has received much less attention. This book ex­
amines a synthesis of plant response to temporal and spatial heterogene­
ity, the exploitation of resources from pulses and patches by plants, and
their competition with neighbors in the face of this variability. Approxi­
mately half of this volume is directed to the aboveground environment,
addressing the nature of canopy patchiness and light transitions—the
mechanisms by which plants perceive, acclimate and exploit this patchi­
ness. The remainder explores analogous questions of the belowground
environment, heterogeneity in the soil environment and how root sys­
tems adjust and acquire nutrients and water in the context of soil tempo­
ral and spatial variability.
While the importance of scale in addressing temporal and spatial het­
erogeneity has long been recognized in ecology, the quantification of
pattern and scale of heterogeneity is still an evolving field. Even the
definition of gaps, sunflecks and fertile soil microsites, though seemingly
straightforward, is more complicated upon further inspection. Geosta-
tistical approaches to assessing the scale and structure of variability are
gaining acceptance in ecological study. Scale-dependent autocorrelation,
rather than continuous autocorrelation, may emerge as a common phe­
nomenon and be linked with plausible causal agents. Applications of
wavelet theory in quantifying light variability may eventually experience
the same adoption as geostatistics belowground. Although physical mea­
sures of heterogeneity receive the most attention and probably will con­
tinue to be emphasized, using the physiological responses of plants to
determine meaningful scales of variability is clearly pertinent (e.g., At
what level are light transitions simply integrated by plants and at what
level are they perceived as significant?). At longer and larger scales, the
growth and reproductive success of individual plants or local populations
is arguably the most meaningful barometer of heterogeneity in a particu-
xv
XVI Preface
lar case study. However, comparative studies across different environ­
ments will still likely depend on physical characterizations.
Plant plasticity is clearly a central theme in plant exploitation of re­
sources in the face of environmental heterogeneity. Altered biomass
allocation of shoots toward canopy gaps or by root proliferation in fertile
soil patches are obvious and well known. However, architectural plasticity
may be more important than biomass allocation in root exploitation of
fertile patches. Plastic adjustment of physiological processes of both indi­
vidual leaves and roots occurs. However, physiological plasticity is usually
closely coupled with growth and development, both above- and below­
ground. While the time scale of biochemical regulatory events, such as
induction of the carboxylating enzyme, may be on the scale of minutes,
acclimatizing physiological changes of both leaves and roots appear to
operate on the scale of days and involve developmental alterations.
Costs of acclimation or foraging are, of course, very pertinent. These
include investments in new structure and in new metabolic capacities that
are well understood at the leaf and whole-plant level, but poorly for
belowground organs. There are clearly linkages between investments in
different parts of the plant in order to maintain functional balance—
more assimilatory capacity of the shoots demands more support in water
and nutrient supply.
Many counterintuitive findings are emerging: Precision in allocating
new root mass preferentially into nutrient-rich patches may be a property
not of the dominant, fast growing plants, but of the subordinate commu­
nity members; slow growing plants may be more adept in capitalizing on
nutrient pulses of short duration than fast growing species; sun-
acclimated leaves do not reap a great return on investment in high light;
high respiration rates in leaves does not necessarily indicate high mainte­
nance costs; root shrinkage during pulses of water deprivation may be an
important regulator of water transport between plant and soil. When
water does move from roots to soil, there can be benefits to the entire root
system in acquiring both water and nutrients.
An effective, timely response to opportunities presented by heteroge­
neous environments requires perception of the opportunities and of
present or impending competition for these resources by neighbors.
Seeds have evolved many responses to environmental cues, including
germination after exposure to millisecond light flashes, and the ability to
differentiate between passing light flecks during the day and opportuni­
ties presented by gap formation. Plants can detect the presence of neigh­
bors long before appreciable shading develops.
Finally, although environmental heterogeneity involves a sizeable ele­
ment of stochasticity, evolutionary molding of plasticity is most likely
driven by this heterogeneity. Yet, little is known about this evo-
Preface XVI i
lution, especially at the genetic level. While the importance of environ­
mental heterogeneity is widely appreciated in modern ecology, the
processes and mechanisms by which plants cope and exploit resources,
and how these mechanisms evolve, remain a pertinent challenge in physi­
ological ecology.
MARTYN M. CALDWELL
ROBERT W. PEARCY
The Role of Plasticity
in Exploiting
Environmental Heterogeneity
J. P. Grime
In recent years, theories of the functioning and evolution of vascular
plants, such as the resource-ratio hypothesis (Huston and Smith, 1987;
Tilman, 1988), have placed heavy emphasis on the relative abundance
of resources above and below ground and trade-offs in the allocation of
captured resources between roots and shoots.
This chapter reviews the results of experimental studies of plant re­
sponses to resource heterogeneity conducted over the period 1958 to the
present. It is concluded that the resource-ratio hypothesis underestimates
the interdependence of roots and shoots and, in particular, does not
sufficiently allow for the expenditure of assimilate necessary to allow the
extension of roots from the localized zones of depletion that are an
inevitable consequence of the rapid rates of mineral nutrient in-flow
achieved by plants of productive habitats. It is suggested that in fast-
growing species exploiting fertile soil, the swift incorporation of carbon
and mineral nutrients into plant tissue and the relative constancy of plant
chemical composition will dictate strong covariance between root and
shoot function.
In the slow-growing plants of unproductive habitats, the relationship
between root and shoot activity may relax considerably; here resource
heterogeneity in time rather than space is often critical and capture of
resources both above and below ground often depends on long-lived
tissues that remain viable under extreme conditions. These tissues exploit
pulses of resource enrichment that may be of insufficient duration to
reward those foraging mechanisms that rely on growth responses.
Evidence is presented of a trade-off between the scale and precision
Copyright © 1994 by Academic Press, Inc.
Exploitation of Environmental Heterogeneity by Plants 1 All rights of reproduction in any form reserved.
2 J. P. Grime
of resource foraging by leaf canopies and root systems. It is suggested
that this trade-off is relevant to theories of species coexistence in plant
communities. Future studies of this trade-off must take account of phylo-
genetic constraints and will need to recognize the modifying effect of
moisture stress on the development and evolution of root morphology.
I. Introduction
In the majority of animals and in most fungi, bacteria, algae, and bryo-
phytes, all essential resources are absorbed through the same surfaces.
This contrasts strongly with the trophic design of vascular land plants,
in most of which photons and carbon dioxide are captured by leaves
whereas mineral nutrients and water are intercepted by roots. Such
specialization in function above and below ground has prompted the
hypothesis that the most severe challenges of environmental heterogene­
ity to the fitness of vascular plants growing in natural environments will
arise from the competing claims of roots and shoots on the synthetic
capacity of the plant. Hence it has been argued (Newman, 1973, 1983;
Iwasa and Roughgarden, 1984; Huston and Smith, 1987; Tilman, 1988,
1989) that, on both an evolutionary time scale and within the life span
of an individual phenotype, trade-offs in allocation of captured resources
between shoot and root will be of paramount importance. Theories that
recognize a pivotal role for root-shoot partitioning in the evolution of
flowering plants have become known collectively as the "resource-ratio
hypothesis" and they have been formally expressed in models of func­
tional types (Huston and Smith, 1987; Tilman, 1988) in which plants
with relatively large shoots (assumed to be superior competitors for light)
are distinguished from those with relatively large roots (assumed to be
strong competitors for below-ground resources).
In this chapter various sources of evidence are assembled to support
an alternative interpretation of the role of plasticity in exploiting environ­
mental heterogeneity. Here, in marked contrast to Huston and Smith
(1987) and Tilman (1988), recognition is given to (1) differences between
habitats with respect to spatial and temporal patchiness in resource sup­
ply, (2) the capacity of fast-growing plants in productive habitats to
generate local resource gradients both above and below ground, (3) limits
to root-shoot trade-offs imposed by the physiological interdependence
of photosynthesis and mineral nutrient capture and the constancy of
plant chemical composition across the plant kingdom, (4) covariance in
the resource foraging characteristics of leaf canopies and root systems
of annual and perennial plants of productive habitats, and (5) genetic
differences between dominant and subordinate components of plant
communities in the scale and precision of resource interception.