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Biologic Markers
of Air-Pollution Stress
l
and Damage in Forests
Committee on Biologic Markers of
Air-Pollution Damage in Trees
Board on Environmental Studies and Toxicology
Commission on Life Sciences
National Research Council
NATIONAL ACADEMY PRESS
Washington, D.C. 1989
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NATIONAL ACADEMY PRESS 2101 Constitution Avenue, NW Washington, DC 20418
NOTICE: The project that is the subject of this report was approved by the Governing Board of the National Research
Council, whose members are drawn from the councils of the National Academy of Sciences, the National Academy
of Engineering, and the Institute of Medicine. The members of the committee responsible for the report were chosen
for their special competences and with regard for appropriate balance. - -
This report has been reviewed by a group other than the authors according to procedures approved by a Report
Review Committee consisting of members of the National Academy of Sciences, the National Academy of Engineering,
and the Institute of Medicine.
The NationalAcademy of Sciences is a private, nonprofit, self-perpetuating society of distinguished scholars engaged
in scientific and engineering research, dedicated to the furtherance of science and technology and to their use for
the generalwelfare. Upon the authority of the charter granted to it by the Congress in 1863, the academy has a mandate
that requires it to advise the federal government of scientific and technical matters. Dr. Frank Press is president of
the National Academy of Sciences.
The National Academy of Engineering was established in 1964, under the charter of the National Academy of Sciences,
as a parallel organization of outstanding engineers. It is autonomous in its administration and in the selection of its
members, sharing with the National Academy of Sciences the responsibility for advising the federal government. The
National Academy of Engineering also sponsors engineering programs aimed at meeting national needs, encourages
education and research, and recognizes the superior achievements of engineers. Dr. Robert M. White is president
of the National Academy of Engineering.
The Institute of Medicine was established in 1970 by the National Academy of Sciences to secure the services of
eminent members of appropriate professions in the examination of policy matters pertaining to the health of the public.
The Institute acts under the responsibility given to the National Academy of Sciences by its congressional charter to
be an adviser to the federal government and, upon its own initiative, to identify issues of medical care, research, and
education. Dr. Samuel O. Thier is president of the Institute of Medicine.
The National Research Council was organized by the National Academy of Sciences in 1916 to associate the broad
community of science and technology with the Academy purposes of furthering knowledge and advising the federal
government. Functioning in accordance with general policies determined by the Academy, the Council has become
the principal operating agency of both the National Academy of Sciences and the National Academy of Engineering
in providing services to the government, the public, and the scientific and engineering communities. The Council
is administered jointly by both Academies and the Institute of Medicine. Dr. Frank Press and Dr. Robert M. White
are chairman and vice chairman, respectively, of the National Research Council.
The project was supported by the Environmental Protection Agency through cooperative agreement No. CR-
814248 01.
Library of Confess Number 89~2584
ISBN 0-309-04078-7
Printed in the United States of America
Cover photograph by Y. Yee, USDA Forest Service
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Committee on Biologic Markers
of Air-PoDution Damage in Trees
George M. Woodwell, Chairman, Woods Hole Research Center, Massachusetts
Edward R. Cook, Tree Ring Research Laboratory, Palisades, New York
Ellis B. Cowling, North Carolina State University, Raleigh
Arthur H. Johnson, University of Pennsylvania, Philadelphia
Thomas W. Kimmerer, University of Kentucky, Lexington
Pamela A. Matson, NASA/Ames Research Center, Moffitt Field, California
Samuel S. McLaughlin, Oak Ridge National Laboratory, Tennessee
Dudley J. Raynal, State University of New York, Syracuse
Wayne T. Swank, Coweeta Hydrologic Laboratory, Otto, North Carolina
Richard H. Waring, Oregon State University, Corvallis
William E. Winner, Oregon State University, Corvallis
James N. Woodman, North Carolina State University, Raleigh
Staff
David Policansky, Program Officer
Robert Smythe, Senior Staff Officer
Dave Johnston, Senior Staff Officer
Norman Grossblatt, Editor
Sylvia Tognetti, Research Assistant
Bernidean Williams, Information Specialist
Melanie Knight, Project Assistant
Leah Gales, Project Assistant
Sandi Fitzpatrick, Project Assistant
· · ~
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Board on Environmental Studies
-and Toxicology
Gilbert S. Omenn, Chairman, University of Washington, Seattle, Washington
Frederick R. Anderson, Washington School of Law, American University,
Washington, D.C.
John Bailar, McGill University School of Medicine, Montreal, Quebec
David Bates, University of British Columbia Health Science Center Hospital,
Vancouver, British Columbia
Joanna Burger, Nelson Laboratory, Rutgers University, Piscataway, New Jersey
Richard A. Conway, Union Carbide Corporation, South Charleston, West Virginia
William E. Cooper, Michigan State University, East Lansing, Michigan
Sheldon K. Friedlander, University of California, Los Angeles, California
Bernard Goldstein, UMDNJ-Robert Wood Johnson Medical School, Piscataway, New Jersey
Donald Mattison, National Center for Toxicological Research and University of
Arkansas for Medical Sciences, Little Rock, Arkansas
Duncan T. Patten, Arizona State University, Tempe, Arizona
Emil Pfitzer, Hoffmann-La Roche, Inc., Nutley, New Jersey
William H. Rodgers, University of Washington, Seattle, Washington
F. Sherwood Rowland, University of California, Irvine, California
Liane B. Russell, Oak Ridge National Laboratory
Milton Russell, Oak Ridge National Laboratory
Ellen K. Silbergeld, Environmental Defense Fund, Washington, D.C.
I. Glenn Sipes, University of Arizona, Tuscon, Arizona
Bruce M. Alberts, Ex Officio, University of California, San Francisco
Staff
Devra L. Davis, Director
James J. Reisa, Associate Director
Karen L. Hulebak, Exposure Assessment and Risk Reduction Program Director
David J. Policansky, Natural Resources and Applied Ecology Program Director
Richard D. Thomas, Human Toxicology and Risk Assessment Program Director
Lee R. Paulson, Manager, Toxicology Information Center
1V
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Commission on Life Sciences
Bruce M. Alberts, Chairman, University of California, San Francisco
Perry L. Adkisson, Texas A & M University, College Station
Francisco J. Ayala, University of California, Irvine
J. Michael Bishop, University of California Medical Center, San Francisco
Freeman J. Dyson, Princeton University, New Jersey
Nina V. Fedoroff, Carnegie Institution of Washington, Baltimore
Ralph W.F. Hardy, Cornell University, Ithaca
Richard J. Havel, University of California, San Francisco
Leroy E. Hood, California Institute of Technology, Pasadena
Donald F. Hornig, Harvard School of Public Health, Boston
Ernest G. Jaworski, Monsanto Company, St. Louis
Simon A. Levin, Cornell University, Ithaca
Harold A. Mooney, Stanford University, California
Steven P. Pakes, University of Texas, Dallas
Joseph E. Rall, National Institutes of Health, Bethesda
Richard D. Remington, University of Iowa
Paul G. Risser, University of New Mexico, Albuquerque
Richard B. Setlow, Brookhaven National Laboratory, Upton, New York
Torsten N. Wiesel, Rockefeller University, New York
Staff
John E. Burris, Executive Director
v
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Preface
There is not much question about the sensitivity of plants to air pollution, nor
is there doubt that air pollution is affecting forests and agriculture in Europe, North
America, Brazil, and elsewhere. The effects on forests are well known--they follow
patterns of impoverishment long recognized as the result of chronic disturbance.
Depending on the severity of the disturbance, the results are reduced growth of plants,
morbidity of trees, shifts in species, and ultimately, replacement of forests by
shrubland, grassland, or barren land that supports little or no vegetation. including
agriculture. Once the process starts, it
lost from
Once the process
plants and soils; nutrient ratios
and, as the vegetation changes, seed sources are lost as well.
_ _ _ 7 C~
can be difficult to reverse. Nutrients are
change; the character of the soils changes;
Experience is rich, and the causes of damage are known; and so are the cures. But
the cures seem expensive; they require specific action aimed at specific pollutants.
The costs of cures are well focused and great, while the damage is diffuse and its
increments seem small. The familiar cry is for better resolution of the relationships
between cause and effect before investing in a cure that might be only marginally
effective. Meanwhile, the damage accumulates and forests move inexorably down the scale
of impoverishment.
The difficulties in addressing the effects of air pollution are made worse by
the fact that effects of many types of disturbances are similar and that the responses
of plants are responses to general stress and are not easily used to diagnose specific
insults. Stress has many causes and collateral effects; such as diseases and pests that
become important when plants are otherwise weakened. Sorting out cause and effect has
frustrated pathologists and ecologists for years.
In a new effort to address this classical challenge that touches sensitive
economic interests and equally sensitive nerves among scientists, the - ~
Protection Agency sought help from the National Research Council to
recent progress in science might be opening new doors that would lead
diagnoses and narrow the issues. The Committee on Biologic Markers
Damage in Trees borrowed from experience in diagnosing
specific criteria to diagnosis the effects of air pollution
Environmental
review whether
to more specific
of Air-Pollutant
human disease to search for
A on trees and forests. The
committee sought the aid of a group of distinguished scholars selected for their recent
technical contributions to this difficult topic. This group met with the committee in
· .
V11
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Little Switzerland, North Carolina, to explore the potential of new approaches. This
book is their answer: progress lags the need, but progress is accumulating. There will
be, however, no simple diagnosis. Diagnosis will be a "most probable cause" derived from
many lines of evidence, each gathered over time and used with other evidence as the basis
of analysis. The potential for progress, however, is real, as shown in this book. It
depends on intensified research, but as in medicine, refinements are available now, and
others clearly are possible.
The completion of this report required not only the tireless efforts of the
committee, but also the patience and persistence of a diverse group of other scholars
who contributed to the symposium, prepared papers for the report, and responded to the
flow of questions that emerged as the report progressed. Dr. David Policansky and Dr.
Robert Smythe of the NRC staff had the awkward duty of reconciling often opposing views
of earnest scholars unaccustomed to compromise with an equally adamant chairman. They
carried the burden masterfully and graciously, aided throughout by the skill of Norman
Grossblatt, editor for the Commission on Life Sciences. To all I offer thanks.
George M. Woodwell, Chairman
Committee on Biologic Markers of
Air-Pollution Damage in Forests
· · ~
vail
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Contents
PART I: THE COMMITTEE'S REPORT
Executive Summarv
Introduction
Using Markers in Combination
The Wnrkshon
7
···························
··························· ~
·························· 9
Introductory Papers ...................
Regional Applications of Markers ..........
Physiologic, Morphologic, and Ecologic Markers
Biochemical, Cellular, and Tissue-Level Markers
Establishing Cause-and-Effect Relationships .............
Using Markers in Surveys and Experimental Studies
Surveys of Stress and Damage
Controlled-Exposure Studies ..........................
Experiments to Determine Mechanism
Developing a Diagnostic Approach
A Strategy for Using Biologic Markers of Stress in Forests
Conclusions and Recommendations
Conclusions ·~
Recommendations
References
11
15
15
16
17
17
17
.
1X
22
22
23
25
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PART II: THE WORKSHOP PAPERS
Introductory Session
Air-Pollutant Distribution and Trends, by R.B.Husar
Elevational Gradients/Local Chemistry, by V.A. Mohnen
Large-Scale Monitoring, byJ.F: Rwrnr~rr]
Use of Biomarkers to Monitor Forest Damage in Europe,
byJ.N.Cape .................................................
Bioindicators in Air Pollution Research--Applications
and Constraints, by D.T.Tingey
New and Emerging Technologies, byP.J.H.Sharpe
and R.D.Spence
Forest Applications of Biologic Markers: Regional Session
Decline of Red Spruce in the Northern Appalachians: Determining
if Air Pollution is an Imnortant FActor. he A. H Johnson
Forest Applications of Biomarkers in Southeastern Forests,
by R.L.Anderson en eeeeeeeeeeeaeeeeeeeeeae~~eeeee~~e
29
47
57
63
73
81
91
105
Biomarkers for Defining Air Pollution Effects in Western Coniferous
Forests, by P.R. Miller 1 1 1
Symptoms as Bioindicators of Decline in European Forests,
by P. Schutt ~ eee
Tree-Stand/Ecosystem Session
Resource Allocation in Trees and Ecosystems, by R. He Waring
Markers of Air Pollution in Forests: Nutrient Cycling,
by De W. Johnson, He Van Miegroet, and W. T. Swank
119
127
133
Human Perturbation of C, N. and S Biogeochemical Cycles:
Historical Studies with Stable Isotopes, by B.Fry 143
Tree-Ring Analysis as an Aid to Evaluating the Effects of Air
Pollution on Tree Growth, by E.Cook and J.Innes 157
Evaluation of Root-Growth and Functioning of Trees Exposed
to Air Pollutants, by J. H. Richards ................................
The Use of Remote Sensing for the Study of Air Pollution
Effects in Forests, by B. N. Rock, J. E. Vogelmann, and
N. J.Defeo ..................................................
x
169
183
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Indigenous and Cultivated Plants as Bioindicators,
by L. H. Weinstein anal J. A. Laurence ....
Experiments and Observations on Epiphytic Lichens as Early
Warning Sentinels of Forest Decline, by M. G. Scott and
T. C. Hutchinson ..............
Fungal and Bacterial Symbioses as Potential Biological Markers
of Effects of Atmospheric Deposition on Forest Health,
by D. H. Marx and S. R. Shafer
Microbial and Rhizosphere Markers of Air Pollution Induced Stress,
by R. K.Antibus and A. E. Linkins, III
Biochemical/Cell-Tissue Session
Foliar Nitrate Reductase: a Marker for Assimilation of
Atmospheric Nitrogen Oxides, by R. J. Norby .....
Free-Radical Mediated Processes as Markers of Air Pollution
Stress in Trees, by C. J. Richardson, R. T. DiGiulio, and
N. J.Tandy ..................................................
Biochemical Indicators of Air Pollution Effects in Trees:
Unambiguous Signals Based on Secondary Metabolites and Nitrogen
in Fast-Growing Species? by C. G. Jones and J. S. Coleman .......
Metals in Roots, Stem, and Foliage of Forest Trees,
by WC. Shortle ......................
The Potential of Trees to Record Aluminum Mobilization and
Changes in Alkaline Earth Availability, by D. A. BondFietti,
C. F. Baes, III, and S. B. McLaughlin
Carbon Allocation Processes as Indicators of Pollutant Impacts
on Forest Trees, by S. B. McLaughlin . .
Photosynthesis and Transpiration Measurements as Biomarkers
of Air Pollution Effects on Forests, by W.E.Winner ..
Nutrient-Use Efficiency as an Indicator of Stress Effects
in Forest Trees, by R. J. Luxmoore .....................
Leaf Cuticles as Potential Markers of Air Pollutant
Exposure in Trees, by V.S. Berg
Air Pollutant-Low Temperature Interactions in Trees,
by R. G. Alscher, J. R. Cumming, and J. Fincher .
········· —
Alteration of Chlorophyll in Plants upon Air Pollutant Exposure,
by R. L. Heath .........................................
Co-occurring Stress: Drought, by M.Tyree
X1
251
261
275
281
.. 293
... 303
... 317
... 341
347
357
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Part i:
The Committee's Report
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