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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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